Seagrass Monitoring in the Florida Keys National Marine Sanctuary

The general objective of seagrass monitoring in the Florida Keys National Marine Sanctuary (FKNMS) is to measure the status and trends of seagrass communities to evaluate progress toward protecting and restoring the living marine resources of the Sanctuary. The scope and depth of this monitoring effort are without precedent or peer for seagrass ecosystems throughout the world. Specific objectives are: 1) To provide data needed to make unbiased, statistically rigorous statements about the status and temporal trends of seagrass communities in the Sanctuary as a whole and within defined strata; 2) To help define reference conditions in order to develop resource-based water quality standards; and 3) To provide a framework for testing hypothesized pollutant fate/effect relationships through process-oriented research and monitoring. In order to meet these objectives, we have developed these goals for the project:

! Provide high-quality, quantitative data on the status of the seagrasses within the FKNMS

To reach these goals, four kinds of data are being collected in seagrass beds in the FKNMS:

! Distribution and abundance of seagrasses and other benthic plants and animals using rapid assessment Braun-Blanquet surveys

! Nutrient quality information using stable isotopic composition of seagrass leaves

These data are being collected at three different types of sites within the FKNMS:

! Level 1 Stations: Sampled quarterly for seagrass abundance, productivity and nutrient availability. These stations are all co-located with the water quality monitoring project’s stations (Figure 1)

! Level 2 Stations: Randomly selected locations within the FKNMS, sampled annually for seagrass abundance and nutrient availability. Each year, new locations for Level 2 stations are chosen.

! Level 3 Stations: Randomly selected locations within the FKNMS, sampled annually for seagrass abundance. Each year, new locations for Level 3 stations are chosen.

In addition to the monitoring activities, we take advantage of the vessel time needed to collect the monitoring data to also conduct manipulative experiments that help us understand the spatial and temporal trends in the monitoring data

The significant changes in seagrass communities at the permanent Level 1 stations that we reported last fiscal year continue to be present after an additional year of sampling. Additional lines of evidence now point towards more geographically widespread, long-term changes in the seagrass communities at the Level 1 stations. These changes are consistent with model predictions of nutrient-induced changes of these systems. There may be reasons for these observations that are unrelated to man’s activities in the region, but the spatial pattern of changes and the agreement of the changes with models of the system suggest that there is regional-scale change in nutrient availability that is causing changes in seagrass beds over a wide portion of the FKNMS.

In 2005, we resurveyed 355 Level 2 and Level 3 stations that were last visited during the summer of 1998. The data collected on these visits is still being assessed, but preliminary analyses indicate that there were significant trends in the abundance of two seagrass species between the 2 years. The largest change was that Halophila decipiens, which had been widespread and abundant on the southwest Florida shelf north of the FKNMS, was much less abundant in 2005 than 1998.

In general, nutrient addition to aquatic environments shifts the competitive balance to faster-growing primary producers. The consequences of this generality in seagrass-dominated environments is that seagrasses are the dominant primary producers in oligotrophic conditions. As nutrient availability increases, there is an increase in the importance of macroalgae, both free-living and epiphytic, with a concomitant decrease in seagrasses because of competition for light. Macroalgae lose out to even faster-growing microalgae as nutrient availability continues to increase: first, epiphytic microalgae replace epiphytic macroalgae on seagrasses; then planktonic microalgae bloom and deprive all benthic plants of light under the most eutrophic conditions. The south Florida case is more complicated than the general case described above because there are 6 common seagrass species in south Florida, and these species have different nutrient and light requirements, hence they have differing responses to eutrophication. Large expanses of the shallow marine environments in south Florida are so oligotrophic that biomass and growth of even the slowest-growing local seagrass species, Thalassia testudinum, are nutrient-limited; at this very oligotrophic end of the spectrum, increases in nutrient availability actually cause increases in seagrass biomass and growth rate. As nutrient availability increases beyond what is required by a dense stand of T. testudinum, there are other seagrass species that will out-compete it (Figure 2). The relative importance of the various primary producers, then, can be used to assess the trophic state of the community.

Figure 2. Idealized change in relative dominance of species along a eutrophication gradient in the FKNMS

Each species in the species dominance-eutrophication gradient model (Figure 2) can potentially dominate over a range of nutrient availability and the model predicts a change in species dominance as nutrient availability changes. These changes are not instantaneous, however. Field evidence suggests that species replacements may take place on a time scale of a decade or more. It is desirable that we be able to predict the tendency of the system to undergo these changes in species dominance before they occur, so that management actions can be taken. Tissue nutrient concentrations can be monitored to assess the relative availability of nutrients to the plants. For phytoplankton communities, this idea is captured in the interpretation of elemental ratios compared to the familiar "Redfield ratio" of 106C:16N:P. For the seagrass T. testudinum, the critical ratio of N:P in green leaves that indicates a balance in the availability of N and P is ca. 30:1, and monitoring deviations from this ratio can be used to infer whether N or P availabilities are limiting this species’ growth. Hence, T. testudinum is likely to be replaced by faster-growing competitors if nutrient availability is such that the N:P of its leaves is ca. 30:1. A change in the N:P in time to a value closer to 30:1 is indicative of eutrophication (Figure 3).

Figure 3. Relative amounts of nitrogen and phosphorus in seagrass leaves change in a predictable way as nutrient availability increases.

In addition to elemental content, the stable isotopic composition of plant tissues change as environmental conditions change. As light availability to the seagrasses is reduced, as occurs when nutrient availability increases and faster growing taxa proliferate, the stable carbon isotopic composition shifts towards values more depleted in the heavier stable C isotope, ¹³C. Hence, long-term changes in d¹³C values of seagrasses can serve as an indicator of changing light environment. Nitrogen stable isotopic composition can also indicate change in nutrient status; however this indicator is much more complicated to interpret. Sewage-derived nitrogen tends to be enriched in the heavier stable isotope, ¹⁵N, while fertilizer-derived nitrogen is depleted of this heavier isotope. Additionally, changes in the availability of light may affect plant stable N contents in a manner similar to the stable carbon isotopic content. While interpretation of patterns in stable N isotope composition are not straightforward, changes in the d¹⁵N of seagrass tissues does indicate a change in the nutrient environment of those plants.

These models lead directly to a definition of trends likely to be encountered in the seagrass communities of south Florida if humans are causing regional changes in nutrient availability because of alterations to quantity and quality of freshwater inputs to the marine ecosystem:

1) regional eutrophication will cause N:P ratios of seagrasses to approach 30:1 from higher or lower values indicative of oligotrophic conditions.

2) regional eutrophication will cause a shift in species dominance in south Florida seagrass beds. The first responses to eutrophication will be evidenced by an increase in the relative abundance of fast-growing seagrass species (H. wrightii and S. filiforme) at the expense of the now-dominant, slow-growing T. testudinum. At later stages of eutrophication, macroalgae and microalgae will become the dominant primary producers.

3) eutrophication will cause a decrease in the d¹³C of seagrass leaves.

4) a change in nutrient availability will cause shifts in the d¹⁵N of seagrass leaves.

Our monitoring data indicates a large spatial gradient in the N:P ratios of Thalassia testudinum across the sanctuary, with N:P ratios predicting nitrogen limitation in the offshore parts of the sanctuary and predicting phosphorus limitation in the nearshore areas. These predictions based on our conceptual model were tested experimentally and reported on in previous fiscal year reports. The nearshore seagrass beds did not respond strongly to nutrient addition (see Ferdie, M. and J.W. Fourqurean, 2004. Responses of seagrass communities to fertilization along a gradient of relative availability of nitrogen and phosphorus in a carbonate environment. Limnology and Oceanography 49(6):2082-2094). We also have completed experiments investigating the role of grazing fish in controlling the distribution of seagrasses in the seagrass beds adjacent to coral reefs in the FKNMS, and we have found that herbivorous fish can exert a greater control than nutrient availability in controlling seagrass community composition along the reef tract of the FKNMS (see Armitage and Fourqurean, in press. Effects of herbivory differ between seagrass species in a coral reef environment. Journal of Experimental Marine Biology and Ecology).

At 7 nearshore Level 1 sites in the Florida Keys, there have been changes in the relative abundance of seagrasses and macroalgae over the period 1995 - 2005 that are consistent with increased nutrient availability (Figure 4). At none of these has there yet been a decrease in seagrass abundance, but our conceptual model predicts that increases in fast-growing macroalgae should precede decreases in seagrass abundance (Figure 2). One example, from site 235 offshore of Lower Matecumbe Key, shows how macroalgae have steadily increased in abundance over the monitoring period (Figure 5).


Figure 4. Red dots indicate Level 1 sites showing changes in relative abundance of primary producers consistent with eutrophication.	Figure 5. An example of a site exhibiting changes in relative abundance of benthic primary producers. See Figure 1 for location.

In addition to these sites where relative abundance of primary producers has changed, at 9 of 30 Level 1 sites there have been long-term shifts in the ratio of nitrogen to phosphorus in seagrass leaves that are consistent with increases in nutrient availability (Figure 6).

Figure 6. Red dots indicate Level 1 sites showing changes in N:P of primary producers consistent with eutrophication

Stable isotopes of C and N of seagrasses also showed some significant long-term trends at some of the Level 1 sites. Decreasing values of d13C, which are consistent with a decrease in light reaching the seagrasses, were found at 3 sites (Figure 7). We measured both increases and decreases in stable nitrogen isotopic composition, with a geographic grouping of sites that increased and decreased (Figure 8).


Figure 7. Location of Level 1 stations exhibiting a decrease in stable isotope ratios of carbon in seagrasses, consistent with a decrease in light available to the plants.	Figure 8. Locations of Level 1 sites showing an increase (red symbols) of decrease (pink symbols) in stable isotope rations of nitrogen.

The sites that showed changes consistent with increased nutrient availability were not randomly distributed across the Sanctuary - rather, all of these sites were relatively close to shore in the Middle and Lower Florida Keys (Figure 9). The lack of any such changes in the Upper Florida Keys suggests that the factor driving the observed changes is not present across the entire Sanctuary, so factors acting at the global scale (like global warming or coastal overfishing) are not likely responsible for the observations. In addition to Level 1 sites that are exhibiting changes that are consistent with long-term increase in nutrient supply, two additional sites were severely impacted by hurricanes over the course of the monitoring period. While the trends in indicators we present are consistent with model predictions of nutrient-induced changes of these systems, there may be reasons for these observations that are unrelated to man's activities in the region. However, the spatial pattern of changes and the agreement of the changes with models of the system suggest that there is regional-scale change in nutrient availability that is causing changes in seagrass beds over a wide portion of the FKNMS.

Figure 9. Locations of Level 1 sites showing long-term trends consistent with eutrophication over the period 1995-2005, and the identity of the changing indicators.

In the previous 2 years of this project, resurveying the Level 2 and Level 3 sites revealed no spatially consistent patterns in changes in relative abundance of seagrass communities from throughout the sanctuary. However, this year we detected significant changes in the abundance and distribution of two seagrass species (Table 1). The changes in Braun Blanquet density for Thalassia testudinum and Syringodium filiforme for the period 1998 and 2005 were not significantly different from zero (mean change in Braun Blanquet density = +0.08 + 0.09 for T. testudinum and +0.04 + 0.09 for S. filiforme based on 355 pairwise comparisons), but there were significant decreases in the abundance and spatial extent of both Halophila decipiens (mean decrease in density of 0.25 + 0.08) and Halodule wrightii (0.06 + 0.04). The number of sites supporting H. decipiens decreased from 87 in 1998 to 26 in 2005; and the number supporting Halodule wrightii decreased from 65 to 46. Whether these changes were caused by environmental forcing or the ephemeral nature of these annual species is currently being investigated. In FY 2006, we will resample an additional 250 sites that were surveyed in 1999.

Table 1. Results of resurveying 363 Level 2 and Level 3 sites in 2005 that had originally been surveyed in 1998.

	1998	2005
Thalassia testudinum
Number of sites where present	206	201
Mean density	1.1	1.2
Median Density	0.3	0.3
Density Range	0.0-4.9	0.0-5.0
Syringodium filiforme
Number of sites where present	128	120
Mean density	0.6	0.6
Median Density	0.0	0.0
Density Range	0.0-5.0	0.0-5.0
Halodule wrightii
Number of sites where present	65	46
Mean density	0.1	0.1
Median Density	0.0	0.0
Density Range	0.0-4.9	0.0-5.0
Halophila decipiens
Number of sites where present	87	26
Mean density	0.29	0.03
Median Density	0.0	0.0
Density Range	0.0-4.3	0.0-1.6

Our surveys have provided clear documentation of the distribution and importance of seagrasses in the FKNMS. The seagrass bed that carpets 80% of the FKNMS is part of the largest documented contiguous seagrass bed on earth. These extensive meadows are vital for the ecological health of the FKNMS and the marine ecosystems of all of south Florida. Maps of spatial distributions and time series of species composition, seagrass productivity, nutrient availability and physical parameters can be found for each permanent monitoring site on the web site, www.fiu.edu/~seagrass or on the CD (2002) or DVD (2003, 2004 & 2005) produced and submitted for the technical report at year end.

Detailed analyses of the monitoring data have led to 21 peer-reviewed publications in the scientific literature (listed below). These publications address aspects of the functioning, status and trends of benthic communities as well as lay the groundwork for forecasting future anthropogenic impacts on this ecosystem. Numerous presentations by PI and students are also listed below.

Publications

1. Sea urchin overgrazing of a large seagrass bed in outer Florida Bay. Rose, C.D., W.C. Sharp, W.J. Kenworthy, J.H. Hunt, W.G. Lyons, E.J. Prager, J.F. Valentine, M.O. Hall, P. Whitfield, and J.W. Fourqurean. 1999. Marine Ecology Progress Series 190:211-222.

2. Spatial and temporal pattern in seagrass community composition and productivity in south Florida. Fourqurean, J. W., A. Willsie, C. D. Rose and L. M. Rutten. 2001. Marine Biology 138:341-354.

3. Competition between the tropical alga, Halimeda incrassata, and the seagrass, Thalassia testudinum. Davis, B.C. and J.W. Fourqurean. 2001. Aquatic Botany 71(3):217-232.

4. Large-scale patterns in seagrass (Thalassia testudinum) demographics in south Florida. Peterson, B. J. and J. W. Fourqurean. 2001, Limnology and Oceanography 46(5):1077-1090.

5. Seagrass distribution in south Florida: a multi-agency coordinated monitoring program. Fourqurean, J. W., M. J. Durako, M. O. Hall and L. N. Hefty. 2002. Pp 497-522 in: Porter, J.W. and K.G. Porter, eds. The Everglades, Florida Bay, and the coral reefs of the Florida Keys. CRC Press LLC, Boca Raton. 1000pp.

6. Disturbance and recovery following catastrophic grazing: studies of a successional chronosequence in a seagrass bed. Peterson, B. J., C. D. Rose, L. M. Rutten and J. W. Fourqurean. 2002. Oikos 97: 361-370.

7. Seagrass nutrient content reveals regional patterns of relative availability of nitrogen and phosphorus in the Florida Keys, FL, USA, Fourqurean, J. W. and J. C. Zieman. 2002. Biogeochemistry 61: 229-245.

8. Monitoring of soft-bottom marine habitat on the regional scale: the competing goals of spatial and temporal resolution. Fourqurean, J.W. and L.M. Rutten. 2003. Pp 257-288 in: Busch, D. and J.C. Trexler, eds. Ecological Monitoring of Ecosystem Initiatives. Island Press, Washington, D.C.

9. Forecasting the response of seagrass distribution to changing water quality: statistical models from monitoring data. Fourqurean, J.W., J.N. Boyer, M.J. Durako, L.N. Hefty, and B.J. Peterson. 2003. Ecological Applications 13(2): 474–489.

10. Intra- and interannual variability in seagrass carbon and nitrogen stable isotopes from south Florida, a preliminary study. Anderson, W.T. and J.W. Fourqurean. 2003. Organic Geochemistry 34:185-194.

11. Spatial and seasonal variability in elemental content, δ¹³C and δ¹⁵N of Thalassia testudinum from south Florida. Fourqurean, J.W. S.P. Escorcia, W.T. Anderson and J.C. Zieman. Estuaries. 2005. 28(3):447-461.

12. The impact of Hurricane Georges on soft-bottom, backreef communities: site- and species-specific effects in south Florida seagrass beds. Fourqurean, J. W. and L. M. Rutten. Bulletin of Marine Science. 2004. 75(2):239-257.

13. Nutrient limitation of benthic primary production in the upper Florida Keys. Ferdie, M., Masters of Science Thesis, Florida International Universtiy, Biology Department, 2002.

14. An assessment of nearshore benthic communities of the Florida Keys. Rutten, L.M., Masters of Science Thesis, Florida International University, Biology Department, 2002.

15. Elucidating seagrass population dynamics: theory, constraints and practice. Fourqurean, J.W., N. Marbà, and C.M. Duarte. 2003. Limnology and Oceanography 48(5):2070-2074.

16. Differential responses of benthic primary producers to nitrogen and phosphorus enrichment in a carbonate coastal marine system. Ferdie, M. and J.W. Fourqurean. 2004. Limnology and Oceanography 49(6):2082-2094.

17. Spatiotemporal variation of the abundance of calcareous green macroalgae in the Florida Keys: A study of synchrony within a macroalgal functional-form group. Collado-Vides, L., L.M. Rutten and J.W. Fourqurean. 2005. Journal of Phycology 41(4):742-752.

18. Dynamics of segrass stability and change. Duarte, C.M., J.W. Fourqurean, D. Krause-Jensen, and B. Olesen. 2006. Pp. 271-294 in Larkum, A.W.D., R.J. Orth and C.M. Duarte (eds) Seagrasses: Biology, ecology and conservation. Springer, Dordrect.

19. Potential role of the sponge community in controlling phytoplankton blooms in Florida Bay. Peterson, B.J., C.M. Chester, F.J. Jochem and J.W. Fourqurean. Marine Ecology Progress Series. In press.

20. The short-term influence of herbivory near patch reefs varies between seagrass species. Armitage, A.R and J.W. Fourqurean. Journal of Experimental Marine Biology and Ecology. In press.

21. Phenology, sexual reproduction, and the factors affecting sexual reproduction of the marine angiosperm, Thalassia testudinum, in the Florida Keys National Marine Sanctuary (FKNMS). Cunniff, K. M. Masters of Science Thesis, Florida International University, Biology Department. 2006.

Presentations

Fourqurean, J.W. and S.P. Escorcia. Long-term patterns of eutrophication in south Florida seagrass beds: water quality, species composition, and chemical proxies. Biennial Estuarine Research Federation meeting, Norfolk, VA Oct 15-20, 2005.

Armitage, A.R. and J.W. Fourqurean. Short-term herbivore impacts and long-term implications of nutrient enrichment on seagrass species distribution. Biennial Estuarine Research Federation meeting, Norfolk, VA Oct 15-20. 2005

Armitage, A.R. and J.W. Fourqurean. 2005. Acute influence of herbivory on seagrass distribution and the long-term implications of nutrient enrichment. 34th Annual Benthic Ecology Meeting. Williamsburg, VA. April 6-12, 2005.

Armitage, A.R., T.A. Frankovich, K.L. Heck, Jr, and J.W. Fourqurean. Experimental long-term nutrient enrichment causes complex changes in seagrass and epiphyte community structure in Florida Bay. Florida Coastal Everglades LTER All Scientists Meeting. Miami, FL. March 2005

Fouqurean, J.W. Invited seminar, Chesapeake Biological Laboratory, University of Maryland, Solomons Island, MD February 14. 2005