Since I last wrote in this column (Octber 2003), much has appeared in the scientific literature. As you can see by the several pages of references below, many of these would be worthy of further description. However, in this month’s column I would like to briefly review a paper that appeared back in 2001. This will then be followed with a more recent publication by the same authors that carries through on the same theme, mainly the effects of water flow on the ability of coral to withstand and recover from coral bleaching brought on by high light and high water temperature.
During the coral bleaching of 1998 that affected large portions of the western Pacific from Palau up to Okinawa, Japan, many observers noted the patchy distribution of the event. It was observed that the same species of coral would bleach on one reef but not on an adjacent reef. In Palau, it was noted that corals in channels with high water flow exhibited far less bleaching than in areas with lower flow rates (Delbeek, pers. obs. 1999). In recent years, there has been a push by some authors in the aquarium hobby to advocate running reef aquariums at higher temperatures. One of the pieces of evidence used to justify these levels was the occurrence of corals on reef flat areas that get quite warm and receive a lot of light, which appear to do survive just fine. What was missing from this example, however, was water flow; these areas may have been subjected to strong tidal flows or ocean surges. The following two articles support the observation that good water flow is an essential component in a successful reef aquarium that houses a lot SPS corals such as Acropora and may help to prevent coral bleaching brought on by increased water temperatures and light levels.
Nakamura, T. and R. van Woesik. 2001. Water-flow rates and passive diffusion partially explain differential survival of corals during the 1998 bleaching event. Marine Ecology Progressive Series 212:301-304.
In this study, several fragments of Acropora digitifera were collected in southern Japan from an area that had a high average flow rate and had resisted the coral bleaching event of 1998. Keep in mind that these corals had already survived one bleaching event and may represent corals with a strain of zooxanthellae better adapted to high temperatures.
The fragments were placed in small flumes in an outdoor tank of running seawater. All of these fragments were submitted to 95% natural PAR levels and varying temperatures. Those fragments subjected to flow rates of 50-70 cm/s (created by Rei-Sea powerheads) and natural temperatures ranging from 26.22 oC (79 oF) to 33.65 oC (93 oF) exhibited no bleaching over a two week period, however, those subjected to those same temperatures but with <3 cm/s water flow exhibited 100% bleaching within 8 days. In the control group, where temperatures ranged from 26.64 oC (80 oF) to 29.74 oC (86 oF), no bleaching appeared after two weeks under either flow regime and under the same light level. It was hypothesized that the reason for this had to do with mass transfer rates. The mass transfer (the diffusion of substances across a boundary layer, in this case the cell membrane) of gases and metabolites is required for organisms to survive, especially when submerged, as are marine organisms. This mass transfer must occur across a boundary layer made up of still water that surrounds every surface underwater. Water flowing across marine organisms causes forces to act upon this boundary layer. As a result, organisms in low-flow environments tend to have thicker boundary layers than organisms in high-flow environments. The thinner the boundary layer, the easier it is for diffusion to take place. One of the theories of coral bleaching states that coral bleaching begins when CO2 fixation under high temperature and irradiance begins to break down and toxic oxygen radicals and their derivatives begin to accumulate in the zooxanthellae. This leads to damaged pigments and proteins that results in to the inactivation of photosynthesis and brings about bleaching. The removal of these derivatives by diffusion before they can cause damage could be the result of high water flows that compress the boundary layer, enhance diffusion rates, and hence, mass transfer rates.
Nakamura, T., Yamasaki, H. and R. vanWoesik. 2003. Water flow facilitates recovery from bleaching in the coral Stylophora pistillata. Marine Ecology Progressive Series 256:287-292.
During the summer of 2002 the authors collected and prepared several fragments of Stylophora pistillata from the Ryukyu Islands, Japan. These fragments were kept for four months at low flow conditions (< 3 cm/s) and low PAR (< 300 μmol/m2/s). To induce bleaching small segments of each fragment were subjected to PAR levels of 1500 μmol/m2/s for six hours using fiber optics attached to a 150 W lamp. The temperature was maintained at 27 oC (81 oF). After bleaching occurred, three samples were immediately frozen and then analyzed for chlorophyll a and c2 concentrations and zooxanthellae numbers were counted and recorded as week 0. The rest of the samples (along with unbleached controls) were placed into the same type of flumes as the previous paper and subjected to two different flow rates (<3 cm/s and 20 cm/s). Samples were then taken at weeks 5, 6 and 7, and measurements were made as in week 0. Note: this study only examined the effects of increased light NOT temperature increases.
All the treated fragments showed bleaching within 6 hours. Measurements at week 0 showed no decrease in chlorophyll concentrations per zooxanthellae therefore the bleaching observed was due to loss of zooxanthellae not loss of pigment. The number of zooxanthellae did not begin to increase until week 3 and only did so in the high flow colonies. The control colonies also showed significant differences in zooxanthellae concentration with low flow control colonies supporting fewer numbers. Chlorophyll concentrations in high flow colonies regained 70% of that found in control colonies after 7 weeks but the low flow colonies remained pale.
Total chlorophyll a concentrations increased throughout the course of the study in the high flow colonies and were significantly higher than in low flow colonies. There was, however, no significant difference in chlorophyll c2 concentration between low and high flow colonies over the course of the study though there was a slight increase in high flow colonies in the last two weeks.
The concentration of chlorophyll a per zooxanthellae increased in the high flow colonies in the first 3 weeks then gradually declined, while the low flow colonies showed a steady decline from week 0 to 7. There was a gradual decrease in chlorophyll c2 concentration per zooxanthellae in both flow treatments.
The above results suggest that coral in the high water flows recover more quickly from light induced bleaching by first photo acclimating to high light by increasing chlorophyll a concentration and then by increasing zooxanthellae number. As the number of zooxanthellae increases, shading of algal cells begins and so the zooxanthellae begin to show a decrease in chlorophyll content to photoacclimate to the lower light caused by the shading. The drop in chlorophyll c2 concentration has also been observed in other studies of coral bleaching and appears to be a reaction to high light levels. In this case, the zooxanthellae that began to populate the bleached areas were thought to come from adjacent, unbleached areas as opposed to the reproduction of remnant zooxanthellae in the damaged tissue.
The results of these two studies point to the possibility that the ability to withstand and recover from coral bleaching brought on by high light and/or high water temperatures involves processes that are driven by mass-transfer- limited processes, since strong water flow directly affects the rate of mass- transfer. For the aquarist the implications of these studies is clear, moderate to strong water motion can be a valuable tool in preventing bleaching in their systems due to higher light levels and/or water temperatures. Indeed, as the second study shows, increased water flow can also lead to a more rapid recovery from light induced bleaching, and most likely temperature induced bleaching as well.
There are several studies in the hobbyist literature that have attempted to look at water flow in home aquaria, the clear result of these studies was that many of the tanks examined have water flows closer to lagoon environments than outer reef areas (see Riddle, 1996 and Harker 1998). To be sure, the advent of more efficient water motion devices over the last 5 years probably means that it is time for another evaluation of water motion in home aquaria.
Using the information from the previous two articles there a few recommendations that hobbyists can take away that will help prevent or deal with coral bleaching. Keep in mind that the above studies only dealt with one SPS coral, so it is most likely that SPS corals would benefit the most from the following suggestions:
- When changing lights or when moving from one lighting scheme to a much brighter one, increase the water flow in your aquarium;
- Increase the water flow when you expect temperature increases such as during the warmer months of the year or if you like to mimic nature and increase water temperatures during certain months;
- Increase water flow if your cooling system fails and;
- Increase water flow if introducing new specimens from dimmer aquaria or place these in areas with greater water flow.
As a final comment I would just like to remind everyone that benefits of increased water flow are not limited to just protection or recovery from coral bleaching but also benefits corals by increasing photosynthesis rates, growth/calcification, phosphate uptake and the generation of UV protectant compounds. Therefore, water flow remains one of the critical aspects of reef aquarium husbandry and should always be a major consideration whenever designing a new system.
- Harker, R. 1998. Measuring turbulent flow in reef tanks. Advanced Aquarist Online, http://www.animalnetwork.com/fish2/aqfm/1998/aug/features/1/default.asp.
- Riddle, D. 1996. Water motion in the reef aquarium. Aquarium Frontiers 3(4):32-39.
Interesting Citations from the Periodical Literature
The following are citations for some of the articles that might also be of interest to aquarists, which were published in the summer and fall of 2003.
- Davy, S.K. and J.R. Turner. 2003. Early development and acquisition of zooxanthellae in the temperate symbiotic sea anemone Anthopleura ballii (Cocks). Biological Bulletin 205(1):66-72.
- Mobley, K.B. and D.F. Gleason. 2003. The effect of light and heterotrophy on carotenoid concentrations in the Caribbean anemone Aiptasia pallida (Verrill). Marine Biology 43(3):629-638.
- Domingues, P., Poirer, R., Dickel, L., Almansa, E., Sykes, A. and J.P. Andrade. 2003. Effect of culture density and live prey on growth and survival of juvenile cuttlefish, Sepia officinalis. Aquaculture International 11(3):225-242.
- Koueta, N. and E. Boucard-Camon. 2003. Combined effects of photoperiod and feeding frequency on survival and growth of juvenile cuttlefish Sepia officinalis L. in experimental rearing. Journal of Experimental Marine Biology and Ecology 296(2):215-226.
- Barnes, D.J., Taylor, R.B. and J.M. Laugh. 2003. Measurement of luminescence in coral skeletons. Journal of Experimental Marine Biology and Ecology 295(1):91-106.
- Benyahu, Y., Yosief, T. and M.H. Schleyer. 2003. Soft corals (Octocorallia, Alcyonacea) in the southern Red Sea. Israel Journal of Zoology 48(4):273-284.
- Coma, R., Atkinson, M.J. and R.A. Kinzie. 2003. Particle removal by coral reef communities: picoplankton is a major source of nitrogen. Marine Ecology Progressive Series 257:12-24.
- Connolly, S.R., Bellwood, D.R. and T.P. Huges. 2003. Indo-Pacific biodiversity of coral reefs: Deviations from a mid-domain model. Ecology 84(8):2178-2190.
- Cruz-Pinon, G., Carricant-Ganivet, J.P. and J. Espinoza-Aralos. 2003. Monthly skeletal extension rates in the hermatypic corals Montastraea annularis and M. faveolata: biological and environmental controls. Marine Biology 43(3):491-500.
- Diamond, A. 2003. Identification and assessment of Scleractinians at Tarou Point, Dominica, West Indies. Coastal Management 31(4):404-422.
- Ferrier-Pages, C., Witting, J., Tanbutte, E. and K.P. Sebens. 2003. Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22(3):229-240.
- Gagan, M.K., McCulloch, M.T., Chappell, J. and W.S. Hantoro. 2003. Coral reef death during the 1997 Indian Ocean dipole linked to Indonesia wildfires. Science 301(5635):952-954.
- Gardner, T.A., Cote, I.M., Gill, J.A., Grant, A. and A.P. Watkinson. 2003. Long-term region-wide declines in Caribbean corals. Science 301(5635):958-960.
- Harii, S. and H. Kayomme. 2003. Larval dispersal recruitment and adult distribution of the brooding stony octocoral Heliopora coerulea on Ishigaki Island, southwestern Japan. Coral Reefs 22(2):185-196.
- Houlbreque, F., Tanbutte, E. and C. Ferrier-Pages. 2003. Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata. Journal of Experimental Marine Biology and Ecology 296(2):145-166.
- Huges, T.F., Baird, A.H., Bellwood, D.R., Card, M., Connolly, S.R., Folke, C., Grosberg, R., Hoegh-Guldberg, O., Jackson, J.B.C., Klepas, J. et al. 2003. Climate change, human impacts and the resilience of coral reefs. Science 301(5635):929-933.
- Jimenez, C. and J. Cortez. 2003. Growth of seven species of scleractinian corals in an upwelling environment of the eastern Pacific (Golfo de Papagnyo, Costa Rica). Bulletin of Marine Science 72(1):187-198.
- Kerswell, A.P. anmd R. J. Jones. 2003. Effects of hypo-osmosis on the coral Stylophora pistillata: nature and causes of ‘low-salinity bleaching’. Marine Ecology Progress Series 253:145-154.
- Lindahl, U. 2003. Coral reef rehabilitation through transplantation of a staghorn coral: effect of artificial stabilization and mechanical damages. Coral Reefs 22(3):217-223.
- McClanahan, T.R. and J. Maiha. 2003. Response of coral assemblages to the interaction between natural temperature variations and rare warm-water events. Ecosystems 6(6):551-563.
- Miller, K. and C. Mundy. 2003. Rapid settlement in broadcast spawning corals: implications for larval dispersal. Coral Reefs 22(2):99-106.
- Oku, H., Yamashiro, H. and K. Onaga. 2003. Lipid biosynthesis from [C-14]-glucose in the coral Montipora digitata. Fisheries Science: 625-631.
- Pandolfis, J.M. et al. 2003. Global trajectories of the long term decline or coral reef ecosystems. Science 301(5635):955-957.
- Perrin, C. 2003. Compositional heterogeneity and microstructural diversity of coral skeletons: implications for taxonomy and control of early diagenesis. Coral Reefs 22(2):109-120.
- Santos, S.R., Gutierrez_Rodrigues, C., Lasker, H.R. and M.A. Coffroth. 2003. Symbiodinium sp. associations with the gorgonian Pseudopterogorgia elisabethae in the Bahamas: high levels of genetic variability and population structure in symbiotic dinoflagellates. Marine Biology 143(1):111-120.
- Sely, G.S. 2003. Corals in the genus Porites are susceptible to infection by a larval trematode. Coral Reefs 22(3):216-217.
- Sprechter, S.G., Galle, J. and H. Reichat. 2003. Substrate specificity and juvenile Faviid predominance of coral colonization at the Maldive Islands following the 1998 bleaching event. Coral Reefs 22(2):130-132.
- Steven, A.D.L. and M.J. Atkinson. 2003. Nutrient uptake by coral-reef microatolls. Coral Reefs 22(2):197-?.
- Winters, G., Loya, Y., Rottgers, R. and S. Beer. 2003. Photoinhibition in shallow-water colonies of the coral Stylophora pistillata as measured in situ. Limnology and Oceanography 48(4):1388-1393.
- Wolstenholem, J.K., Wallace, C.C. and C.A. Chen. 2003. Species boundaries within the Acropora humilis group (Cnidaria: Scleractinia): a morphological and molecular interpretation of evolution. Coral Reefs 22(2):155-166.
- Yap, H.T. and R.A. Molina. 2003. Comparison of coral growth and survival under enclosed, semi-natural conditions and in the field. Marine Pollution Bulletin 46(7):858-865.
- Ben-haim, Y., Zicherman-Keren, M. and E. Rosenberg. 2003. Temperature- regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Applied Environmental Microbiology 69(7):4236-4267.
- Borger, J.L. 2003. Three scleractinian coral diseases in Dominica, West Indies: Distributive infection patterns and contribution to coral tissue mortality. Revista de Biologia Tropical 51(4):25-38.
- Banaazak, A.T., Ayorla-Schiaffino, B.N., Rodriguez-Roman, A., Enriquez, J. and R. Eglesias-Preito. 2003. Response of Millepora alcicornis (Milleporina: Milleporidae) to two bleaching events in Puerto Marlos Reef, Mexican Caribbean. Revista de Biologia Tropical 51(4):57-66.
- Croquer, A., Paulis, S.M. anmd A.L. Zubillaga. 2003. White plague disease outbreak in a coral reef at Los Roques National Park, Venezuela. Revista de Biologia Tropical 51(4):39-46.
- McGrath, T.A. and G.W. Smith. 2003. Comparison of the 1995 and 1998 coral bleaching events on the patch reefs of San Salvador Islands, Bahamas. Revista de Biologia Tropical 51(4):67-76.
- Miller, J., Rogers, C. and R. Waaren. 2003. Monitoring the coral disease, plague type II, on coral reefs in St. John, US Virgin Islands. Revista de Biologia Tropical 51(4):47-56.
- Sheppard, C.R.C. 2003. Predicted recurrences of mass coral mortality in the Indian Ocean. Nature 425(6915):294-296.
- West, J.M. an R.V. Salm. 2003. Resistance and resilience to coral bleaching: Implications for coral reef conservation and management. Conservation Biology 17(4):956-975.
- Canler, J.P., Perret, J.M., Lengrand, F. and A. Iwema. 2003. Nitrification in biofilters under variable load and low temperature. Water Science and Technology 47(11):129-136.
- Ebeling, J.M., Sibrell, R.L., Ogden, S.R. and S.T. Summerfelt. 2003. Evaluation of chemical coagulation-flocculation aids for the removal of suspended solids and phosphorus from intensive recirculating aquaculture effluent discharge. Aquacultural Engineering 29(1-2): 23-42.
- Gelfand, I., Barak, Y., Even-Chen, Z., Cytryn, E., van Rijn, J., Kram, M.D. and A. Neori. 2003. A novel discharge intensive seawater recirculating system for the culture of marine fish. Journal of the World Aquaculture Society 34(3):344-358.
- Katsogiannis, A.N., Kornares, M. and G. Lyberatos. 2003. Enhanced nitrogen removal in SBRs by passing nitrate generation accomplished by multiple aerobic/anoxic phase pairs. Water Science and Technology 47(11):53-60.
- Kim, J.S., Hwang, Y.W., Kim, G.G. and J.H. Bae. 2003. Nitrification and denitrification using a single biofilter packed with granular sulfur. Water Science and Technology 47(11):153-156.
- Laeko, N., Drysdale, G.D. and F. Bux. 2003. Anoxic phosphorus removal by denitrifying heterotrophic bacteria. Water Science and Technology 47(11):17-22.
- MacKinnon, I.D.R., Bau, K., Miller, E., Hunter, S. and T. Pimei. 2003. Nutrient removal from wastewater using high performance materials. Water Science and Technology 47(11):101-108.
- Rasheed, M., Badran, M.I. and M. Huethel. 2003. Particulate matter filtration and seasonal nutrient dynamics in permeable carbonate and silicate sands of the Gulf of Aqaba, Red Sea. Coral Reefs 22(2):167-177.
- Shoji, Satoh, H. and T. Mino. 2003. Quantitative estimation of the role of denitrifying phosphate accumulating organisms in nutrient removal. Water Science and Technology 47(11):23-30.
- Summerfelt, J.T. 2003. Ozonation and U.V. irradiation- an introduction and examples of current applications. Aquacultural Engineering 28(1-2):21-36.
- Asoh, K. 2003. Reproductive parameters of female Hawaiian damselfish Dascyllus albisella with comparison to other tropical and subtropical damselfishes. Marine Biology 43(3):803-810.
- Buston, P.M. 2003. Mortality is associated with social rank in the clown anemonefish ( Amphiprion percula ). Marine Biology 43(3):811-816.
- Carlson, J.K. and G.R. Parsons. 2003. Respiratory and haematological responses of the bonnethead shark, Sphryna tiburon to acute changes in dissolved oxygen. Journal of Experimental Marine Biology and Ecology 294(1):15-26.
- Kendrick, A.J. and G.A. Hyndes. 2003. Patterns in the abundance and size- distribution of syngnathid fishes among habitats in a seagrass-dominated marine environment. Estuarine, Coastal and Shelf Science 57(4):631-640.
- Losey, G.S. 2003. Crypsis and communication functions of UV-visible coloration in two coral reef damselfish, Dascyllus aruanus and D. reticulatus. Animal Behaviour 66:299-308.
- Losey, G.S., McFarland, W.N., Loew, E.R., Zamzaw, J.P., Nelson, P.A. and N.J. Marshall. 2003. Visual biology of Hawaiian coral reef fishes. I. Ocular transmission and visual pigments. Copeia 3:433-454.
- Marshall, N.J., Jennings, K., McFarland, W.N., Loew, E.R. and G.S. Losey.
- Visual biology of Hawaiian coral reef fishes. II. Colors of Hawaiian coral reef fishes. Copeia 3:455-466.
- Marshall, N.J., Jennings, K., McFarland, W.N., Loew, E.R. and G.S. Losey.
- Visual biology of Hawaiian coral reef fishes. III. Environmental light and an integrated approach to the ecology of reef fish vision. Copeia 3:467-480.
- Oshitani, S., Nakano, S. and S. Tanaka. 2003. Age and growth of the silky shark Carcharinus falciformis from the Pacific Ocean. Fisheries Science: 456-464.
- Takamoto, G., Seki, S., Nakashima, Y., Karino, K and T. Kuwamura. 2003. Protogynous sex change in a haremic triggerfish Sufflamen chrysopterus (Tetradontiformes). Ichthyological Research 50(3):281-283.
- Westera, M., Lavery, P. and G. Hyndes. 2003. Differences in recreationally targeted fishes between protected and fished areas of a coral reef marine park. Journal of Experimental Marine Biology and Ecology 294(2):145-168.
- Whiteman, E.A. and I.M. Cote. 2003. Social monogamy on the cleaning goby Elacatinus evelynae: ecological constraints or net benefit? Animal Behaviour 66:281-292.
- Wilson, A.B., Ahnesjo, I., Vincent, A.C.J. and A. Meyer. 2003. The dynamics of male brooding, mating patterns and sex ratios in pipefishes and seahorses (family Syngnathidae). Evolution 57(6):1374-1386.
- Brandt, L.A. and E.W. Koch. 2003. Periphyton as a UV-B filter on seagrass leaves: a result of different transmittance in the UV-B and PAR ranges. Aquatic Botany 76(4):317-328.
- Gras, A.F., Koch, M.S. and C.J. Maddon. 2003. Phosphorus uptake kinetics of a dominant tropical seagrass Thalassia testudinum. Aquatic Botany 76(4):299-316.
- Lang, T.C., Ang, P.O. and P.K. Wang. 2003. Development of seaweed biomass as a biosorbent for metal ions. Water Science Technology 47(10):49-54.
- Lima, J.V.M., Carvalho, A.F.F.U., Freitas, S.M. and V.M.M. Melo. 2003. Antibacterial activity of extracts of six macroalgae from the northeastern coast of Brazil. Brazilian Journal of Microbiology 33(4):311-313.
- Miller, M.W., Aronson, R.B. and T.J.T. Murdoch. 2003. Monitoring coral reef macroalgae: Different pictures from different methods. Bulletin of Marine Science 72(1):199-206.
- Rollon, R.N., Van Steveninck, E.D.D. and W. van Vierssen. 2003. Spatio- temporal variation in sexual reproduction of the tropical seagrass Enhalus acoroides L.F. Boyle in Caper Bolinao, N.W. Philippines. Aquatic Botany 76(4):339-?.
- Seraty, J.E., Fannce, C.H. and J.J. Lorenz. 2003. Mangrove shoreline fishes of Biscayne Bay, FL. Bulletin of Marine Science 72(1):161-180.
- Silva, J. and R. Santos. 2003. Daily variation patterns in seagrass photosynthesis along a vertical gradient. Marine Ecology Progressive Series 256:37-44.
- Assavaaree, M., Hagiwara, A., Kogane, T. and M. Arimoto. 2003. Effect of temperature on resting egg formation of the tropical SS-type rotifer Brachionus rotundiformis Tschugunoff. Fisheries Science: 520-528.
- Baldwin, A.P. and R.T. Bauer. 2003. Growth, survivorship, life-span, and sex change in the hermaphroditic shrimp Lysmata wurdemanni (Decapoda: Caridea: Hippolytidae). Marine Biology 143(1):157-166.
- Dom, H.G. and R.M. Lopes. 2003. Omnivory in the calanoid copepod Temora longicornis: feeding, egg production and egg hatching rates. Journal of Experimental Marine Biology and Ecology 292(2):119-138.
- Hotos, G.N. 2003. Growth, filtration and ingestion rare of the rotifer Brachionus plicatilis fed with large ( Astermonas gracilis ) and small ( Chlorella sp.) celled algal species. Aquaculture Research 34(10):793-802.
- Meekon, M.G., Carleton, J.H., McKinnon, A.D., Flynn, K. and M. Funas. 2003. What determines the growth of tropical reef fish larvae in the plankton: Food or temperature? Marine Ecology Progressive Series 256:193-204.
- Woods, C.M.C. and F. Valentine. 2003. Frozen mysis as an alternative to live Artemia in culturing seahorses Hippocampus abdominalis. Aquaculture Research 34(9):757-764.
- Eiler, A., Langenheder, S., Bertilsson, S. and L.J. Tranvik. 2003. Heterotrophic bacterial growth efficiency and community structure at different natural organic carbon concentrations. Applied Environmental Microbiology 69(7):3701-3738.
- Nielsen, T. and F.O. Anderson. 2003. Phosphorous dynamics during decomposition of mangrove ( Rhizophora apiculata ) leaves in sediments. Journal of Experimental Marine Biology and Ecology 293(1):73-88.
- Reidel, G.F. and J.G. Sanders. 2003. The interrelationships among trace element cycling, nutrient loading, and system complexity in estuaries: A mesocosm study. Estuaries 26(2A):339-351.