A Review of Certain Aspects of the Life, Death, and Distribution of the of the Southeastern United States 1960-1985

Joseph C. Zieman

Department of Environmental Sciences University of Virginia Charlottesville, Virginia 22903

ABSTRACT

Seagrass meadows are among the richest and ecologically most important coastal habitats. In the United States,the greatestseagrass resources are along the south and west coastsof Florida, with over 5,500 km' of seagrassin south Florida, and a secondextensive bed coveringover 3,000 kme betweenTampa and Apalachee Bay. Well developed meadows occur at depths over 10 m in clear waters, but are often limited to less than 2 rn in turbid, polluted estuaries. In these latter areas, suspended particulate rnatter, as well as over- growthsof epiphytic algae,brought about by excessnutrients in the water column,can stress the seagrasses.In more pristine waters, seagrasses maintain high productivity by obtaining nutrients from the sediments via ex- tensive root and rhizome systems, which, coupled with the current-baftling effect of the leaf canopy, protect and stabilize the sediments. In turbid, shallow seagrass systems, much of the food web is based on epiphytic algal grazing, but the dominant trophic pathway in most seagrass systems seems to be via the detrital food web, Seagrass leaves are a relatively rich food source, compared to saltmarsh and mangroves, but are grazed directly by few organisms, especially outside of tropical Caribbean waters. In addition to contributing to local food webs, detached seagrass blades are often exported great distances and serve as food sources hundreds of kilometers from their source beds,

INTRODUCTION - HISTORICAL PERSPECTIVE

Today, seagrassmeadows are recognizedamong Although the time scale is greatly compressed, the richest and most productive of all coastal compared to that of the classical sciences, seagrass ecosystems, providing habitat and food for innumer- ecologyhas progressedthrough recognizable stages able organisms. However, recognitionof the immense in this 25-year period, finally emerging as a mature importanceof these systemsin maintaining the area of study. Initially, nearly all of the literature abundance of commercial and sports fisheries, as was descriptive and qualitative. By 1970, most well as the numerous other benefits that they con- published works were quantitative, and development vey, is a comparatively recent development, In 1960, of conceptual models was just beginning. By 1980, the number of published papers concerning seagrass increasingly robust models of the mechanisms by ecology,or any aspectof seagrassbiology, could be which the systems develop and maintain their pro- counted on the fingers of very few hands. By 1978, ductivity were being proposed and used as guidesto a bibliography compiled by the Seagrass Ecosystem proposed research. Study listed over 1400 titles worldwide Bridges et In addition to advances in scientific equipment al,, 1978!, and, by 1982, a community profile of the and techniques, and increasingly powerful computer south Florida seagrasses contained over 550 refer- facilities, another technological advancement aided ences. the development of seagrass research to a degree 54 FLORIDA MARINE RESEARCH PUBLICATIONS impossible to overestimate: SCUBA. Seagrass re- protection. This seems to be due to the area's search has benefited immeasurably from the in- unique physical conditions, which create one of the creasing availability of safe, reliable, and relatively world's few zero-energy coastlines Murali, 1982; inexpensiveunderwater breathing gear, Researchers Tanner, 1960!. This meadowcovers 3,000 km2 and are no longer constrainedto wading in shallowbeds, is second in size only to the enormous beds in which were often quite stressed due to their shallow Florida Bay and behind the Florida Reef Tract, nature, and, therefore, not representative of most which spread from just south of Key Biscayne to seagrassmeadows. Seagrass meadows are ideal sub- west of Key West, totaling 5,500 km~ in area jects for the use of SCUBA techniques, because Iverson and Bittaker, 1986!. Seagrassesare reduced most occur in depths of less than 10 m, where use or excluded where excess runoff and turbidity create of SCUBA is relatively unrestricted. unfavorable conditions, such as off the Ten Thousand The objectiveof this paper is to review pro- Islands Iverson and Bittaker, 1986! or in Apalachi- gress, over the past 25 years, in our understanding cola Bay Livingston, 1984!, but are found in most of seagrass systems and what makes them so other estuaries. Other major estuarine or lagoonal beneficiaL Topics that will be addressedare distri- seagrass beds are found in Tampa Bay, Charlotte bution, biomassand production,nutrient cycling, Harbor, and the Indian River, decomposition and detrital processing, export, and a brief summary of general trophic structure as it ZONATION relates to the other topics. Although extensive development of seagrass beds is confined to depths of 10-12 m or less, sea- grasses have been recorded from as deep as 42 m. DISTRIBUTION The principal factors determining depth distribution are light and perhaps! pressure at depth, and ex- AREAL DISTRIBUTION posure and resultant dessication at the shallow end of the gradient. Nearly all of the seagrass resources in the The seagrasses of Florida are all subtidal, southeastern coastal region of the United States, tolerating little exposure. Exposure to air does occur from South Carolina to the Mississippi River, occur at certain low tides on shallow T. testudinum or in the coastalwaters and estuariesof Florida. By Halodule u rightii Aschers. fiats, and heavy leaf 1960, the distribution of seagrassesin this region mortality results, unless exposure is extremely brief. was relatively well described, but major gapain the Rafts of dead seagrassleaves frequently are carried literature left nearly a quarter of the coastline of from shallow fiats following spring low tides, but, Florida undescribed Phillips, 1960!. Much of this normally, rhizomes are not damaged and the plants unknownarea was addressedby Moore963!, who recover, gave a detailed observational and qualitative des- Numerous studies in Florida, from Phillips cription of the areal distribution of Thalassia 960! and Strawn 961! to Lewis et aL 985!, testudinumBanks ex Konig. McNulty et al. 972! have illustrated patterns of zonation in the state' s estimated the vegetative coverage of nearshore seagrass beds Figure 1!, Localized conditions waters and embayrnentsof inner Florida Bay and create much variability, but patterns of zonation the west coast of Florida, and found seagrass exhibit a definite commonality. The general pattern coverageto total 2,106 km~, tidal marshes,2,615 described below represents a typical gradient ob- km, and mangroves,1,591 km served throughout clear waters in Florida. In turbid Florida possessesone of the largest seagrass water areas, the same pattern could be expected, resources on earth Beds of various sizes are found but the ranges of various species would be attenu- in much of the protected waters from the Indian ated. A vertical zonation gradient that extends 10- River, on the central east coast, to Santa Rosa 15 m in the Keys or the Dry Tortugas, would be Sound, on the northwestcoast. Typically, beds compressed to 2 m or less in highly impacted occur in somewhat protected waters behind reefs, estuaries such as Tampa Bay or northern Biscayne barrier islands,or some other form of protection. Bay, or even in certain basins in Florida Bay that The Big Bend area of the northwest coast of Florida are free of any human impact. is quite unique in having seagrass meadows ex- Halodule terightii and Ruppia maritima L. gener- tending tens of kilometers offshore with no seaward ally are found in the shallowestwater and appear to NUMBER 42

Of all the major species,S. jiliforrne often has the most discontinuousdistribution. It is commonly found intermixed with T. test&inurn in deeper portions of the latter's range, but is virtually never found in waters as shallow as Thalassia or Halodule, because its stiff leaves do not bend sufficiently to conform to the sediment surface and reduce dessi- cation, Syringodiurnleaves are quite brittle, com- pared to those of other species, and break easily if bent at a sharp angle. However, the seems well adapted to both turbulence and rapid water flow. In highly turbulent waters immediately behind the Florida Reef Tract, Synngodiurn is commonly found either in dense monospecificstands or inter- mixed with Thalassia. Both plants seem to possess sufficientleaf strengthand root holdingcapacity to exist in this rigorous environment. Dense stands of Syrirtgodium are also commonly found in deep channelsthroughout the Florida Keys, where tidal current velocities are very high, and high turbidity reducesthe incident light.

Figure l, Zonation of seagrassesha an area of Tampa Bay. From PRODUCTION ECOLOGY Phillips, 1960!, Seagrassesoccur in a very wide range of den- sities, butunder optimum conditions,they can form vast high-density meadows. The literature on this be more tolerant of exposurethan the other species. subjectis extensiveand often bewilderingbecause The relatively high flexibility of their leaves allows values have been reported in a variety of forms. For them to conform to the damp sediment surface consistency, the terms used here conform to those during periods of exposure, thus minunizing leaf of Ziemanand Wetzel 980!: "standingcrop" refers surfaces available for dessication. Thalassia testu- to above-ground above-sediment!material, whereas dinum is found in waters nearly as shallow. The "biomass" refers to the weight of all living plant shallowest H. wrightii, R. rnantima, and T. testudi- material, includingroots and rhizomes. Both are ex- nam flats are commonly exposed by spring low pressed in terms of mass per unit of area. tides, frequently with considerableleaf mortality. All of the species may be found, singly or BIOMASS mixed, throughout the range of 1-10 m; however, T. testudinum ia unquestionably dominant in most Seagrassbiomass varies widely, depending on areas, frequently forming extensive meadows that the species and local conditions, especially water stretch for tens of kilometers. Although the absolute clarity, circulation, sediment depth, and nutrient depth limit of this species is deeper, mature content.The biomassof Halophila spp, is always meadows of Thaiassia are not found below 10-12 m small,whereas biomass exceeding 7 kg m 2 hasbeen Figure 2!. At this depth, Synngodium jilijorme recorded for T. testudinum Burkholder et al, 1959!. KQtzing replaces Thalassia and forms meadows Tables 1 and 2 give representativeranges for the down to the region of 15 m. Past the maximum speciesin the southeasternregion and in neighbor- depth for Syringodium development, H. wrightii ing areas for comparison. Because of the extreme often occurs, but it rarely develops extensively at variations found m nature and refiected in the litera- deptlL Fine carpets of Halophila spp. can occur at ture, one must be careful not to place too much depths greater than 40 tn. In the shallow but highly value on a few local measurements.Many studies turbid waters off the Shark River in southwest have been summarizedby Lewis et al. 985!, Florida, Halophila is sparse but widespread. McRoy and McMillan 977!, Thayer et al, 984!, 86 FLORIDA MARINE RESEARCH PUBLICATIONS

Figure2. Maximumdepth of occurrenceof seagrassspecies at St. Croix. From Phillips and Lewis, 1983!.

Zieman and Wetzel 980!, and Zieman 982!. more developed root network for nutrient absorption However, because these studies represent a variety in coarser sediments, which tend to be lower in of habitats, different sampling times and seasons, nutrients and organic matter. wide variation in sample replicates if any!, as well Structurally, T. testudirturrt has the best de- as diverse reasons for which various investigators veloped root and rhizome system of all local sea- collected the samples, caution must be used in grasses. Halodule tcrightii and S. filiforme typically attempting to generalize from literature values. will have much more of their total biomass in leaves Although the standing crop of leaves is quite than Thalassia Zieman, 1982!; areas where the leaf significant, most seagrass biomass is in the sedi- component is 50% to 60% of the total biomass are ments; this is especially true of larger species. not uncommon. Maximum values for the species Thalassia testudinurrt typically has about 15% to also vary widely. Dense stands of H. tUrightii 20% of its biomass in emergent leaves, although typically have values of several hundred g m~; S. published values range from 10% to 45%; the re- filifor7ne reaches maximum development at 1200- mainder is in roots, rhizomes, short-shoots, and 1500 g rn 2; maximum reported values for T. testu- sheathing leaves Zieman, 1975a, 1982!. Leaf-to- dirtum are over 7000 g m Z. root-and-rhizome ratios of T. testudinum decrease from I:3 in fine mud, to 1:5 in mud, and 1:7 in coarse sand, due to a two-fold increase in below- PRODUCTIVITY ground material in the coarser sand sediments Burkholder et aL, 1959!. This can be interpreted to Seagrasses are noted for their high primary indicate either the positive effect of richer fine muds productivity. Literature values for seagrass produc- on more robust plant development, or the need for a tivity, like those for biomass, vary enormously, NUMBER 42

TABLE 1. REPRESENTATIVE SEAGRASS BIOMASS g dwt m r!.

Species Location Range Mean Source

Hatodute wrightii

Florida 10-300 60-260 Zieman, unpubL data

Texas 10-250 90 McMahan, 1968; McRoy, 1974

North Carolina 22-208 Kenworthy, 1981

Syriqgodium f'diforme

Florida 15-1,100 100-300 Zieman, unpubL data

Texas 30-70 45 McMahan, 1968

Thalassia testudinam Cuba 30-500 350 Buesa, 1972, 1974; Buesa and Olaechea, 1970 Florida 20-1,800 125-800 Odum, 1963; Jones, east coast! 1968; Zieman, 1975b

Florida 75-8,100 500-3,100 Bauersfeld et aL, west coast! 1959; Phillips, 1960; Taylor et aL, 1973

Puerto Rico 60-560 80-450 Burkholder et aL, 1959; Margalef and Rivero, 1958

Texas 60-250 150 Odum, 1963; McRoy, 1974

depending on species, density, season, and measure- An unfortunate probletn surrounding study of ment technique. Table 3 shows some representa- seagrass productivities is that the three major tive productivity values for local species. Most methods utilized marking, 02, and C all give early studies emphasized T. testttdinum, but in the sotnewhat different results. Measurements for sea- past several years, information on H. wrightii and S. grasses and freshwater macrophytes show that the filiforme has begun to accumulate, oxygen technique produces the highest productivity Productivity values for south Florida sea- values, and marking techniques the lowest, with C grassesrange from less than 0.5 g C m day to 16 g values intermediate Kemp et al., 1981; Zieman and C m2 day 1. However, the highest reported values Wetzel, 1980!. Nonetheless, in a carefully developed e.gOdum, 1963! utilize community metabolism study, Bittaker and Iverson 976! found marking and reflect the products of seagrasses, epiphytic and radiocarbon techniques give virtually identical algae, and benthic algae. Measurement methods results. The marking technique Fry, 1983; Zieman, specific for seagrass production show that net 1974, 1975a! underestimates net productivity be- above-ground production is commonly 1-4 g C cause it does not account for below-ground pro- m day, although maximum rates can be several duction, excreted carbon, or herbivory, but it gives times these values Zieman and Wetzel, 1980!. the least ambiguous answers, The '4C method 58 FLORIDA MARINE RESEARCH PUBLICATIONS

TABLE 2. REPRESENTATIVE ABOVE-GROUND AND BELOW-GROUND SEAGRASS BIOMASS VALUES.

Biomass g dwt m2! Species Above-Ground Below- Ground Reference

Thalassia testudinum

Boca Ciega Bay BCB! 32.4 48.6 Pomeroy, 1960 Bird Key BCB! 325 Phillips, 1960 a Cat's Point BCB! 98 Phillips, 1960a Boca Ciega Bay BCB! 636 Bauersfeld et sL, 1969 320-1,198 Taylor and Saloman, 1968 Tarpon Springs 601-819 Dawes et aL, 1979 Tampa Bay 0.41-5 2. 7 Heffernan and Gibson, 1983 Tampa Bay 25-180 600-900 Lewis and Phillips, 1980

Syri ngodiurn /ili forrne

Tampa Bay 5-11 Heffernan and Gibson, 1983 Tampa Bay 50-170 160-400 Lewis and Phillips, 1980

Halodule torightii

Tampa Bay 4-27 Heffernan and Gibson, 1983 Tampa Bay 38-50 60-140 Lewis and Phillips, 1980

Rappia rnaritima

Tampa Bay 1,48 18-48 Lewis and Phillips, 1980

allows partitioning of the relative amounts of photo- underlying high seagrassproductivity, and definite synthate within the plants. Figure 3, taken frotn patterns in speciesresponse and regional response Bittaker and Iverson 976!, shows the location of are emerging,Seagrass productivity is largely gov- radioactive carbon in a T. teatudinttm plant after a erned by the availablenutrient supply and quantity 4-hour incubation period. While the leaves comprised and possibly quality! of light reachingthe leaf only 13% of the total biomass, they contained 49% surface. Williatns and McRoy 982! have shown of the labeled carbon. that tropical and subtropical American and Carib- As studies of seagrass productivity have beanspecies exhibit two characteristicproductivity matured, they have begun to explore the mechanisms responsesto light intensity. These patterns comple-

TABLE 3. REPRESENTATIVE SEAGRASS PRODUCTIVITIES.

Productivity Species Location g C m' day'! Source

Halodule u righdi North Carolina 0.5-2.0 Dillon, 1971

Syringodiam fih'forme Florida 0.8-3.0 Zieman, unpubL data Texas 0.6-9.0 Odum and Hoskin, 1958; McRoy, 1974

Thalass a testudi num Florida 0.9-16.0 Odum, 1957, 1963; Jones, east coast! 1968; Zieman, 1975b Cuba 0.6-7.2 Buesa, 1972, 1974 Puerto Rico 2,5-4,5 Odum et al., 1960 Jamaica 1.9-3.0 Greenway, 1974 Barbados 0.5-3.0 Patriquin, 1972, 1973 VUMBER 42 59

eoTOtalno uptake to TOtalweight Emergent, new leaves on a T. testudinurn short- Atter4-hour tncubationpenod shoot show rapid growth,with the overall growth rate decreasing exponentially with age Patriquin, 1973; Zieman, 1975a!. In BiscayneBay, growth leaves 49.D t3.3 averaged 2.5 mm per day, and increased with leaf width and robustness. Maximum rates of up to 1 cm per day were observedfor a 15- to 120-day period Zieman, 1975a!. For S, filiforme, Fry 983! has shown that on each upright shoot containing 1-3 Sheath 23.3 leaves,only the youngestleaf showsatty significant growth. Elongationrates in Indian River lagoon rhrtome 26.6 SQ3 varied from 0.9 to 3.1 cm d1. roe'ts 23

TEMPORAL AND SPATIAL PATTERNS Figure,'3. Distribution of recently fixed carbon in T. testudinum. iFrom Btttaker and lvereon, 1976!. Tropical and subtropical American seagrasses ment the observed successional roles of the plants grow in widely varied environmental conditions and Figure 4!. The more robust, successionallyinter- seasonalprogramming throughout their range. This mediate and climax species S. fili forme and T. has a pronounced effect on annual productivity and testudin.um, from Puerto Rico, showed a relatively biomass cycles, Figure 5 illustrates some of the slow initial carbon uptake and a relatively linear seasonal variability observed in a south Biscayne response throughout the range of tested irradiance, Bay T. testudinurn bed, over a 16-month period. with no indication of inhibition at 100% irradiance Productivity and standing crop varied seasonally, Figure 4!. In contrast, H. torightii had a higher with high values during the warmer months and low initial carbon-uptake rate that greatly increased at values during winter, the highest standing crop higher light intensities, but with an indication of values were about 2.5 to 3 times the winter some inhibition at 100% irradiance. All species minimum. This seasonalityvaries latitudinally with a tested showed a pronounced regional effect, with maximum-to-minimum leaf standmg crop ratio of plants from the tropical environment having much 1.2-2,5 on the northwestern coast of Cuba Buesa, higher photosyntheticrates. Mean maximum uptake 1974!, generally 2-3 in south Florida Zieman, rates in Puerto Rico were2.96 mg C g dwt1 h1 for 1975b, 1982!, and 6-8 on the northwest coast of Thalassia, 3,33 for Syringodium, and 11,42 for Florida Iverson and Bittaker, 1986!. Halodule; in Texas the relative rates were 1.38 for A major question in any ecosystemstudy is Thalassia, 1.35 for Syringodi um, and 2,76 for what regulatesproductivity. With the seagrassesof Halodule, the Gulf and Caribbean, areal productivity is ap- A study of seagrassesin the Indian River parently a primary function of biomass,and specific lagoon in Florida obtained much lower carbon fixa- productivity, a function of available light and tion rates Heffernan and Gibson, 1983!, The nutrient supply. Figure 6 is a scattergram of the highest mean rates from three stations measured in ar'eal production g m ! of T. testudinum as a March and Ju]y were 0.40 g C g dwt1 d1 for H. function of biomass in Florida Bay Ziernan and wrightii, 0.79 for T. testudinurn, and 1.72 for S. Fourqurean, in preparation!. This shows a tight filiforme. Epiphyte fixation in this turbid lagoonwas linear relationshipbetween production and standing high, with rates up to 1.02 g C g dwt d . However, crop r =,91!. The range of standing crop varied valuesfrom 12 stationsin Florida Bay in August by a factor of 79;1, from 1.8 to 142.9 g m 2, while showedthe rangeof 14Cfixation to be 0.85-3.67mg the turnover rate, an analog of specific productivity C g dwt h for T. testudinum, 1.26-2.42 for S. g production day to g standing crop! varied by a filiforme, and 1.47-6.21 for H. urrightii Zieman et factor of only 2.4:1, from 1.5% d1 to 3.6% d1, al, m preparation!, In Florida Bay, macroalgal Like other plant parameters, the turnover rate fixation was lower than that for seagrasses, with of T. testudinum varies regionally and latitudinaliy. values of 0.26-1.48 for all species sampled. These In north Florida waters, measured leaf turnover ranges are comparable to the tropical values rates average 0.9% d estimated from Bittaker and reported by Williams and McRay 982!. Iverson, 1976!. In south Florida, average values, in FLORIDA MARIVB RESEARCH PIJBLICATIONS

10.0

O I' e.o

Y z 0.0 0 C

2,0

25 75

5 SUR F ACE IR R ADI ANCE

Figure 4. Routes ot' carhon up- take for sea grasses in Puerto Rico and Texas. Fri>rn %ili>ams and McRoy, 1482!.

44

40 20 30 4! 50 00 70 $0 90 100 tt>SURFACE 1 RAADtAteCE NUMBER 42 61

though many patterns are emerging in this area, $0 many of the results seem contradictory. This can ~ 0 0 easily come about through attempts to force the 20 results of field or laboratory experimentation into 20 too simplistic a modeL Focusing on a particular pro- 140 cess or pathway under study is all too easy, even ' ~ 120 0 though nature may, in reality, have numerous 2 4 00 alternate pathways proceeding to the same end point 2 ~ ~ N C In dealing with detrital processing and nutrient 1 cycling, researchers must keep in mind that these functions are not independent, but are part of elemental cycles Fenchel and Jorgensen, 1977!. As 40 seagrasses or marsh plants die and decay, portions SO ~ of the fragmenting material may provide nutrition 20 for higher consumers, while other fractions of the same plant may be buried and remineralized, pro- 20 viding nutrients for primary producers. These are 1 12 but two alternate pathways of the same elemental cycles in marine ecosystems Figure 7!.

NUTRIENT SUPPLY

One of the most important and challenging areas of seagrass study is determining how the eco- systern maintains an adequate flow of nutrients to seagrasses, enabling them to sustain high produc- sa tivity. In 1960, virtually no studies addressed 20 nutrient cycling and supply in seagrass systems. Wood 959! had noted that Australian Zostera 20 beds required a reducing sediment in order to main- tain an active sulfur cycle and, thereby, nutrient J J A S 0 N 0 J F 20 A 02 J J A regeneration, but direct studies of nutrient dynamics Figure 5. Seasonalvariation in environmentaland plant para- in seagrass systems did not begin to appear in the meters in south Biscayne Bay. From Zieman, 1975!. literature until 1970. A coherent picture of the range and magnitude of dynamic processes influ- the summer months, are 1.9% for Biscayne Bay encing seagrass nutrient supply is beginning to Zieman, 1975b!, 2.0% for Florida Bay Zieman and emerge, but it is far from complete. Moreover, Fourqurean, in preparation!, and 2.1% in Pine despite much concentrated effort in other areas of Channel J. C. Zieman and R T, Zieman, unpub- seagrass ecology, very little of the work on seagrass- lished data!. In the tropical Caribbean, turnover rates system nutrient dynamics has been done in Florida for T. testudintun average 3.5% for St Croix Zieman and the southeast. Moat of the studies have utilized et aL, 1979, 1984! and 2.9% for Vieques Zieman, the temperate seagrassZostera marina I unpublished data!. Seagrasses are virtually unique in the inarine environment in that they inhabit both the water column and sediments. They are capable of nutrient uptake through either their roots or their leaves DETRITUS, NUTRIRNTS, AND MICROBES McRoy and Barsdate, 1970!, but are more efficient and show greater uptake rates through their root The past few years have brought a virtual ex- systems Penhale and Thayer, 1980!. In addition, plosion in the amount of literature dealing with seagrasses are capable of taking in nutrients froro detritus, nutrients, and microbial interactions related the sediments through their roots, translocating the to seagrasses, marsh plants, and rnangroves. Al- nutrients, and pumping them out through the leaves 62 FLORIDA MARINE RESEARCH PUBLICATIONS

3,5

3 04

3 2 ~ 5

1.5 CP

0 Q.

0.5

0 20 40 60 80 100 'l 20 140 160 1 BO 200

Standing Crop g dw m !

Figure6, Relationshipof productionto standingcrop in FloridaBay, FromZieman and Fonrqurean, in preparation!. into the surroundingwaters McRoy and Barsdate, cient root tissue for adequatenutrient absorption. 1970!, although this may be of importance only in Thus, to sustain growth, the plants need more areas of high ambient sediment nutrients Penhale nutrient-absorptive tissue in sediments that contain and Thayer, 1980!. less nutrients. Sediment-depth requirement varies Because seagrasses derive most of their with species. Due to its shallow, surficial root nutrients through their root systems,the depth of systems, H. tcrtghtii can colonize thin sediments if sediments directly affects seagrass development. the area is sufficiently stable hydraulically.Thalassia Although sedimentdepth is a neutral factor in many testudinumis a much more robust plant, requiring regions of seagrassdistribution where deep sedi- 50 cm of sedimentto achievelush growth, although ments predominate, in much of coastal Florida, meadow fortnation can begin with less sediment where thin veneers of sediments cover eroded Karst depth Zieman, 1972!. Scoffin 970! found that, in topography, it often is a controlling distributional the Bahamas, T, testttdirtum did not appear until factor. Figure 8 shows the developmentof greater sediment depth reached at least 7 cm leaf length and density in a T. testudinum bed as a Microbially mediated chemical processes in function of increased depth of sediments below the marine sediments provide the main source of seagrasses Zieman, 1975b!. A certain amount of nutrients for seagrassgrowth Capone and Taylor, sediment depth is useful in increasing the plants' 1980!. Although seagrassesrequire a variety of holding capacity, but the implication is that a mini- macro- and micronutrients, most research effort has mum depth of sedunent is necessary to allow suffi- beendirected to the sourceand rate of supply of NUMBER 42 63

WATER

SED tKHI T SuRFACE

AERODIC

ZONEOF DEMITRI- FICATION

ZONEOF suLFATE REDVC J OHI

AMINOACIDS COZ ZOHEOF MOHOAHD Dt- PART ICVLATE ACIDFER- SHORTCI1AIIO METHANE MET MANE SACCHARIDES DETRITus HEHTATIDH FATTYACIDS FORIPATIOH FORMATION LDNDCHAIH FATTYACIDS HZ

REFRACTORYMATERtAL

Figure 7. A conceptual model of carbon metabolism in a shallow marine system. From Fenchel and Jorgensen, 1977!.

nitrogen, Seagrasses have three potential nitrogen phytic community,while fixationin the rhizosphere sources: recycled nitrogen in the sediments, nitrogen contributedmainly to macrophyteproduction. Indi- in the water column, and nitrogen fixation. Bacterial processes convert organic nitrogen compounds to 110 W t~ ~ r ammonia, primarily in the anoxic sediment that 300 P ~ tl usually exists only a few millimeters beneath the i a! ~ 0 sediment surface. The ammonia that is not rapidly 30 bound by these processes will diffuse upward to the ~ lid' ze D aaity~ aerobiczone, where it can either escape to the water I lli diir 10 taa~ taZ! column or be converted to nitrate by nitrifying bac- 0 20 teria in the presence of oxygen. Nitrate is usually in ~ I~ di IO very low abundance or absent in sediments because t ~asti it is either rapidly metabolized or converted to dini- tileI trogen N2! by denitrifying bacteria sad>Niit 10 Nitrogen fixation can occur in either the rhizo- Diat l 20 sphere or the phyllosphere. Transfers between i m! leaves and epiphytes have also been demonstrated I" 30 s .5 I.s I.s Z.O Z.S Harlin, 1971; McRoy and Goering, 1974!. Capone D IPTAsct sc loss DED tau and Taylor 980! concludedthat nitrogen fixed in Figure 6, The relationship of leaf developmentand sediment the phyllosphere contributed primarily to the epi- depthin a seagrassbed in southFlorida. FromZieman, 1975!. 64 FLORIDA MARINE RESEARCH PUBLICATIONS

rectly, the contribution of nitrogen fixing epiphytes or hydrolyze organic phasphates.In addition, some is important because, after the leaves senesce and bacteria produce organic acids that can solubilize detach, most of them decay and become part of the inorganic phosphates by lowermg the pH Fenchel litter, some of which will be incorporated in the and Blackburn, 1979!. Rapid uptake and remineral- sediments, Other sediment sources include animal ization of phosphate by bacteria and their grazers excretion, particulate rnatter trapped by the dense can return phosphate to the inorganic pooL leaves, and dead root and rhizome materiaL Capone In a shallow-water successional sequence and Taylor 980! agreed with Patriquin 972! that leading to T. testudirrum, the early stages are often the primary source of nitrogen for leaf production is characterized by low sediment organic matter and recycled material from sediments, but found that open nutrient supply; the community relies on rhizosphere fixation can supply 20% to 50% of the nutrients brought in from adjacent areas by water plant's requirements. In an interesting experiment movement, instead of in situ regeneration. With the in Chesapeake Bay, Orth 977! applied commercial development from rhizophytic algae to Thalassia, a fertilizers directly to a Z. marina bed and found progressive development occurs in the below-ground that, after two to three months, the length and biomass of the community, as well as in the portion density of leaves had increased, the biomass of exposed in the water column Table 4!, With the roots and rhizomes was 30% greater than that of the progressive increase in leaf area, sediment trapping controls, and the standing crop of leaves had and particle retention increase. This material adds increased by a factor of 3-4. Available evidence sug- organic matter to further fuel sedimentary microbial gests that seagrasses are extremely efficient at cycles. capturing and utilizing nutrients, and this is a major factor in their ability to maintain high productivity in a relatively nutrient-poor environment. DE COMPOSITION AND The cycling of nitrogen differs greatly from DETRITAL PROCESSING that of phosphorus. In normal biogeochemical cycling, phosphorous has no gaseous phase, does The Traditional Detritus Concept not change valence state, and, ultimately, has one primary source, i.e., the weathering of phosphate The past 25 years have brought major changes minerals. Phosphorous is in very low concentration in researchers' understanding of how photosynthetic in tropical waters, but is often relatively abundant in plant energy is made available to higher consumers the sediments, mare so in the sediments af seagrass Figure 9!. The concept of detrital food webs and beds than in sediments outside the beds McRoy et the changes in organic plant matter that occur during aL, 1972; Patriquin, 1972!. Patriquin 972! reparted decomposition have been central to this under- high levels of HCl-extractable phosphate in the root standing. The theory of detrital food webs in marine layer af T. testirdirrum in carbonate sediments in and aquatic ecosysterns is based on the concept Barbados, but found that dissaived pore water con- that, for the majority of animals that derive all or centrations were low. Based on the slow rate of dis- part of their nutrition fram ma eraphytes, the solution of apatite, the primary mineral source of greatest proportion of fresh plant material is not phosphate in these sediments, Patriquin 972! con- readily utilizable as a food source. For these cluded that the overlying waters are the primary organisms, macrophyte organic matter becomes a source of phosphate to the seagrasses. Rosenfeld food source of nutritional value only after under- 979! found that Florida Bay pore water concentra- going decomposition to particulate organic detritus, tions were two orders of magnitude lower than those which is defined as dead organic matter along with in Long Island Sound and attributed the difference its associated microorganisms Heald, 1969!. to the adsorption of phosphate by calcium carbo- nate. Rapid adsorption of phosphate occurs on This section will only briefly describe the detrital foad web concept and then discuss recent calcite and aragonite Berner and Morse, 1974; Morse et aL, 1979!. Thus, phosphate is possibly work pertinent to seagrass ecasystems. For reference more limiting than nitrogen to seagrassesin tropical and background, numerous reviews exist, including carbonate sediments. Fenchel and Jorgensen 977!, Lee 980!, Nedwell 983!, and Tenore and Rice 980!. For reviews The role of microbes in controlling availability more specific to seagrasses see Klug 980!, of phosphate is unclear. Plants take up only ortho- Robertson 982!, and Thayer et aL 984!. Much phosphate, but bacteria can also directly incorporate recent and highly pertinent work was presented in NUMBER 42 65

TABLE 4. A GRADIENT OF PARAMETERS OF SEAGRASS SUCCESSION FRO54 TAGUE BAY LAGOON, ST, CROIX, U.S.V.I. Williams, 1981!. Dash indicates no data; values shown are averages.

Rhizophytic Colonizing Immature Thalossio Bare algal seagrass s eagreas seagrass Parameters sediments community bed bed climax

No, plants mz 254 981 3,089 1,533

Biomass 185 89 1,244 2,241 g dwt nr~!

No. Thaiossio. No Syringodinm: No. Halodtde

0:0:0 0:0:0 1:17:33 1:2:2 1:1:0

Interstitial NH4 0.0 1,0 304 6-200 micromoles N!

Adsorbed NH4 0.63 2.50 3.05 12.82 micromoles N g dry sedimenct!

77talnssio blade length 14.08 16.25 22.37 cm!

Thalossio blade width 8.33 10.17 10.87 mm!

Sediment deposition 240 2,168 2,941 g dwt m~ dayt!

Detrital seagrass Z5.Zl 25'2.10 g dwt ms weekt!

the Proceedings of the Symposium on Detritus seagra sacs salt marsh plants and rnan groves Dynamics in Aquatic Ecosysterns Roman and Figure 10!. The rate of degradation is increased by Tenore, 1984!. physical breakdown and fragmentation, alternate As plant litter begins to decay, it generally wetting and drying Zieman, 1975a!, action of passes through three recognizable phases Godshalk grazers Fenchel, 1970; Morrison and White, 1980!, and Wetzel, 1978!. The first is a rapid weight loss and increased nutrients in the medium Fenchel and due to leaching and autolysis of plant compounds. Harrison, 1976!. Typically, this phase is very rapid and the materials During decomposition and detritus formation, released are readily utilized. In the second phase, the size of the particulate rnatter is decreased, decay is slower and weight reduction is due to frag- making it available as food for a wider variety of rnentation and degradation of the substrate by animals. Reduction of particle size increases the microbial activity. At the end of the second phase, surface area available for microbial colonization, the remaining substrate is highly refractory and of thus increasing decomposition rate. Fine detrital greatly lowered food value. The third phase is the particles, whether utilized locally as suspended or relatively slow decomposition of this higMy resistant deposited organic matter or transported by water to residual material, distant areas, provide food for trophically important Depending on source material and environ- fauna of seagrass beds and adjacent benthic com- mental conditions, this degradation process may munities, such as polychaete worms, amphipods and take from several weeks to years. Increasing resis- isopods, ophiuroids, certain gastropods, and mullet. tance to degradation is roughly in the order. algae~ Unlike many animals, bacteria, fungi, and FLORIDA MARINE RESEARCH PUBLICATIONS

Fignre S. COnCeptualmOdel of detrital prOCeSsing. From Lee, 19SO!.

other microorganisms have the enzymatic capacity The food value of detritus commonlyhas been to degrade the increasingly refractory macrophyte considered a function of nitrogen content Odum organic matter, converting a portion of it to micro- and de la Cruz, 1967!. However, ' ecause up to 30% bial protoplasm and mineralizing a large fraction. of the nitrogen can exist in tightly bound nonprotein Nitrogen is typically 2% to 4' of the dry weight of fractions Harrison and Mann, 1975; Odum et al seagrasses, but microflora contain 5% to 10% 1979a; Suberkropp et al., 1976!, nitrogen content nitrogen. The microflora may utilize nitrogen from alone can lead to overestimation of the nutritional the macrophyte substrate, but they also have the value of the material. As decomposition progresses, capacity to incorporate inorganic nitrogen from the the proportion of total nitrogen that is nonprotein surrounding medium sediments or water column! can increase through several processes: complexing into their cells during decomposition, enriching the of proteins in the lignin fraction Suberkropp et al., detritus with proteins and other soluble nitrogen 1976!; production of chitin, a major cell wall com- compounds.In addition, carbon compounds of the pound of fungi Odum et al., 1979a!; and decom- microflora are much less resistant to digestion than position of bacterial exudates Lee et al., 1980!, the fibrous components of macrophyte litter, Thus, yielding a food source of lower value. However, decomposition is accompanied by gradual minerali- protein Thayer et al., 1977! and amino acid zation of the highly resistant fraction of seagrass Zieman et al., 1984! contents increase in some organic matter and by the corresponding synthesis macrophytes during decomposition, presumably of microbial biomass that contains a much higher leading to an enriched food source. Inhibitory com- proportion of soluble compounds. pounds found in macrophyte leaves also decrease in NUMBER 42 67

>0O

g 80 Z X

eo K

Z C9 40

g

TIME IN MONTHS Figure10. Comparativedecay rates of macrophytea. From Zieman, l975, audThayer et ai., l984!.

older and decomposing macrophyte leaves and litter 1982!. This fraction is rapidly assimilated by micro- Harrison and Chan, 1980!. organisms. In 14 days, the released DOC supported Additional sources of nutrition for micro- 10 times more microbial biomassper unit of carbon organisms are dissolved organic carbon and nitrogen than the particulate carbon fraction Robertson et DOC and DON! released by seagrasses during aL, 1982!. growth and decomposition. The DOC fraction A major tenet of detrital food web theory has released during growth and early decomposition been that microorganisms are necessary trophic contains many of the soluble carbohydrates and pro- intermediaries between macrophyte litter and detri- teins of the plants. It is quickly assimilated by tivorous animals. Much evidence suggests that these microorganisms, but is generally available to con- animals derive the largest portion of their nutritional sumers in significant quantities only after this requirements from the microbial component of conversion to microbial biomass. Under sterile con- detritus Fenchel, 1970; Hargrave, 1970; see also, a ditions, living T, testttdinum leaves released 2% to review in Levinton et aL, 1984; Tenore, 1977!. 10% of recently fixed material Wetzel and Penhale, Detritivores typically assimilate microfloral com- 1979!, while dried Tha assia and S. filiforme leaves pounds with efficiencies of 50% to almost 100%, released 13% and 20% of their respective organic whereas plant compound assimilation is often low carbon contents during leaching Robertson et al,, Cammen, 1980; Lopez et al., 1977; Yingst, 1976!. 68 FLORIDA MARINE RESEARCH PUBLICATIONS

Newell965! found that deposit-feedingmolluscs functioning of the microbial community Rice, 1982; removednitrogen from sedimentparticles by re- Tenore, 1977, 1983!. This variation can strongly movalof the microorganisms,but did not measurably affect the apparent trophic role of the seagrassesm reduce the total organic carbon content of the sedi- individual beds. ments,which, presumably, are dominated by detrital Although seagrassesare marine macrophytes, plant carbon.When nitrogen-poor, carbon-rich feces they differ in many ways from salt marsh plants and were incubated in seawater, their nitrogen content mangroves, with which they are frequently com- increased due to the growth of attached micro- pared. For instance,upon enteringthe systemunder organisms.A new cycleof ingestionby the animals normal conditions, seagrass leaves are much higher wouldagain reduce the nitrogencontent as the fresh in nitrogen content than either salt marsh plants or crop of microorganismswas digested.Also, by mangroveleaves Figure ll!. They contain up to 4% selectivegrazing, amphipods and other crustaceans total nitrogen Zieman et al., 1984! and up to 25% ingestedthe microbial componenton leaf litter protein Dawes and Lawrence, 1983; Vicente et aL, without ingesting the substrate Morrison and 1980!. Although senescent leaf tips are low in White, 1980!. However,the grazing action of detri- nitrogen, the bases of recently detached leaves tivores can have positive feedback and enhance pro- typically retain a significant proportion of living duction of microbial populations an the detrital green material Figure 12; Table 5!. particles.Microbial respiration rates associated with During decomposition, the nitrogen content of rnacrophytedetritus were stimulated by the feeding mangrove and salt marsh material increases Heald, activities of animals,possibly as a result of physical 1969; Odum and de la Cruz, 1967; Rice, 1982!, fragmentationof the detritus Fenchel,1970; Foulds while that of seagrassesremains relatively constant and Mann, 1978! or by the removal of inhibitory Rice, 1982! or decreases somewhat Figure 13!. decompositionproducts Lee, 1980!. Similarly, the protein and amino acid contents of While the importance of the microbial com- mangroves rise during decomposition, but decrease ponentsof detritus to detritivoresis firmly estab- or show no change in seagrasses Rice, 1982; lished, other studies have indicated that consumers Zieman et aL, 1984!. may be capableof assimilatingthe plant substrate When seagrasses and mangroves decompose Foulds and Mann, 1978!. In someinstances, the under similar conditions, carbon stable isotope high abundanceof particulate material compensates ratios do not change for either. Nitrogen stable for low assimilation efficiency Hargrave, 1976!. isotope ratios also do not change during seagrass Cammen980! found that only 26% of the carbon decomposition, but they do change dramatically in requirementsof a population of deposit-feeding mangroves Ziemsn et aL, 1984!. Mangrove litter polychaeteswould be met by ingestedmicrobial bio- also shows much greater uptake rates of ammonium mass, although the microbial biomasscould supply per gram of plant litter R. T. Zieman,unpublished 90% of the population's nitrogen requirements. data!. These and other parameters lead to the con- Tlius, while microbial biomassis assimilatedat high clusion that seagrass decomposition largely utilizes efficiencies of from 50% to 100% Lopez et aL, the internal nitrogen pool, while mangroves require 1977; Yingst, 1976! and can supply proteins and extensive exogenous nitrogen input by microbes. essentialgrowth factors, the large quantities of In addition ta compositional differences be- ingestedplant materialmay be assimilatedat low tween seagrassesand other rnacrophytes, which can efficiencies less than 5%! to supply carbonrequire- lead to different mechanisms of decomposition, ments, differences among the seagrass plants themselves also have been reported. Dawes and Lawrence SeagrassDetritus vs, Other Macrophytes 983! showed a shift in the protein content of T. testudiriurn leaves from 13% in Tampa Bay, to 16% at Key West, to 25% in Belize. Thus, within this In its broadest form, the detrital food web species, the mode of decomposition and the quality still seems the most applicable to seagrass systems. of resulting detritus may vary widely, depending an A wide variety of current information re-examines regional origin. the role of seagrassesas food sources.A primary cnnceptof this re-examinationis that the initial com- EXPORT positionof macrophytelitter varieswidely, and that this variation affects the food value and decomposi- Seagrasses and associated epiphytes provide tion rate of the initial material, as well as the food for trop hie ally higher organisms via three NUMBER 42 69

2.0 O r 00 1 4 2.0 i.s

Z a. IS 4 15 Z

Z WZ' Q 1,4 V 3 10 r IJJ Z tu Q 1.2 1- O4 0.5K Z IJJ ! 1.0 1- 0 ui 50 100 150 K 0.80 50 100 DETRITUS AGE t Days ! DETRITUS AGE I Days!

~ 1,20

is I.IO a 1.4 I.oo

1.2 O 0.90ar

1.0 ~ 0.80 Z~ 08 +~0.70 06 Z~ 04 0- o.eo ~ 0,50 Q0 02 50 0 ~9 0 2S So75 ioo I25 DETRITUS AGE Days ! DETR TUS AGE 0ys!

Figure 11, Comparativechanges of the nitrogenousconstituents of marineand estuarineplants during decomposition. From Rice, 1982!

distinct routes: 1! direct herbivory, 2! detrital food conditions in these environments result in different webs within grass beds, and 3! export of material rates of physical decomposition Zieman, 1975a!; that leaves the donor beds as either macroscopic for instance, seagrass leaves exposed ta alternate leaf fragments or as detritus and is consumedin wetting and drying or wave action break down very other systems. In different seagrass systems, the rapidly. relative magnitude of the pathways may differ In exposed areas, leaves and large chunks of greatly, and either herbivory or export or both! may leaf, rhizome, and sediment can be detached by be!acking. storm action. In clear tropical waters, leaf detach- Seagrass leaves are frequently detached and ment is mast often caused by the action of grazers. transported away from the beds. Large quantities In Tague Bay, St, Croix, the feeding of parrotfish is are fOund arnOng mangrOveS, in wrack lineS alang largely responsible for the creation of large drift beaches, floating in large mats, and in depressions lines of exported seagrass blades. Here, T. testttd rturrt on unvegetated areas of the bottom. Studies have production was 2.7 g dwt m 2 d t, of which only shown that differences in physical and biological about 1% was exported; 60'7e to 100% of the 0.3 g 70 FLORIDA lVIARINE RESEARCH PUBLICATIONS

l.eat C/N Epiphytea

Dark Green ta Srown; SeneICent; COrenClnly Heavily Epiphytized

Older Decreaaed Kpiphytiam

YaunO, Green, Rapidly Growing, Few Kpiphytel

~ s I I ~ I 0'l t4 0 10M 30

% N C/N Epiphytel

Figure 12, Relative changes of carbon and nitrogen with aging of a Tholassia tesrttdinrrrn leaf. From Thayer et al, 1984!,

dwt m2 d I production of S. filiforme was exported material, although it may be a small proportion of Zieman et al., 1979!. A conservative estimate from the donor beds. This species contains large air these figures is that about 70% of the daily prodrtc- spaces and can remain afloat for long periods, while tion of seagrasses was available to the detrital T. testttdinlsm rarely fioats for more than a single system, whether locally or at a distance. day, In the Indian River lagoon, Fry 983! found The export described abcve is typical, in that that 47% Of the SyringOditsmwaS tranSperted frOm S. filiforme constitutes the major portion of the drift the beds. As this was the dominant seagrass, he

TABLE 5. CHANGES IN CONSTITUENTS IN Thafossirr testrrdinrrm RELATED TO SEASON, LOCATION, AND AGE OF LEAF,

Seasons Location Tampa Bay, Key West, Glovers Winter Spring Summer Fall Fl. FL Reef, Belize

Protein "ri! 9 22 13 13 16 25

Insoluble carbohydrates ri! 34 47

Leaf age and conditions Fresh Old Old green epiphytiz ed brown

Nitrogen /c AFDWI 1.6-2.0 0.5-1.7 0.6-1.1

C/N 13,8-19.8 21,1-25.2 27.5-41.6

Dawes and Lawrence 980!. west coast of Florida. ve Dawes and Lawrence 983!, eeeZieman et aL 984!, St, Croix, U.S.V.L NUMBER 42 7l

SEAGRASS MAMGROV E

PINE CHANNEL ROOKERY BAY PINE CHA NNEL ROOKERY BAY

THAL SYR THAL HAL GREEN YELLOW GREEN YELLOW

N 1%dwI

EAA trlllllOI 9

RIhlhO-N f9XRI

5 10 -15 .50 -55 .50

D-Glu

0 5 0 0 5 ~ 0 S 5 0 5 ~ 0 5 0 0 5 ~ 0 5 WEIEKS WEEItS

Figure 13, Comparative changes of the constituents of seagrass and mangrove leaves during decomposition. From Zieman et al, 1984!,

concluded that this, in part, increases the importance occurs away from the beds. Highly decomposed, fine of algal components of the food web. detrital particles 0.5 mm! are easily resuspended and are widely distributed by currents Odum et al., In the St. Croix trench, at a depth of 4,000 m, 1979b!. They contribute to the organic detritus pool sea urchins primarily consume 9, jitiforme leaves, at in the surrounding waters and sediments, where a great distance from the leaves' source. Menzies they continue to support an active Inicrobial popu- and Rowe 969! and Menzies et aL 967! found a lation and are browsed by deposit feeders. surprising density of T. testudirtum leaves in 3,160 m of water off the coast of North Carolina, at a LITERATURE CITED distance of at least 1000 km from the nearest source beds. Off the west coast of south Florida, vast rafts of drifting seagrasses can be seen several hundred BAUERSFELD, P., R. R KLEER, N. W. DURRANT, km from their source in Florida Bay, potentially and J. E. SYKES contributing nutritive material to the highly pro- 1969. Nutrient content of turtle grass Thalassia ductive shrimping grounds of the region Zieman, testudirtttrn!.Proc. Int. SeaweedSymp. 6: 19S2!. In addition to the export of large fragments 637-645. of leaves, much of the contribution of seagrasses to BERNER, R. A., and J. W. MORSE higher trophic levels, through detrital food webs, 1974. Dissolution kinetics of calcium carbonate 72 FLORIDA MARINE RESEARCH PUBLICATIONS

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