The Rise of Ruppia in Seagrass Beds: Changes in Coastal Environment and Research Needs

Home , Cymodoceaceae, Halodule, Posidonia, Ruppia, Ruppia maritima, Syringodium

Chapter 12

THE RISE OF RUPPIA IN SEAGRASS BEDS: CHANGES IN COASTAL ENVIRONMENT AND RESEARCH NEEDS

Hyun Jung Cho*1, Patrick Biber*2 and Cristina Nica1 1 Department of Biology; Jackson State University; 1400 Lynch St., Jackson, MS 39217, USA 2 Department of Coastal Sciences; The University of Southern Mississippi; 703 East Beach Drive, Ocean Springs, MS 39564

ABSTRACT

It is well known that the global seagrass beds have been declining due to combining effects of natural/anthropogenic disturbances. Restoration efforts have focused on revegetation of the lost seagrass species, which may well work in cases the seagrass loss is recent and the habitat quality has not been altered substantially. Recent studies in several estuaries in the U.S. report the similar change in the seagrass community structures: much of the habitats previously dominated by stable seagrasses (Thalassia testudinum and Syringodium filiforme in tropical and Zostera marina in temperate regions) are now replaced by Ruppia maritima, an opportunistic, pioneer species that is highly dependent on sexual reproduction. The relative increases of R. maritima in seagrass habitats indicate that: (1) the coastal environmental quality has been altered to be more conducive to this species; (2) the quality of environmental services that seagrass beds play also have been changed; and (3) strategies for seagrass restoration and habitat management need to be adjusted. Unlike Zostera or Thalassia, Ruppia maritima beds are known for their seasonal and annual fluctuations. The authors’ previous and on-going research and restoration efforts as well as literature reviews are presented to discuss the causes for and the potential impacts of this change in seagrass community on the coastal ecosystem and future restoration strategies.

Keywords: seagrass, Ruppia maritima, coastal, estuaries.

* Tele: 601-979-3912; Fax: 601-979-5853; E-mail: [email protected] * Tele: 228 872 4200; Fax 228 872 4204; E-mail: [email protected] 2 Hyun Jung Cho, Patrick Biber and Cristina Nica

CHANGES IN COASTAL ENVIRONMENT AND SEAGRASS BEDS

Located at the land-water interface, coastal areas are affected by both land and ocean processes. In addition, the low-lying coastal areas and estuaries are particularly prone to the environmental modifications resulted from global climate change. Coastal wetlands have been lost at alarming rates in some areas (as high as 100 km2/year in Louisiana) [11] due to numerous factors that include, but not limited to: (1) levee construction along major rivers that isolate the rivers from supplying sediment and nutrients for delta formation and wetland development; (2) subsidence and global warming that attribute to the Relative Sea Level Rise (RSLR), (3) wave energy and storms; (4) saltwater intrusion to freshwater wetlands, and (5) development for human usages. Habitat loss and environmental changes in shallow coastal areas will likely continue with the trend of global warming that accelerates sea level rise, augments the frequency and intensity of extreme weather conditions such as hurricanes and extreme El Niño Southern Oscillation events [40]. Vegetation communities are often the fundamental components and the keystones of the coastal ecosystems [33]. Submerged aquatic vegetation (SAV), a unique group of vascular plants that have adapted to live underwater, ranges from marine seagrasses to freshwater angiosperms. Coastal seagrass beds: are among the most productive ecosystems in the world; perform a number of vital ecological functions in chemical cycling and physical modification of the water column and sediments; and provide food and shelter for commercially and ecologically important organisms [3, 22, 30]. With the environmental changes listed above, seagrass beds have reportedly been declining globally. Examples include: losses of large beds of Zostera spp. (eelgrass) from algal competition, poor water quality, wasting disease, impacts of shellfisheries, air exposure due to sedimentation, light reduction from eutrophication, and prop scars in temperate regions; reductions of the beds of Posidonia spp. due to modifications brought by dredging, shoreline modification and constructions, light limitation from algal growths, competition from introduced species, increased water temperature in Australia and the Mediterranean [43, 21, 19]. In more tropical areas, large beds of Thalassia testudinum (turtlegrass), Halodule wrightii (shoalgrass), and Syringodium filiforme (manateegrass) have been significantly reduced from similar causes [19]. While it is true that global seagrass habitats are declining due to numerous anthropogenic activities that also exacerbate impacts of natural processes, studies have reported expansion of the SAV species, Ruppia maritima L., into the areas that were previously occupied by other seagrass species, especially after disturbances such as hurricanes [7], salinity changes [18, 29] and extreme meteorological events such as El Niño Southern Oscillation [24, 9]. During the 2007 Estuarine Research Federation conference (http://www.erf.org/erf2007/ERF07 Program.pdf) held in Providence, Rhode Island, USA, several presentations on studies conducted in the U.S. estuaries reported the changes in the seagrass community structures: much of the habitats previously dominated by stable seagrasses (T. testudinum and S. filiforme in tropical and Zostera marina in temperate regions) are now replaced by R. maritima, an opportunistic, pioneer SAV species that is highly dependent on sexual reproduction.

The Rise of Ruppia in Seagrass Beds 3

CHARACTERISTICS OF RUPPIA MARITIMA

Wigeongrass, R. maritima, is a euryhaline species that tolerates a wide range of salinities from near-freshwater to hypersaline conditions [31, 29], which is why many scientists do not consider it as a true seagrass species [30]. Because of its sporadic occurrence in low salinity habitats and peripheral/opportunistic growth in marine environments, its importance has been underestimated compared to other seagrass species. However, R. maritima is the most widely distributed cosmopolitan seagrass species occurring in broad latitudinal ranges in both northern and southern hemispheres [44, 42]. Ruppia maritima not only consists of populations that are distributed throughout the salinity zones, but also withstands abrupt salinity pulses [45, 29]. It grows better in nutrient- enriched environments that can be stressful to other seagrasses [4] and has a broader temperature tolerance [31]. Being able to rapidly reproduce sexually and asexually, R. maritima can colonize into a bare habitat, grow, and establish quickly. In ephemeral lagoons or estuarine environments with fluctuating water levels, water movements, and salinity, the plants produce an enormous number of seeds (several thousands to tens of thousands seeds per square meter) [24, 32, 10, 25]. The seeds that are protected by sturdy seed coats can resist harsh conditions such as desiccation [26, 8] or even gut-passages of waterfowl and fish, which also aids in long-distance dispersal of the propagules [1, 15, 6, 14]. It is still controversial among the seagrass experts in predicting how global climate change would affect seagrass habitats. While there is little doubt that the climate change will increase the rates of habitat loss and degradation for seagrass beds, Orth et al. [38] noted that the increases in water temperature and CO2 concentrations, when not linked to their indirect effects, may provide a more favorable environment to tropical seagrass species, but they also warned that the current rates of environmental changes may be too fast for adequate adaptation by the species. Considering the traits of R. maritima, the species’ relative abundance and ecological importance are expected to grow in the global seagrass community with the changing climate and environment [24, 18, 25]. The relative increases of R. maritima in seagrass habitats indicate that: (1) the coastal environmental quality has been altered to be more conducive to this species; (2) the quality of environmental services that seagrass beds play also have been changed; and (3) strategies for seagrass restoration and habitat management need to be adjusted. Compared to Zostera or Thalassia beds, R. maritima dominated beds are known for their seasonal and annual fluctuations [12, 31, 35, 18, 29, 7]. Ruppia-dominated beds also have lower peak biomass and productivity than Thalassia or Zostera beds, which would affect food webs [18]. The fauna that rely on resources in the fluctuating seagrass beds will also increase their exposure to predators due to frequent movements, which will also negatively affect survival and reproduction of the predators, who need to spend more time/energy to find prey.

DO WE NEED TO RESTORE RUPPIA BEDS?

The decline of overall seagrass beds, an essential nursery habitat, directly impacts the marine fishing industry. For example, the economic valuation of the fisheries industry in Mississippi provided by the Center for Fisheries Research and Development at the University 4 Hyun Jung Cho, Patrick Biber and Cristina Nica of Southern Mississippi indicates there are more than 50 species of finfish and shellfish that are commercially harvested in state waters with a market value of $900 million in 2003, and a recreational industry valued conservatively at over $400 million in 2000 [39]. Clearly, loss of habitat would have a disproportionate impact on the socio-economic activities in coastal states. Therefore, restoration of seagrass beds is one of the primary goals in many estuaries [17]. Seagrass restoration often involves transplanting of the species that have been lost, especially for those species with no substantial seed bank and which show slow growth and natural recovery [2]. However, seagrass communities and their habitat quality in the coastal environment have been altered as described above; without preceding restoration of the suitable environmental conditions, the lost seagrass species would not be successfully re- established. Insufficient underwater light due to increased turbidity became the main limiting factor for Thalassia growth in many areas in Mississippi Sound [34]. Several wetland restoration programs conducted in Louisiana and Florida involve artificial diversions of seasonal freshwater flows to the degrading wetlands, which affects salinities and turbidities of brackish marshes and bay areas [18]. The increased turbidity and fluctuating salinities in salt marshes, bayous, and estuarine areas prevent natural recolonization or successful establishment of transplanted Thalassia and Syringodium. Even with the freshwater diversion efforts, salinities of these areas are often too high for freshwater SAV species such as Wildcelery (Vallisneria americana), Pondweeds (Potamogeton spp.), and Southern Naiad (Najas guadalupensis). These transitional areas between the freshwater SAV zones and the remaining true seagrass beds will be increasing and left without persisting SAV if no proper restoration actions are undertaken. Often times, Ruppia maritima is the only SAV species that would successfully survive and thrive in these transitional areas that have recently lost seagrass or brackish SAV, under current habitat conditions [18, 20]. The importance and possibility of using R. maritima, in seagrass restoration in northern Gulf of Mexico to revegetate the areas that have lost the previously persisting vegetation due to the freshwater diversion projects and from the loss of true seagrasses has long been overdue. The main concern for use of R. maritima in seagrass restoration has been its unpredictable growth that haphazardly occurs and disappears. Its growth is often inconsistent and unpredictable when growing with Thalassia or Zostera spp. probably due to competition from the better-adapted resident plants [36], episodic high turbidity and wave energy associated with storms [9], or factors affecting development from seeds (seed bank distribution, dormancy, germination, and seedling growth) [41, 28, 27, 8]. However, revegetation using R. maritima is important because the new beds will help settle down suspended particles and stabilize sediment, despite the fact the growth may be variable sometimes. It must be noted that the ultimate goal of restoration using R. maritima is not to promote Ruppia growth alone, but to maintain the areas from further degradation to support potential colonization of stable species in the future. It is true that Ruppia maritima displays several characteristics of pioneer species [10]. Then a restoration approach that complies with natural succession should be pursued; and more fundamental research on Ruppia maritima seed biology, transplanting methods, and genetics is required to develop successful seagrass restoration methods and strategies.

The Rise of Ruppia in Seagrass Beds 5

CASE STUDY: RUPPIA MARITIMA OF THE MISSISSIPPI COAST, THE USA

Changes in the Seagrass Community

As with the global trend, seagrass beds have been also declined in northern Gulf of Mexico (http://gulfsci.usgs.gov/gom_ims/pdf/pubs_gom.pdf). In Mississippi Sound, T. testudinum, S. filiforme and Halophila engelmannii were commonly found according to surveys conducted in 1970’s [12]. These seagrass beds reportedly declined more than 50 percent between 1969 and 2003 since the 1969 Hurricane Camille [12, 34, 19]. Significant declines occurred in the Thalassia and Syringodium beds, resulting in local extinctions at many locations. Currently, seagrass beds of R. maritima and H. wrightii primarily occur on the protected northern sides of the barrier islands, and some locations along the mainland coast including Grand Bay National Estuarine Research Reserve (Grand Bay NERR).

Changes in the Seagrass Beds after the 2005 Hurricane Katrina at Grand Bay NERR

The Grand Bay National Estuarine Research Reserve (Grand Bay NERR; figure 1) is one of the 27 National Estuarine Research Reserves (NERRs) in the US, located in extreme southeastern Mississippi (http://grandbaynerr.org/aboutus/). As with the other NERRs, Grand Bay NERR participates in monitoring the health of the nation’s estuaries to foster wise stewardship of natural resources. This reserve encompasses terrestrial maritime forests and pine savannas, extensive salt marshes and saltpans, and about 30% of the total reserve area is shallow bays and bayous. In Grand Bay NERR, we have conducted biannual surveys at the seagrass beds of Ruppia and Halodule (figure 2) using fixed transects since 2005 [7]. The coverage and distribution of the beds dominated by R. maritima and the Ruppia – Halodule mixed beds of the tidal bay area (the estuarine area) in the reserve vary substantially primarily due to changes in R. maritima abundance between summer and fall [7] (figure 3). The estuarine Ruppia population that grows in the shallow, high wave energy environment has an annual growth pattern: seedling growth in early spring, rapid vertical growth in April, producing abundant inflorescence and seeds in May and June (figure 4), and senescence in the fall. On the other hand, R. maritima that occurs in the bayous and marsh in the reserve area, where tides and wind-driven wave actions are less severe, rarely flowers and sets seeds [78]. A similar pattern occurs in the Lake Pontchartrain estuarine area, Louisiana: the R. maritima populations growing in brackish marsh, bayous, and streams rarely produce seeds, while the near-by estuarine R. maritima populations significantly depends on sexual reproduction [10].

6 Hyun Jung Cho, Patrick Biber and Cristina Nica

Figure 1. Seagrass survey sites in Grand Bay National Estuarine Research Reserve, Mississippi. The map in the inset indicates the location of the Reserve in the state.

The Rise of Ruppia in Seagrass Beds 7

Figure 2. Patchy seagrass beds of Ruppia maritima and Halodule wrightii at Grand Bay National Estuarine Research Reserve.

Figure 3. Temporal changes in percent SAV coverage (mean proportion of a 200-meter-transect length that is covered by SAV shoots) at the survey sites of Grand Bay National Estuarine Research Reserve. Error bars indicate standard errors.

8 Hyun Jung Cho, Patrick Biber and Cristina Nica

Figure 4. Seeds on Ruppia maritima plants.

The sexually reproducing Ruppia populations are known to be highly resilient to temporary disturbances and seasonal extreme conditions [13, 32, 9]. This was also evidenced in the Ruppia maritima populations of the northern Gulf of Mexico after the 2005 hurricanes: the physical disturbance and sedimentation associated with Hurricanes Katrina (Landfall August 29, 2005) and Rita (Landfall September 24, 2005) had little negative impacts on the seagrass beds in the following year (figure 3) in Grand Bay NERR and also in the Alabama coast [5]. In fact, both R. maritima and H. wrightii were more abundantly growing in 2006, the year after the hurricanes, than any other years (figure 3). The similar case of R. maritima increase the year after the 1998 Hurricane George was also observed in Lake Pontchartrain [9]; and the possible explanations for the increase were the increased salinity and water clarity that occurred during the La Niña-related drought that followed Hurricanes George [9]. Another possible explanation for the notable increase of R. maritima in Lake Pontchartrain in 1999 and in Grand Bay NERR in 2006 is that the storms’ physical disturbance helped expose deep-buried seeds in the seed bank into the oxygenated upper layer. The changed photoperiod and redox potential for the seeds [37] could have been the trigger for Ruppia seed germination in the spring. However, we noted a different effect of the hurricanes on Ruppia maritima in a bayou of the reserve. As mentioned earlier in this chapter, the bayou R. maritima hardly produces seeds. We surveyed Bayou Cumbest prior to Hurricane Katrina in summer of 2005 and found R. maritima to be common, but the beds had been lost since the hurricane until we found small Ruppia patches growing in the bayou in early October 2008. This slow recovery of the non-flowering R. maritima in Bayou Cumbest is probably due to the lack of a viable seed bank and the remoteness from the estuarine source populations.

Ruppia Maritima Restoration Efforts in Bayou Cumbest

In 2008, we have initiated a restoration project to promote Ruppia maritima growth back in Bayou Cumbest. The R. maritima seeds collected from the flowering shoots of the estuarine populations in summer of 2007 and 2008 were germinated in the laboratory (figure 5); and the seedlings were grown in biodegradable mats to promote anchoring of the plants, which were later transplanted into peat pots (figure 6). Seedlings were grown on different The Rise of Ruppia in Seagrass Beds 9 substrates: biodegradable mats, sandy soil in peat pots, or organic rich topsoil in peat pots for a period of 3-6 months prior to field transplanting. Plants were held in 500L outdoor tanks (figure 7) with recirculating and filtered water, salinities were monitored weekly and adjusted with Instant Ocean salt mix as necessary. Salinity was increased to half of anticipated field conditions 1-2 weeks prior to transplanting to allow osmoacclimation and reduce transplant stress. Soil type and transplanting technique were tested at two locations: the Gulf Coast Research Laboratory (GCRL), Ocean Spring, Mississippi and three sites in Bayou Cumbest. The GCRL site was a high energy coastline exposed to the predominant southeasterly winds, while the Bayou Cumbest sites were in sheltered locations; depth was similar at all four sites, ranging from 0.1 to 0.8m depending on tide, with a mean depth of 0.4m. Plants were transferred to the field sites from the tanks in closed plastic containers and kept submerged (within 2 hours). At the field site, transplant units (mats or pots) were placed out in predefined randomly allocated treatment blocks (figure 8) of 12.5cm2. Peat pots were buried to the rim, and sediments filled in to keep the surface level with the surrounding bottom, biodegradable mats were held in place with 15cm long steel staples, and further anchored with a PVC plastic frame that served to outline the six treatment blocks. The PVC frame was anchored in the soft sediments by four 50cm long legs; a small subsurface float aided in relocating the PVC frame and transplanting units. Results obtained to date indicate that the high energy field site at GCRL was not suitable for the plants, and a temporary wave break would need to be placed in front of the transplant site to enable the R. maritima plants to establish. We expect a better result at the low energy sites in Bayou Cumbest where we are monitoring the transplants monthly.

Figure 5. Ruppia maritima seedlings germinated in a laboratory. 10 Hyun Jung Cho, Patrick Biber and Cristina Nica

Figure 6. Peat pots containing seedlings grown in biodegradable mats to promote anchoring of the plants.

Figure 7. Monitoring plants held in 500 L outdoor tanks at Gulf Coast Research Laboratory, Ocean Springs, Mississippi, for grow out until ready to transplant at restoration location. The Rise of Ruppia in Seagrass Beds 11

Figure 8. Layout of transplant blocks to test four different propagation methods (1) seeds in biodegradable mat, (2) seedlings in peat pots, (3) plants collected from Bayou Cumbest and grown in peat pots, (4) natural plants occurring at transplant site.

Further Research Needs

Restoration practices for Ruppia maritima are poorly investigated whereas much more effort has been put into restoration of high salinity seagrass species. It is still not confirmed whether the difference in reproductive/growth strategy between the estuarine and the bayou Ruppia populations truly comes from genetic differences; or from plastic ecotypic adaptations of the same species to the varying habitats. In fact, the scientific name of Ruppia maritima includes “sensu lato”, which means in Latin “in the broad sense”. Transplanted plants have higher chances to survive if the recipient sites have genetically similar populations [16]. Also, genetically diverse seagrass populations had a higher resistance to ecosystem disturbances [23]. Therefore, some of the questions need to be answered for successful Ruppia maritima restoration using laboratory grown seedlings. Can harvested seeds from annual Ruppia populations be used to revegetate areas that have lost perennial populations? How would the Ruppia gene pool of one area be affected by restoration through seeds broadcast from other areas? 12 Hyun Jung Cho, Patrick Biber and Cristina Nica

In order to answer these questions, genetic diversity and gene flow among the isolated populations of R. maritima along the northern Gulf of Mexico need to be investigated. The phylogenetic relationship among the Ruppia populations as well as the genetic diversity of Ruppia within a broad geographical range and across several habitats need to be assessed and compared among the individuals within populations, among populations, among geographic regions, among habitat types, and between reproductive strategies. If the isolated Ruppia populations have a significantly low genetic diversity, seagrass in these areas will have low resistance to natural/anthropogenic disturbances [23]. If the populations with the low genetic diversity primarily depend on vegetative reproduction and do not produce abundant seeds, they will be more vulnerable to environmental changes and perturbation. The future study outcomes on genetic variation across the Ruppia populations will provide critical, but currently lacking information that needs to be considered in seagrass restoration in brackish marsh and estuarine areas.

CONCLUSION

The relative abundance and ecological importance of Ruppia maritima L are expected to grow in the global seagrass community with the changing climate and coastal environment. It is a candidate species for re-vegetation in transitional areas between the freshwater submerged vegetation zones and the remaining true seagrass beds. Development of suitable techniques for transplanting this species is required, due to it’s fragile morphology and lack of substantial below-ground biomass. Genetic diversity and gene flow among the isolated populations of R. maritima also need to be investigated to ensure successful restoration. Nonetheless, Ruppia, once established, will rapidly colonize and expand into bare habitats which would promote natural succession to more stable climax seagrass species such as Thalassia or Zostera that have been declining globally.

ACKNOWLEDGMENTS

The research and restoration projects conducted at Grand Bay National Estuarine Research Reserve, Mississippi, are supported by grants from the NOAA-ECSC (Grant No.NA17AE1626, Subcontract # 27-0629-017 to Jackson State University), Mississippi Department of Marine Resources (Tidelands Project), MS-AL Sea Grant Consortium (Grant Number USM-GR02639/OMNIBUS-R/CEH-29-PD), and NOAA through National Estuarine Research Reserve System. We thank Christopher May, Jonathan Jones, Christina Watters, Melissa Larmer, and Philemon Kirui for their significant role in field surveys.

REFERENCES

[1] Agami, M. & Waisel, Y. (1988). The role of fish in distribution and germination of seeds of the submerged macrophytes Najas marina L. and Ruppia maritima L. Oecologia, 76, 83-88. The Rise of Ruppia in Seagrass Beds 13

[2] Bastyan, G. R. & Cambridge, M. L. (2008). Transplantation as a method for restoring the seagrass Posidonia australis. Estuarine, Coastal and Shelf Science, 79, 289-299. [3] Beck, M. W., Heck, K. L., Able, K. W., Childers, D. L., Eggleston, D. B., Gillanders, B. M., Halpern, B., Hays, C. G., Hoshino, K., Minello, T. J., Orth, R. J., Sheridan, P. F., & Weinstein, M. P. (2001). The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bio-Science, 51, 633–641. [4] Burkholder, J. M., Glasgow, H. B. Jr., & Cooke, J. E. (1994). Comparative effects of water-column nitrate enrichment on eelgrass Zostera marina, shoalgrass Halodule wrightii, and widgeongrass Ruppia maritima. Marine Ecology Progress Series, 105, 121-138. [5] Byron, D. & Heck, K. (2006). Hurricane effects on seagrasses along Alabama’s gulf coast. Estuaries, 29, 939-942. [6] Charalambidou, I., Santamaria, L., & Langevoord, L. (2003). Effect of ingestion by five avian dispersers on the retention time, retrieval and germination of Ruppia maritima seeds. Functional Ecology, 17, 747-753. [7] Cho, H. J. & May, C. (2008). Short-term Spatial Variations in the Beds of Ruppia maritima (Ruppiaceae) and Halodule wrightii (Cymodoceaceae) at Grand Bay National Estuarine Research Reserve, Mississippi, USA. Journal of the Mississippi Academy of Sciences, 53, 2-3. [8] Cho, H. J. & Sanders, Y. L. (in press). Note on Organic Dormancy of Estuarine Ruppia maritima seed. Hydrobiologia. [9] Cho, H. J. & Poirrier, M. A. (2005a). Response of Submersed Aquatic Vegetation (SAV) to the 1997-2001 El Niño Southern Oscillation Shifts in Lake Pontchartrain, Louisiana, Estuaries ,28 (2), 215-225. [10] Cho, H. J. & Poirrier, M. A.(2005b). Seasonal growth and reproduction of Ruppia maritima L. s.l. in Lake Pontchartrain, Louisiana. Aquatic Botany, 81, 37-49. [11] Day, J. W., Boesch, D. F., Clairain, E. J., Kemp, G. P., Laska, S. B., Mitsch, W. J., Orth, K., Mashriqui, H., Reed, H. D., Shabman, L., Simenstad, C. A., Streever, B. J., Twilley, R. R., Watson, C. C., Wells, J. T., & Whigham, D. F. (2007). Restoration of the Mississippi Delta: Lessons from Hurricanes Katrina and Rita. Science, 23,1679 – 1684. [12] Eleuterius, L. N. (1987). Seagrass ecology along the coasts of Alabama, Louisiana, and Mississippi. In: Durako, M. J., Phillips, R. C., Lewis, R. R. 111 (Eds.), Proceedings of Symposium on Subtropical-Tropical Seagrasses Southeastern. [13] Estevez. E. D., Sprinkel, J., & Mattson, R. A. (2002). Responses of Suwannee River tidal SAV to ENSI-controlled climate variability. In H. Greening (ed.), Seagrass Management: It’s Not Just Nutrients! (August 22-24 2000 Symposium Proceedings. Tampa Bay National Estuary Program, 133-144). St. Petersburg, Florida. [14] Figuerola, J. & Green, A. J. (2004). Effects of seed ingestion and herbivory by waterfowl on seedling establishment: a field experiment with wigeongrass Ruppia maritima in Doñana, south-west Spain. Plant Ecology, 173, 33-38. [15] Figuerola, J., Green, A. J., & Santamaria, L. (2002). Comparative dispersal effectiveness of wigeongrass seeds by waterfowl wintering in south-west Spain: quantitative and qualitative aspects. Journal of Ecology, 90, 989-1001. 14 Hyun Jung Cho, Patrick Biber and Cristina Nica

[16] Fonseca, M. S. (1990). Regional analysis of the creating and restoration of seagrass systems. In Kusler, J.A., Kentula, M.E. (Eds.). Wetland Creation and Restoration (171- 193). Island Press, Washington. [17] Fonseca, M., Kenworthy, W., Thayer, G. (1998). Guidelines for the Conservation and Restoration of Seagrasses in the United States and Adjacent Waters. NOAA Coastal Ocean Office, Silver Spring, MD. 222p. [18] Fourqurean, J. W., Boyer, J. N., Durako, M. J., Hefty, L. N., & Peterson, B. J. (2003). Forecasting responses of seagrass distribution to changing water quality using monitoring data. Ecological Applications, 13, 2, 474-489. [19] Green, E. P. & Short, F. T. (2003). World Atlas of Seagrasses. Prepared by the UNEP World Conservation Monitoring Centre. University of California Press, Berkeley. [20] Handley, L., Altsman, L. & DeMay, R. (2006). Seagrass Habitat in the northern Gulf of Mexico. Gulf of Mexico Program Report. http://gulfsci.usgs.gov/gom_ims/ pdf/pubs_gom.pdf. [21] Hemminga, M. A. & Duarte, C. M. (2000). Seagrass Ecology. Cambridge University Press. The Edinburgh Building, Cambridge CB2 8RU, UK. [22] Heck, Jr., Hays, K. L. C., & Orth, R. J. (2003). A critical review of the nursery role hypothesis for seagrass meadows. Marine Ecology Progress Series, 253,123– 136.3.??????????? [23] Hughes, A. R. & Stachowicz, J. J. (2004). Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proceedings of the National Academy of Sciences, 101, 8998-9002. [24] Johnson, M. R., Williams, S. L., Lieberman, C. H. & Kolbak, A. (2003). Changes in the abundance of the seagrasses Zostera marina L. (eelgrass) and Ruppia maritima L. populations in San Diego, California, following an El Niño event. Estuaries, 26,106- 115. [25] Kahn, A. E. & Durako, M. J. (2005). The effect of salinity and ammonium on seed germination in Ruppia maritima from Florida Bay. Bulletin of Marine Science, 77, 3, 453-458. [26] Kantrud, H. A. (1991). Widgeongrass (Ruppia maritima L.): a literature review. U.S. Fish and Wildlife Service, Fish and Wildlife Research. [27] Koch, E. W. & Dawes, C. J. (1991). Influence of salinity and temperature on the germination of Ruppia maritima L. from the North Atlantic and Gulf of Mexico. Aquatic Botany, 40, 387-391. [28] Koch, E. W. & Seeliger, U.(1988). Germination ecology of two Ruppia maritima L. populations in southern Brazil. Aquatic Botany, 31, 321-327. [29] Koch, M. S., Schopmeyer, S. A., Kyhn-Hansen, C., Madden, C. J. & Peters, S. (2007). Tropical seagrass species tolerance to hypersalinity stress. Aquatic Botany, 86, 14-24. [30] Larkum, A. W. D., Orth, R. J., & Duarte, C. M. (2007). Seagrasses: Biology, Ecology, and Conservation. Springer, Dordrecht, The Netherlands. [31] Lazar, A. C. & Dawes, C. (1991). A seasonal study of the seagrass Ruppia maritima L. in Tampa Bay, Florida. Organic constituents and tolerances to salinity and temperature. Botanica Marina, 34, 265-269. [32] Malea, P., Kevrekidis, T., & Mogias, A. (2004). Annual versus perennial growth cycle in Ruppia maritima L.: temporal variation in population characteristics in The Rise of Ruppia in Seagrass Beds 15

Mediterranean lagoons (Monolimni and Drana Lagoons, Northern Aegean Sea). Botanica Marin ,47, 357-366. [33] Mills, S. L., Soule, M. E., & Doak, D. F. (1993). The Keystone-Species Concept in Ecology and Conservation BioScience, 43, 4, 219-224. [34] Moncreiff, C. A., Randall, T. A., & Caldwell, J. D. (1998). Mapping of Seagrass Resources in Mississippi Sound. Report to the MS Department of Marine Resources. BY3-156-3238. University of Southern Mississippi, Gulf Coast Research Laboratory, Ocean Springs MS. [35] Moore, K. A., Wilcox, D. J., & Orth., R. J. (2000). Analysis of the abundance of submersed aquatic vegetation communities in the Chesapeake Bay. Estuaries, 23, 115- 127. [36] Orth, R. J. & Moore, K. A. (1988). Distribution of Zostera marina L. and Ruppia maritima L. sensu lato along Depth Gradients in the Lower Chesapeake Bay, U.S.A. Aquatic Botany, 32, 291-305. [37] Orth, R. J., Harwell, M. C., Bailey, E. M., Bartholomew, A., Jawad, J. T., Lombana, A. V., Moore, K. A., Rhode, J. M., & Woods, H. E. (2000). A review of issues in seagrass seed dormancy and germination: implications for conservation and restoration. Marine Ecology Progress Series, 200, 277-288. [38] Orth, R. J., Carruthers, R. J. B., Dennison, W. C., Duarte, C. M, Fourqurean, J. W., Heck, K. L., Hughes, A. R., Kendrick, G. A., Kenworthy, W. J., Olyarnik, S., Short, F. T., Waycott, M., & Williams, S. L. (2006). A global crisis for seagrass ecosystems. BioScience, 56, 987-996. [39] Perry, H. (2005). Marine Resources and History of the Gulf Coast. MS Department of Marine Resources, Biloxi, MS [40] Scavia, D., Field, J. C., Boesch, D. F., Buddemeier, R. W., & Burkett, V. (2002). Climate Change Impacts on U.S. Coastal and Marine Ecosystems. Estuaries, 25, 149- 164. [41] Seeliger, U, Cordazzo, E., & Koch, E. W.(1984). Germination and Algal-free Laboratory Culture of Widgeon Grass, Ruppia maritima. Estuaries, 7, 176-178. [42] Short, F. T, Carruthers, T., Dennison, W., & Waycott, W. (2007). Global seagrass distribution and diversity: A bioregional model. Journal of Experimental Marine Biology and Ecology, 350, 3-20. [43] Short, F. T & Wyllie-Echeverria, S. (1996). Natural and human-induced disturbance of seagrasses. Environmental Conservation, 23, 1, 17-27. [44] Verhoeven, J. (1979). The ecology of Ruppia dominated communities in Western Europe. I. Distribution of Ruppia representatives in relation to their autecology. Aquatic Botany 6, 197-268. [45] Verhoeven, J. (1980). The ecology of Ruppia dominated communities in Western Europe. III. Aspects of production, consumption and decomposition. Aquatic Botany 8, 209-253.