Salinity Reduction from Freshwater Canal Discharge: Effects on Mortality and Feeding of an Urchin (Lytechinus Variegatus) and a Gastropod (Lithopoma Tectum)

BULLETIN OF MARINE SCIENCE, 61(3): 869–879, 1997

SALINITY REDUCTION FROM FRESHWATER CANAL DISCHARGE: EFFECTS ON MORTALITY AND FEEDING OF AN URCHIN (LYTECHINUS VARIEGATUS) AND A GASTROPOD (LITHOPOMA TECTUM)

E. Irlandi, S. Maciá and J. Serafy

ABSTRACT We conducted laboratory experiments to study the effects of rapid salinity fluctuation associated with freshwater canal discharge on survivorship and grazing rates of two common herbivores in South Florida seagrass beds, Lytechinus variegatus (Echinodermata) and Lithopoma tectum (Gastropoda). Urchins suffered 100% mortality when subjected to a short-term change in salinity from 36 to 2 to 36‰, a salinity change characteristic of a major canal discharge event. Gastropod survivorship, however, was unaffected by short- term exposure to reduced salinity. Urchins and gastropods both survived exposure to a less severe oscillation in salinity (from 36 to 18 to 36‰). Grazing rates of urchins and snails were affected by the 50% drop in salinity, but the effects were different for each group. Urchins demonstrated decreased grazing while gastropods increased their con- sumption of algae after exposure to reduced-salinity water. Our results suggest that water management strategies can significantly influence field distributions and feeding of invertebrate grazers in South Florida seagrass beds and other areas where freshwater runoff is controlled by canal locks.

In South Florida and other coastal regions, man-made canals drain low-lying lands for agricultural development and for flood control in urban areas (Fig. 1). The canals redirect natural surface flow and periodically release freshwater into coastal bays and sounds. Large volumes of water that are discharged when the flood gates are opened can drasti- cally change salinity at the mouths of canals over very short time intervals with salinities fluctuating from full seawater to full freshwater and back up again within a matter of a few hours (Fig. 2) (Fatt, 1986; Wang and Cofer-Shabica, 1988; Cofer-Shabica and Wang, 1990). The drop in salinity is less severe with increasing distance from the canal mouth, and reductions in ambient salinity can be experienced beyond the immediate vicinity of freshwater discharge. Depending on the hydrodynamics of the area, plumes of low salinity water drift from discharge sites and potentially influence plant and animal populations that are distant from canal mouths (Wang and Cofer-Shabica, 1988; Cofer-Shabica and Wang, 1990). Marine animals respond to reduced salinity stress in a variety of ways. Motile animals may move out of an area when salinities are reduced (Perez, 1969; Moser and Gerry, 1989; Jury et al., 1994; 1995), but sessile and slow-moving invertebrates are at the mercy of the changes in salinity occurring in the surrounding water column. Many mollusks tightly close their operculum to limit short-term exposure to sub-optimal conditions (Dav- enport, 1982). Some mollusks also have the capacity for ion regulation (Kinne, 1971) providing limited protection from osmotic stressors. Other invertebrates, including echinoderms, however, have a permeable body wall and poor ion regulating abilities (Drouin et al., 1985) making these animals more susceptible to higher osmotic stress when salinities are altered.

869 870 BULLETIN OF MARINE SCIENCE, 61(3): 869–879, 1997

Figure 1. Map of Biscayne Bay, Florida, and the numerous canals that drain agricultural fields and urbanized areas of its watershed.

The urchin, Lytechinus variegatus, and the gastropod, Lithopoma tectum, are common invertebrate grazers in Biscayne Bay, Florida, USA (Moore et al., 1963; Oliver, 1987; pers. obs.). Based on preliminary data (Irlandi and Maciá, unpubl. data), pers. obs., and records from the Dade County Department of Environmental Resource Management (Dade County, Miami, FL), urchin and gastropod abundance tend to be greater in areas of higher and more stable salinity regimes typical of the eastern side of the bay, but they do occur in IRLANDI ET AL.: CANAL DISCHARGE EFFECTS ON MORTALITY AND FEEDING OF GRAZERS 871

Figure 2: Reproduction of data presented in Wang and Cofer-Shabica (1988) demonstrating salinity fluctuation associated with Mowry Canal in Biscayne Bay, FL. regions where salinities are less than full-strength seawater. Given the overwhelming influence of freshwater discharge from the canal system in south Florida and the hydrodynamics of the region, many areas of Biscayne Bay are subject to salinity fluctuations to some degree (Fatt, 1986; Wang and Cofer-Shabica, 1988; Cofer-Shabica and Wang, 1990), even locations that support healthy populations of both species of invertebrates. The effects of salinity fluctuations on survivorship and feeding behavior of echinoderms and gastropods may have cascading effects on seagrass-dominated ecosystems by altering grazing rates on seagrass-associated primary producers (e.g., seagrass, macroalgae, epiphytes). In this study we conducted laboratory experiments to examine the effects of 872 BULLETIN OF MARINE SCIENCE, 61(3): 869–879, 1997

Figure 3. Schematic representation of one of the four experimental set-ups testing the effects of reduced salinity on urchin and gastropod survival. short-term reduced salinity stress, characteristic of the influence of canal discharge, on survivorship and grazing rates of L. variegatus and L. tectum.

METHODS

SALINITY REDUCTION AND SURVIVAL. — We conducted two salinity stress experiments to examine the effects of freshwater pulses associated with canal discharge on survivorship of L. variegatus. The experiments were carried out in sixteen 18.9-L buckets arranged into groups of four. Each group received water from an additional 18.9-L bucket that served as a mixing chamber (Fig. 3). We collected 16 urchins ranging in test diameter from 40.2 to 71.3 mm in December, 1995, from seagrass beds adjacent to the University of Miami’s Rosenstiel School of Marine and Atmospheric Science. The collection site was dominated by turtle grass (Thalassia testudinum) and was not adjacent to a canal mouth. Urchins were placed individually in each bucket and held in flowing seawater for 5 d prior to use in the experiments. Twice during the 5-d period we fed the urchins a mix of green and decayed leaves of turtle grass. In the first experiment, we exposed half of the urchins (i.e., eight individuals) to a rapid decline in salinity (the other eight served as controls) from ambient levels (36‰) to near freshwater (2‰) and then back to ambient levels to mimic a major canal discharge event. This was achieved by turning off the saltwater flow into two of the mixing buckets and pumping in fresh water that had been aerated for 24 h to remove water treatment chemicals. We measured salinity in each of the buckets every 10 min to quantify changes in salinity. After 50 min, we resumed saltwater flow to the two experimental mixing buckets and continued to record salinity levels in all of the buckets every 10 min for an additional 70 min. Twenty-four hours later, we examined all animals and recorded whether they were alive or dead. We conducted a second salinity stress experiment with a new group of L. variegatus following the same protocol as above, except the salinity was reduced by 50% (reduction from approximately IRLANDI ET AL.: CANAL DISCHARGE EFFECTS ON MORTALITY AND FEEDING OF GRAZERS 873

Figure 4. The average salinity plotted over the duration of the experiments examining the effects of reduced salinity on urchin (a: 100% freshwater dilution, b: 50% freshwater dilution) and gastropod (c: 100% freshwater dilution) survival. The X’s represent plots for control buckets and the filled circles represent treatment buckets. Error bars represent ±1 SE. Lack of an error bar indicates no variation about the recorded mean salinity.

36 to 18 then to 36‰) to mimic a less drastic canal discharge event and/or lesser salinity changes that might result from plumes of freshwater drifting through the bay. In this experiment, we dropped one replicate from the final analysis because detritus was clogging the water line limiting the amount of freshwater delivered to the bucket. Also in December, 1995, we used the same experimental procedure to examine the impact of freshwater discharge from canals on survivorship of the gastropod L. tectum. However, since no mortality was observed with a severe drop in salinity (see results below) we did not subject the snails to a 50% drop in salinity. 874 BULLETIN OF MARINE SCIENCE, 61(3): 869–879, 1997

WF.seitinilasdecuderoterusopxeretfah42sdoportsagdnasnihcrufosetarytilatroM.1elbaT retawhserf=

Stseicep Tndreatmen %Dea Lytechinusvariegatus18000%FW 10 c80ontrol Lytechinusvariegatus5700%FW c80ontrol Lithopomatectum18000%FW c80ontrol

SALINITY REDUCTION AND GRAZING. — In another series of laboratory experiments we tested the effect of a non-lethal 50% reduction in salinity on grazing rates of urchins and snails. In February, 1996, we collected 20 urchins (50.0-68.8 mm test diameter) and placed them in individual 9.5-L plastic buckets filled with seawater and supplied with an air stone. The buckets were placed in a constant temperature water bath (25° C) in a greenhouse. We emptied the water in each bucket and refilled it with new seawater every other day. The urchins were fed Thalassia testudinum leaves and miscellaneous macroalgae (mostly Laurencia poitei, Polysiphonia echinata) for approximately 11 d followed by 48 h with no food. We then exposed the urchins to a short-term 50% drop in salinity by emptying half of the seawater out of all of the buckets. Ten of the buckets were refilled with aerated seawater (control group) while the other 10 were refilled with aerated freshwater (experimental group). We measured salinity in all of the buckets and after approximately 1 h, we emptied each bucket and refilled them all with fresh seawater. We repeated the same procedure on the following day resulting in two consecutive days of 1 h of reduced salinity stress. After the buckets were replenished with fresh seawater on the second day of stressing, we placed 25 ml of algae (P. echinata - 25 ml measured by water displacement in a graduated cylinder) in each bucket. After 24 h we determined the volume of algae left in each bucket. The change in volume of algae was analyzed as the dependent variable in a one-way ANOVA. Cell means for this and all subsequent experiments were tested to confirm homoscedasticity of error variances prior to analyses (F- max, α = 0.05). We did a similar experiment using L. tectum (14.1-17.5 mm, shell height) to determine the effects of a non-lethal 50% drop in salinity on their feeding. For this experiment, eight replicates for each treatment (control and stressed) were used. We used small amounts of algae (Dictyota cervicornis) to feed the snails. It was difficult to accurately measure volume of these small quanti- ties of algae. Instead, we measured initial and final wet weights of the algae added to each bucket. The change in wet weight was calculated and used as the dependent variable in a one-way ANOVA.

RESULTS

SALINITY REDUCTION AND SURVIVAL. — In the first experiment with the urchins, salinity dropped from 36 to ca. 2‰ over a 30-min time interval in all eight of the experimental buckets, and remained at 36 to 37‰ throughout the experiment in the controls (Fig. 4a). Low salinity was maintained in the treatment buckets for an additional 20 min followed by a rapid increase back to ambient levels (36-37‰). After 24 h, 100% of the urchins exposed to the drop in salinity had died while all urchins in the control buckets were alive (Table 1). In the second experiment, we reduced the salinity by almost 50% over a 20 to 30-min time interval (Fig. 4b); both control and experimental urchins survived this 50% drop in salinity (Table 1). L. tectum were also exposed to a similar reduction in salinity from seawater to near freshwater. Salinity dropped from 36 to ca. 2‰ in approximately 30 min and remained IRLANDI ET AL.: CANAL DISCHARGE EFFECTS ON MORTALITY AND FEEDING OF GRAZERS 875

L. tectum

Figure 5. Volume of algae consumed by control and stressed (short-term, 50% reduction in salinity) L. variegatus (a) and wet weight of algae consumed by control and stressed L. tectum (b). Error bars represent ± 1 SE and unlike letters denote a statistical difference between treatments. low for an additional 20 min before the seawater flow was restored and salinity was re- turned to ambient levels (Fig. 4c). All snails survived exposure to freshwater (Table 1). SALINITY REDUCTION AND GRAZING. — For the trials with L. variegatus the average salinity during the freshwater stressing on the first day in the experimental buckets was 17.7‰ (± 0.21 SE) while it was 38.5‰ (± 0.17 SE) in the control buckets. On the second day of 876 BULLETIN OF MARINE SCIENCE, 61(3): 869–879, 1997

freshwater stressing, salinity in the experimental buckets was reduced on average to 18.8 ‰ (± 0.36 SE) while it remained high at 37.6 ‰ (± 0.16 SE) in control buckets. The water temperature in all buckets was between 24.5 and 25.0° C on both days. Twenty four hours after the second freshwater dosing, the control group had consumed significantly more (F(1,18 )= 6.5; P = 0.02) algae than those in the experimental group that had experienced two consecutive days of freshwater pulsing (Fig. 5a). In the trials with L. tectum the salinity in the experimental buckets dropped to 17.9‰ (± 0.40 SE) while it was 36.3‰ (± 0.37 SE) in controls on the first day. On the second day of stressing, experimental buckets averaged 18.8‰ (± 0.25 SE) while controls averaged 37.1 ‰ (± 0.13 SE). The water temperature in all buckets on both days was between 27 and 28° C. The ANOVA on the change in wet weight of algae over the 24-h period

indicated that stressed Lithopoma consumed more algae than non-stressed snails (F(1,14) = 9.9; P = 0.0072) (Fig. 5b).

DISCUSSION

The effect of reduced salinity stress differed between gastropods and urchins. Charac- teristic of other gastropods, adult L. tectum showed limited influence of lowered salinity on survival, while urchins suffered high rates of mortality when subjected to pulses of near-zero salinity water. The degree of tolerance to salinity variation, however, may vary with ontogeny. For example Kinne (1971) found the eggs and larvae of other species of gastropods could not survive low salinities that are tolerated by adults. Early stages of development in urchins are also adversely affected by low salinities. Fertilization of L. variegatus gametes is greatly reduced, larval development is abnormal, and larval meta- morphosis is suppressed at salinities lower than 30‰ (Roller and Stickle, 1993). The narrow range of tolerance by early invertebrate life stages to lowered salinity may directly limit the distribution of L. variegatus and L. tectum in Biscayne Bay to regions distant from canal mouths. In regions where adult populations are established, the influence of freshwater plumes that drift from canal discharge sites appears to be minimal for L. tectum with no effects on survival and increased grazing rates. For urchins, however, our data show that drastic and rapid decreases in salinity are capable of killing adult urchins, and that while less catastrophic changes in salinity do not result in mortality, they do significantly lower grazing rates of urchins on macroalgae. Reductions in grazing rates may be the result of impaired use of tube feet that occurs at sub-optimal salinities (Lawrence, 1975). Grazing is an important process that can influence community composition and ecosystem function in many marine ecosystems. It has been suggested that intense grazing pressures in tropical and subtropical waters may be responsible for limiting algal growth, thus allowing reef-building corals to persist (Potts, 1977; Brock, 1979; Sammarco, 1980; Johannes et al., 1983; Steneck et al., 1988). In temperate waters, various levels of grazing by urchins maintain kelp beds and barren grounds (Ebeling et al., 1985; Harrold and Reed, 1985; Watanabe and Harrold, 1991). L. variegatus and other urchins are signifi- cant grazers in seagrass ecosystems (Camp et al., 1973; Greenway, 1976; Ogden, 1980; Zieman and Zieman, 1989; Valentine and Heck, 1991; Klumpp et al., 1993; Heck and Valentine, 1995). They consume both live and dead seagrass leaves (Montague et al., 1991; Klumpp et al., 1993), and can create barren patches when urchin densities are high IRLANDI ET AL.: CANAL DISCHARGE EFFECTS ON MORTALITY AND FEEDING OF GRAZERS 877

(Camp et al., 1973; Heck and Valentine, 1995). Urchins also consume macroalgae found in seagrass beds (Lowe, 1975; Lowe and Lawrence, 1976; Vadas et al. 1982; Klinger and Lawrence, 1984). Accumulations of drift algae often harbor large numbers of fauna and provide additional structural complexity to seagrass beds (Virnstein and Howard, 1987; Kulczycki et al., 1981; Holmquist, 1994). When algal abundance is high and residence times are long, drift algae can also have deleterious effects on the underlying seagrass (Holmquist, 1992). Differential rates of grazing on algae brought about by periodic pulsing of freshwater can thus directly affect both the fauna and the flora of subtropical seagrass communities. Grazing by gastropods like L. tectum and other micrograzers is important in reducing epiphyte loads on seagrass blades (Howard, 1982; van Montfrans et al., 1982; Orth and van Montfrans, 1984; van Montfrans et al., 1984; Neckles et al., 1993). Epiphyte cover shades the surface of the leaves and has been shown to significantly decrease growth of several species of seagrasses including T. testudinum (Irlandi, unpub. data) and Zostera marina (Orth and van Montfrans, 1984; Williams and Ruckleshaus, 1993; Short et al., 1995; Wright et al., 1995). Our data suggest that grazing of epiphytes by L. tectum may periodically be increased in Biscayne Bay when populations are subjected to pulses of low salinity water. Most previous investigations on the effects of fluctuating salinity on subtidal marine invertebrates have involved tidally-driven salinity changes which are more cyclic and gradual than those associated with canal discharge. Canal discharge can be sudden and the rates of water flow are often as high as 300 cfs in Biscayne Bay (Fatt, 1986). Our data show that water management practices in South Florida can potentially influence species distributions and grazing rates of herbivores; factors that may have cascading effects on seagrass ecosystem function.

ACKNOWLEDGMENTS

Special thanks to B. Orlando, R. Orhun, C. Schmitz, and L. Kaufman for assisting us with animal collection and running the experiments. We are grateful to T. Capo who provided tanks and space for the survival trial. Gratitude is also extended to G. Diaz and C. Rivero for graphics. This work was partially supported by funding from the Army Corps of Engineers/WES, project# DACW39- 94-K-0032, to The University of Miami’s Center for Marine and Environmental Analyses.

LITERATURE CITED

Brock, R. E. 1979. An experimental study on the effects of grazing by parrotfishes and role of refuges in benthic community structure. Mar. Biol. 51: 381-388. Camp, D. K., S. P. Cobb and J. F. Van Breedfield. 1973. Overgrazing of seagrasses by regular urchins, Lytechinus variegatus. BioScience 23:37-38. Cofer-Shabica, S. V. and J. D. Wang. 1990. Freshwater leakage around coastal water control struc- tures, and salinities in Biscayne Bay, Biscayne National Park. National Park Service - South- east Region, Research/Resources Management Report SER-90/02. 67 p. Davenport, J. 1982. Environmental simulation experiments on marine and estuarine animals. Adv. Mar. Biol. 19: 133-256. Drouin, G., J. H. Himmelman and P. Béland. 1985. Impact of tidal salinity fluctuations on echino- derm and mollusc populations. Can. J. Zool. 63: 1377-1387. 878 BULLETIN OF MARINE SCIENCE, 61(3): 869–879, 1997

Ebeling, A. W., D. R. Laur and R. J. Rowley. 1985. Severe storm disturbances and reversal of community structure in a southern California kelp forest. Mar. Biol. 84: 287-294. Fatt, J. C. 1986. Canal impact on Biscayne Bay salinities. M.S. Thesis, University of Miami, Coral Gables, FL. 229 p. Greenway, M. 1976. The grazing of Thalassia testudinum in Kingston Harbour, Jamaica. Aquat. Bot. 2: 117-126. Harrold, C. and D. C. Reed. 1985. Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66: 1160-1169. Heck, K. L. and J. F. Valentine. 1995. Sea urchin herbivory: evidence for long-lasting effects in subtropical seagrass meadows. J. Exp. Mar. Biol. Ecol. 189:205-217. Holmquist, J. G. 1992. Disturbance, dispersal, and patch insularity in a marine benthic assem- blage: influence of mobile habitat on seagrasses and associated fauna. Ph.D. Dissertation. Florida State University, Tallahassee, FL. 183 p. Holmquist, J. G. 1994. Benthic macroalgae as a dispersal mechanism for fauna: Influence of a marine tumbleweed. J. Exp. Mar. Biol. Ecol. 180: 235-251. Howard, R. K. 1982. Impact of feeding activities of epibenthic amphipods on surface-fouling of eelgrass leaves. Aquat. Bot. 14: 91-97. Johannes, R. E., W. J. Wiebe, C. J. Crossland, D. W. Rimmer and S. V. Smith. 1983. Latitudinal limits of coral reef growth. Mar. Ecol. Prog. Ser. 11: 105-111. Jury, S. H., W. H. Howell and W. H. Watson, III. 1995. Lobster movements in response to a hurricane. Mar. Ecol. Prog. Ser. 119: 305-310. ______, M. T. Kinnison, W. Huntting Howell and W. H. Watson, III. 1994. The behavior of lobsters in response to reduced salinity. J. Exp. Mar. Biol. Ecol. 180: 23-37. Kinne, O. 1971. Salinity: animals: invertebrates, Chapter 4.31. Pages 821-995 in O. Kinne, ed. Marine Ecology, Vol. 1, Part 2, Wiley Interscience. 1244 p. Klinger, T. S. and J. M. Lawrence. 1984. Phagostimulation of Lytechinus variegatus (Echinoder- mata: Echinoidea). Mar. Behav. Physiol. 11: 49-67. Klumpp, D. W., J. T. Salita-Espinosa and M. D. Fortes. 1993. Feeding ecology and trophic role of sea urchins in a tropical seagrass community. Aquat. Bot. 45:205-229. Kulczycki, G .R., R. W. Virnstein and W. G. Nelson. 1981. The relationship between fish abundance and algal biomass in a seagrass-drift algae community. Est. Coast. Shelf Sci. 12: 341- 347. Lawrence, J. M. 1975. The effect of temperature-salinity combinations on the functional well- being of adult Lytechinus variegatus (Lamarck) (Echinodermata, Echinoidea). J. Exp. Mar. Biol. Ecol. 18: 271-275. Lowe, E. F. 1975. Absorption efficiencies, feeding rates, and food preferences of Lytechinus variegatus (Echinodermata: Echinoidea) for selected marine plants. M.S. Thesis, University of South Florida, Tampa, FL. 97 p. Lowe, E. F. and J. M. Lawrence. 1976. Absorption efficiencies of Lytechinus variegatus (Lamarck) (Echinodermata: Echinoidea) for selected marine plants. J. Exp. Mar. Biol. Ecol. 21:223-234. Montague, J. R., J. A. Aguinaga, K. L. Ambrisco, D. L. Vassil and W. Collazo. 1991. Laboratory measurement of ingestion rate for the sea urchin Lytechinus variegatus (Lamarck) (Echinoder- mata: Echinoidea). Fla. Sci. 54: 129-134. Moore, H. B., T. Jutare, J. C. Bauer and J. A. Jones. 1963. The biology of Lytechinus variegatus. Bull. Mar. Sci. 13: 23-53. Moser, M. L. and L .R. Gerry. 1989. Differential effects of salinity changes on two estuarine fishes, Leiostomus xanthurus and Micropogonias undulatus. Estuaries 12: 35-41. Neckles, H. A., R. L. Wetzel and R. J. Orth. 1993. Relative effects of nutrient enrichment and grazing in epiphyte-macrophyte (Zostera marina L.) dynamics. Oecologia 93:285-295. Ogden, J. C. 1980. Faunal relationships in Caribbean seagrass beds. Pages 173-198 in R. C. Phillips and C .P. McRoy, eds. Handbook of seagrass biology: an ecosystem perspective. Gar- land, STPM Press, New York. IRLANDI ET AL.: CANAL DISCHARGE EFFECTS ON MORTALITY AND FEEDING OF GRAZERS 879

Oliver, G.D. 1987. Population dynamics of Lytechinus variegatus. M.S. Thesis, University of Miami, Coral Gables, FL. 92 p. Orth, R. J. and J. van Montfrans. 1984. Epiphyte seagrass relationships with an emphasis on the role of micrograzing: A review. Aquat. Bot. 18: 43-69. Perez, K. T. 1969. An orthokinetic response to rates of salinity change in two estuarine fishes. Ecology 50: 454-457. Potts, D. C. 1977. Suppression of coral populations by filamentous algae within damselfish terri- tories. J. Exp. Mar. Biol. Ecol. 28: 207-216. Roller, R. A. and W. B. Stickle. 1993. Effects of temperature and salinity acclimation of adults on larval survival, physiology, and early development of (Lytechinus variegatus Echinodermata: Echinoidea). Mar. Biol. 116: 583-591. Sammarco, P. W. 1980. Diadema and its relationship to coral spat mortality: grazing, competition, and biological disturbance. J. Exp. Mar. Biol. Ecol. 45: 245-272. Short, F. T., D. M. Burdick and J. E. Kaldy, III. 1995. Mesocosm experiments quantify the effects of eutrophication on eelgrass, Zostera marina. Limnol. Oceanogr. 40: 740-749. Steneck, R. S., J. H. Choat, D. Barnes, M. A. Borowitzka, J. C. Coll, P. J. Davies, P. Flood, B. G. Hatcher and D. Hopley. 1988. Herbivory on coral reefs: A synthesis. Proc. 6th Int’l. coral reef symposium, Townsville, Australia, 8-12 August 1988. Plenary addresses and status reviews. Vol. I: 37-49. Vadas, R. L., T. Fenchel and J. C. Ogden. 1982. Ecological studies on the sea urchin Lytechinus variegatus, and the algal-seagrass communities of the Miskito Cays, Nicaragua. Aquat. Bot. 14: 109-125. Valentine, J. F. and K. L. Heck, Jr. 1991. The role of sea urchin grazing in regulating subtropical seagrass meadows: evidence from field manipulations in the northern Gulf of Mexico. J. Exp. Mar. Biol. Ecol. 154: 215-230. van Montfrans, J., R. J. Orth and S. A. Vay. 1982. Preliminary studies of grazing by Bittium varium on eelgrass periphyton. Aquat. Bot. 14: 75-89. ______, R. L. Wetzel and R. J. Orth. 1984. Epiphyte-grazer relationships in seagrass meadows: Consequences for seagrass growth and production. Estuaries 7: 289-309. Virnstein, R. W. and R. K. Howard. 1987. Motile epifauna of marine macrophytes in the Indian River Lagoon, Florida. 2. Comparisons between drift algae and three species of seagrasses. Bull. Mar. Sci. 41: 13-26. Wang, J. D. and S. V. Cofer-Shabica. 1988. The effects of freshwater canal discharges on salinities in Biscayne National Park. Report to the National Park Service. January, 1988. 17 p. Watanabe, J. M. and C. Harrold. 1991. Destructive grazing by sea urchins Strongylocentrotus spp. in central California kelp forest: Potential roles of recruitment, depth, and predation. Mar. Ecol. Prog. Ser. 71: 125-141. Williams, S. L. and M. H. Ruckelshaus. 1993. Effects of nitrogen availability and herbivory on eelgrass (Zostera marina) and epiphytes. Ecology 74: 904-918. Wright, A., T. Bohrer, J. Hauxwell and I. Valiela. 1995. Growth of epiphytes on Zostera marina in estuaries subject to different nutrient loading. Biol. Bull. 189:261. Zieman, J. C. and R. T. Zieman. 1989. The ecology of seagrass meadows of the west coast of Florida: A community profile. U.S. Fish and Wildl. Serv. Biol. Rep. 85(7.25). 155 p.

DATE ACCEPTED: January 16, 1997.

ADDRESS: University of Miami, Rosenstiel School of Marine and Atmospheric Science, Division of Marine Biology and Fisheries, 4600 Rickenbacker Causeway, Miami, Florida 33149-1098.