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OIKOS 72: 349-358. Copenhagen 1995




The effects of long-term manipulation of nutrient supply on
competition between the seagrasses Thalassia testudinum and
Halodule wrightii in Florida Bay

James W. Fourqurean, George V. N. Powell, W. Judson Kenworthy and Joseph C. Zieman


                     Fourqurean, W., Powell, G. V. N., Kenworthy, J. and Zieman,J. C. 1995. The
                           J.              W.
                     effects of long-termmanipulation nutrientsupply on competitionbetween the
                                     of
                     seagrasses Thalassia testudinum and Halodule wrightii in Florida Bay. - Oikos 72:
                     349-358.

                     Long term(8 yr) continuous  fertilization application birdfeces) of established
                                         (via      of
                     seagrassbeds in FloridaBay, FL, USA caused a change in the dominantseagrass
                     species.Beforefertilization, seagrassbeds were a Thalassiatestudinum
                                   the                      monocul-
                     ture;after 8 yr of fertilization seagrassHalodulewrightiimade up 97% of the
                                     the
                     aboveground  biomass.Fertilization a positive effect on the standingcrop of T.
                                       had
                     testudinum thefirsttwo yearsof the experiment. transition
                           for                  The      fromT. testudinum-
                     dominated H. wrightii-dominated dependent thetimingof colonization the
                          to            was     on              of
                     sites by H. wrightii;the decreasein T. testudinum standingcrop and densityat the
                     fertilizedsites occurredonly afterthe colonization the sites by H. wrightii.There
                                              of
                             in
                     wereno trends thestanding   cropordensityof T.testudinum controlsites,andnone
                                                   at
                     of the controlsites werecolonizedby H. wrightii.The effects of fertilization these
                                                           on
                     seagrassbedspersisted least 8 yr afterthe cessationof nutrient
                                at                    addition, suggesting
                     thatthese systemsretainand recycle acquired  nutrientsefficiently.
                     Resultsof these experiments  suggestthatHalodulewrightii,the normalearly-succes-
                     sionalseagrassduringsecondary  successionin Caribbean seagrass communities, ahas
                     highernutrient  demandthanThalassiatestudinum, normallate successionalspe-
                                              the
                     cies, and that the replacement H. wrightiiby T. testudinum
                                     of                during secondary
                     successionis due to the abilityof T.testudinum drawnutrient
                                            to        availabilitybelowthe
                     requirements of H. wrightii.

                     J. W.Fourqurean and J. C. Zieman, Dept of Environmental Sciences, Univ. of Virginia,
                     Charlottesville, VA22903, USA (present address of JWF: Dept of Biological Sciences
                     and Southeast Environmental Research Program, Florida International Univ., Miami,
                     FL 33199, USA). - G. V. N. Powell, RARE Center for Tropical Conservation, 1529
                     Walnut St., Philadelphia, PA 19102, USA. - W. J. Kenworthy, National Marine
                     Fisheries Service, Southeast Fisheries Center, Beaufort, NC 28516-9722, USA.




Species composition of plant communities is dependent     to reach equilibrium following a disturbance, resource-
on a number of factors, including prevailing resource     based models of community structure predict that the
supply rates, the length of time since the last disturbance  species composition of the community will be deter-
(successional state), the historical make-up of the com-   mined by the resource supply rates to the community
munity, and the likelihood of colonization of the area by   (Tilman 1982, 1985, 1988). A resource (sensu Tilman
individual species (Harper 1977, Grime 1979, Tilman      1982) is any factor consumed by an organism that causes
1982, 1988). Given sufficient time for plant communities   an increase in growth rate or survival. Using this defini-


Accepted 1 September1994
Copyright OIKOS1995
     ?
ISSN 0030-1299
         -
Printedin Denmark all rightsreserved

OIKOS 72:3 (1995)                                                    349
                                               Fig. 1. Site map of Florida
                                               Bay.




tion, light, nutrients and water are resources, but factors  nutrient-limited; fertilization of the Thalassia testudi-
such as temperatureare not. This model explicitly consid-   num-dominated seagrass meadows in northeast Florida
ers trade-offs in the ability of plants to compete for    Bay increases biomass of T. testudinum (Powell et al.
resources in two realms: aboveground and belowground.     1989). The biomass of T. testudinum on a bay-wide scale
Due to the limited energy available to a plant, allocation  is positively correlated with the concentration of dis-
to gathering belowground soil nutrients and water must    solved inorganic phosphorus in the sediment porewater
necessarily decrease the relative allocation to gather abo-  (Fourqurean et al. 1992a), and the observed increasing
vegound resources (e.g. light; for review see Chapin     trend in biomass from northeast to southwest in Florida
1980).                            Bay is a direct result of the increase in P availability
  The resource-ratio model predicts that availability of   along the same transect (Fourqureanet al. 1992b).
both soil nutrients and light exert a strong influence on    Species composition of seagrass beds of Florida Bay
the species composition of plant communities, and ma-     also is correlated with nutrient availability. Zonation of
nipulations of the resource supply rates of either the    species in relation to point sources of nutrients in other-
above- or belowground resources may lead to changes in    wise oligotrophic northeast Florida Bay suggests that
community composition. Addition of nutrients to a com-    Halodule wrightii occurrence is correlated with areas of
munity composed of species with different aboveground/    higher nutrient availability than Thalassia testudinum
belowground resource acquisition strategies should favor   (Powell et al. 1991), and after four years of continuous
species that have relatively less of their energy allocated  fertilization of once-monospecific T. testudinum beds, H.
to nutrient acquisition (and consequently more of their    wrightii colonizes the fertilized sites (Powell et al. 1991).
energy allocated to light gathering). Nutrient addition    Across the entire bay, areas that support H. wrightii have
experiments provide a means for testing ecological theo-   higher concentrations of dissolved inorganic P in the
ries concerning the effects of nutrient availability on    sedimentary porewater than areas that support only T.
community composition and successional development.      testudinum (Fourqureanet al. 1992a).
  Seagrass meadows of the tropical western Atlantic       Why Halodule wrightii should be restricted to areas of
provide an accessible system in which to test the re-     high nutrientavailability is not well understood, but it has
source-based model of ecological succession. The small    been suggested that H. wrightii has a higher demand for
number of seagrass species, the simplified successional    nutrients than Thalassia testudinum (Fourqurean et al.
sequence of these seagrass communities, and the        1992a). In most places in Florida Bay, T. testudinum is
strengths of environmental gradients in shallow marine    the competitive dominant; Zieman et al. (1989) state that
systems, all are desirable features for testing model pre-  H. wrightii is the dominant seagrass only in areas phys-
dictions on the roles of resource supply rates in structur-  ically unsuitable for T. testudinum. In the secondary suc-
ing plant communities.                    cessional sequence in seagrass beds of south Florida and
  Seagrass communities in Florida Bay (Fig. 1) are      the Caribbean, H. wrightii is an early successional spe-
strongly affected by the availability of nutrients. Devel-  cies and T. testudinum is a late successional species (see
opment of seagrass meadows in northeast Florida Bay is    Zieman 1982 for review). The mechanism of the replace-

350                                                    OIKOS 72:3 (1995)
ment of H. wrightii by T. testudinum during the succes-
sional process has been speculated to be competition for
                               Data collection
light, with T. testudinum eventually overtopping H.      The species composition, leaf biomass and short shoot
wrightii due to its larger size. This proposed mechanism   (SS) density of the seagrass bed around each control and
is unsatisfactory in Florida Bay, since the T. testudinum   fertilization treatment stake was measured when the ex-
canopy that replaces H. wrightii is often thin and sparse,  periment was begun, and in late October or early Novem-
with small effects on the amount of light that reaches the  ber for the next 8 yr. Short shoot density data were not
sediment surface (pers. obs.). Further,H. wrightii is more  collected in 1988. In 1987, 1989, 1990 and 1991, these
shade-tolerant than T. testudinum (Wiginton and McMil-    same variables were measured at the markers where fer-
lan 1979, Iverson and Bittaker 1986), and H. wrightii     tilization had been discontinued in 1983. For each sam-
exists in many locations as an understory in very dense    pling, 4 quadrats(10 cm x 10 cm) were placed within 50
seagrass beds (pers. obs.).                  cm of the marker stakes. The number of short shoots of
  This paper presents the results of experimental manip-   each seagrass species were counted, and the seagrass leaf
ulations of the nutrient supply to shallow water seagrass   biomass within the quadratswas harvested. These leaves
beds in Florida Bay. These experiments were designed to    were separated by species, washed in 10% V/V HCl to
elucidate the mechanisms underlying the apparent com-     remove epiphytes, and dried to a constant weight. Leaf
petition between Thalassia testudinum and Halodule      biomass, commonly called standing crop in seagrass liter-
wrightii. Two types of manipulations were performed: 1)    ature, and short shoot (SS) density, were expressed on a
continuous fertilization of previously undisturbed, T. tes-  m-2 basis.
tudinum-dominated seagrass beds, and 2) cessation of
fertilization of H. wrightii-dominated seagrass beds pre-
viously created by 28 months of continuous fertilization.   Statistical analyses
                               The average value for the four quadrats from each stake
                               were used in statistical analyses. Differences in the stand-
Methods                            ing crop and short shoot density of seagrasses at control
                               (CONT) and fertilized (FERT) stakes as a function of
Experimental design                      both treatment and time were assessed using mixed-
This study was conducted on Cross Bank, a shallow (< 30    model univariate repeated measures analysis of variance
cm deep), narrow (< 50 m wide) seagrass-covered car-     (Winer 1971) with treatment (CONT vs FERT) and year
bonate mud bank in east-central Florida Bay (Fig. 1). In   as within-subjects factors. Each pair of CONT and FERT
July 1981, location markers were placed at 100-m in-     stakes constituted a subject in these analyses. Five of
tervals along the center of Cross Bank as part of a sep-   these ANOVAs were run: one each for differences in
arate study on feeding behavior of wading birds (Powell    short shoot densities of Thalassia testudinum and Halo-
1987). The markers were constructed of 1.5 m long, 1.2    dule wrightii, differences in standing crop of both spe-
cm diam. PVC pipe with a 5 cm x 10 cm x 10 cm block      cies, and differences in total seagrass standing crop.
of wood on top. Once in place, these markers were        The discontinuation of fertilization treatment (DISC)
heavily used as roosts by royal terns (Sterna maxima) and   was not included in the above analyses since there were
double-crested cormorants (Phalacrocorax auritus). By     no measures made of the seagrasses around these stakes
November 1983, a patch of unusually dense seagrass was    in the years 1983-1986 or 1988. Differences between
evident around each location marker. At that time, we     years in the standing crop and short shoot density at these
began our experiment to test the hypothesis that deposi-   stakes were assessed with repeated measures ANOVA,
tion of feces by the roosting seabirds was responsible for  with years as the within-subjects factor.
the observed increase in seagrass density around the
markers. Five of the markers, spaced at 600-m intervals,
were pushed down into the sediment so that birds could
no longer roost on them, and a pair of new markers were
                               Results
placed 5 m on either side of the old marker. One of the
new markers was identical to the old marker, while the    Some results from the first four years of this experiment
other new markerwas cut to a point to prevent birds from   have been reported elsewhere (Powell et al. 1989, 1991).
roosting. This design provided five sites, each with three  Marker stakes in the FERT treatmentgroup hosted roost-
treatments: 1) a control treatment, in which the pointed   ing birds 84% of the time; 0.68 g of nitrogen and 0.13 g
stake provided the same hydrological effects as the bird   of phosphorus were deposited daily as bird feces at each
roost stake (CONT); 2) a fertilization treatment, where    of these roost markers. From 1983-1987, this nutrient
birds could roost on the marker and defecate into the     input caused increases in the leaf biomass and a change in
water (FERT); and 3) a treatment in which 28 months of    the species composition of the seagrass meadows in
fertilization was discontinued where the markers had     5.4 m x 2.6 m elliptical patches surrounding the roost
been pushed into the sediment (DISC).             marker stakes, while no trends occurred at the control

OIKOS 72:3 (1995)                                                  351
         Fertilized            Control         the sites. Very small patches of Halodule wrightii grew
    200              200                 elsewhere on Cross Bank, but none was within 10 m of
    150              150
                                      our sites. In 1991, after 8 yr of fertilization, the seagrass
a1)                                    beds at the FERT sites were dominated by H. wrightii,
    100               100
                                      while T. testudinum remained the only seagrass species
U)    50               50
                                      present at the CONT sites. In 1991, there were 860 ? 125
     0                0                 (+ 1 SE) SS m-2 of T. testudinum at the CONT stakes,
    200              200
CN                                     compared with 40 + 35 SS m-2 at the FERT sites. H.
    150              150
                                      wrightii densities were 6260 ? 319 SS m-2 at FERT sites,
a)   100               100                 and 90 + 80 at the controls.
:t
U)    50               50
                                        Annual trajectories of the standing crop of Thalassia
                                      testudinumand Halodule wrightii were site-specific (Fig.
      0               O   *     a     a .
                                   .
    200              200                 2). At all of the FERT sites, T. testudinum standing crop
r()                                    increased in the first year. At the sites where H. wrightii
    150               150
                                      became established in 1984 (sites 1, 3 and 4), T. testudi-
-ci  100               100                 num standing crop decreased thereafter.At sites 2 and 5,
UT)
     50               50                 T. testudinumstanding crop continued to increase until H.
                                      wrightii became established (1985 and 1987, respec-
.4-
                    200                 tively); after H. wrightii became established, T. testudi-
                    150                 num standing crop at these sites decreased. By 1989, H.
 a)                                    wrightii was the dominant seagrass at all of the FERT
                    100
                                      sites, while there was no H. wrightii at any of the CONT
                     50                 sites. There was considerable yearly variation in the
                     0   *   ?
                           a  1-   .   .  standing crop of T. testudinum at the CONT sites.
     200              200                  The total standing crop of seagrass was affected by
if)
     150              1 50                fertilization (Fig. 3). When averaged through time, there
 a1)
LC)
                   10 00                 was a significant difference in the total seagrass standing
     100
U)t   50               50
                                      crop between CONT and FERT treatments (ANOVA,
              *
                                      Treatment main effect, Fl,4 = 10.1, P = 0.03), but when
            *3
            9     99  1 0 O   1 3   51  1
        19831985198719891991      19831985198719891991     averaged across treatments, there were no significant
                                      differences in seagrass standing crop as a function of time
Fig. 2. Trajectoriesthrough time of the standingcrop(in g(dry)       (Time main effect, F8,32= 1.12, P = 0.38). However, there
m-2) of Thalassia testudinum(open circles) and Halodule           was a significant treatment by time interaction (F8,32 =
wrightii(filled circles)at the pairedcontrolandfertilizedsites.       9.8, P < 0.001), indicating that the patternthrough time in
                                      the total seagrass standing crop differed between CONT
                                      and FERT treatments. For the first three years of fertil-
markers.The fertilization led to 20-fold increases in pore-
                                      ization, FERT sites had 2 - 3 fold higher seagrass stand-
water dissolved phosphate concentration, and a 6-fold
                                      ing crops than controls, but from 1987 - 1991, there was
increase in porewater ammonium. Water column nutrient            no difference (Fig. 3).
concentrations were not different between FERT and
CONT sites, owing to the flow of water past the sites.
  After 8 yr of fertilization, the seagrass beds surround-                      Total Seagrass
                                           200 -
ing FERT stakes differed from CONT stakes. While there           N
was no significant difference in the total standing crop of
                                        E
seagrass after the 8 yr, the species composition and the
relative contributions of seagrass species to the total bio-
mass of the beds was very different. Analysis of the             -o

seagrass bed composition around the DISC stakes                   1 00 -
showed that the differences in the seagrass beds caused             0       o.,,,a_         f <,#)..
                                        L-
by fertilization persisted until the end of the experiment          CO
in 1991, even in the absence of continued nutrientinputs.
                                        C   50-
                                        c
                                        0
Fertilized versus control treatments                     cn    0    I  r   I   I   I   I  I   I  I
The species composition of the seagrass beds changed                     1983 1984  1985  1986  1987  1988 1989  1990 1991

markedly at the FERT sites when compared to the con-
trols. At the beginning of the experiments in 1983, mono-          Fig. 3. Total seagrass standingcrop at the fertilized (filled
                                      circles) and control(open circles) sites. Valuesare means+ 1
specific Thalassia testudinummeadows surroundedall of            SE.

352                                                                  OIKOS 72:3 (1995)
              Thalassia  testudinum                       Thalassia    testudinum
      1200                               0.25

      1000                       U)
                                       0.20
N      800
                               a)       0.15
       600                       N
                               U)
       400                       0
                               0
                                       0.10
                                c-
       200                       u)
                               L-       0.05
   -+J      0                     o

   Cn
   ci                                   0.00
   CQ)

               Halodule  wrightii      Fig. 5. Size of shortshoots(g of greenleavespershortshoot)of
   J
   0   9000                       Thalassiatestudinum the FERTsites. N.D. indicatesno data
                                          at
   r-)                           for 1988.Eachvalueis the meanof the 5 site means,+ 1 SE, n =
      7500                       5.
   -c
   Cr)  6000

   0   4500
   0
   6-  3000
   03                                            Thalassia     testudinum
      1500                               150

          0                             125

                                  -N    100
            *  Fertlized   O Control     CN
                               1        75

Fig. 4. Mean short shoot densities (? 1 SE) for Thalassia      E     50
testudinum (top)andHalodulewrightii(bottom) bothcontrol
                      at
and fertilizedsites.
                                        25
                                  L

  The change from Thalassia testudinum-dominatedsea-       -o      0
grass beds to Halodule wrightii-dominated beds occurred         -)
gradually from 1983 to 1991 (Fig. 4). There were signif-
icant differences in the SS density of H. wrightii between
CONT and FERT treatments throughout the experiment
                                  o
(ANOVA, Treatmentmain effect, Fi,4 = 85.7, P = 0.001).       *_    150
Also, averaged across treatments, the density of H.
wrightii changed through time (Time main effect, F7,28  =     0     125
23.8, P < 0.001). At FERT sites, H. wrightii density       U()
                                       100
increased through time, while there was no change at the
controls (Treatmentby Time interaction, F7,28= 23.5, P <      c
                                        75
0.001). A more complicated patternwas evident in the SS       c-
density of T. testudinum during the experiments (Fig. 4).           50
There was an overall effect of the treatmenton T. testudi-     o)
num density when averaged through time (ANOVA,                 25
Treatmentmain effect, Fl,4 = 21.0, P = 0.01). Also, there
                                        0
were significant differences among years averaged across
                                                      :
treatments (Time main effect, F7,28 = 2.4, P = 0.05). The              ,\'     \(  \C^    '\^  \    \,:
density of T. testudinum at FERT sites exhibited a differ-
ent pattern through time than the CONT sites (Treatment                  *  Fertilized         0   Control
by Time interaction, F7,28 = 11.4, P < 0.001). At the FERT
                               Fig. 6. Mean standingcrop (? 1 SE) for Thalassiatestudinum
sites, T. testudinum density remained constant from     (top) andHalodulewrightii(bottom)at bothcontrolandfertil-
1983-1985, and then decreased rapidly from 1985-1991.    ized sites.

23  OIKOS 72:3 (1995)                                                          353
                      L  . T. testudinum  at the controls. Standing crop of H. wrightii increased
                        H H. wrightii    through time when averaged across treatments (Time
   100                              main effect, F8,32= 7.0, P < 0.001), and the trend in
Q_
Q                                 standing crop through time was different for the FERT
                                  sites than the controls (Treatment by Time interaction,
     80
     4
                                     =
                                  F8,32 6.8, P < 0.001).
                                    As with the SS density data (Fig. 4), the pattern in the
                                  standing crop of Thalassia testudinumthrough the exper-
     0                             iment was more complicated than for Halodule wrightii
v,   40
                                  (Fig. 6). Averaged across all years of the experiment,
                                  there was a significant difference in the standing crop of
O    20
     20                             T. testudinum between FERT and CONT sites (ANOVA,
                                  Treatmentmain effect, F,4 = 8.2, P = 0.05), and averag-
     0                             ing both treatments, the change in standing crop of T.
       198319841985198619871988198919901991         testudinumwas significant (Time main effect, F832= 2.5,
                                  P = 0.03). The patterns in standing crop through time
Fig. 7. Average proportion (? 1 SE) of the seagrasses Thalassia   were very different between CONT and FERT treat-
testudinum and Halodule wrightii at the fertilized sites.      ments, however (Treatment by Time interaction, F8,32 =
                                  21.9, P < 0.001). At FERT sites, standing crop of T.
                                  testudinum almost tripled between 1983 and 1984, and
There was no apparentpatternin the density of T. testudi-      then declined steadily between 1984 and 1991. There was
num at the CONT sites.                       no such discernable pattern at the CONT sites.
  Changes in SS density do not completely describe the        The net result of fertilizing the Thalassia testudinum-
change in the species composition of these seagrass beds      dominated seagrass community normally prevalent on
since short shoots of Thalassia testudinum are much         Cross Bank was a change from a T. testudinum-dom-
more massive than those of Halodule wrightii. Averaged       inated meadow to one almost completely composed of
over all of our measurements, T. testudinum shoots aver-      Halodule wrightii (Fig. 7). In 1983, 100% of the total
aged 0.133 + 0.009 g of dry leaves per shoot, compared       seagrass standing crop at the FERT sites was T. testudi-
to 0.013 ? 0.003 for H. wrightii. At the FERT sites, the      num. After only one year of fertilization, H. wrightii
size of T. testudinum shoots was strongly effected by        began growing at these sites, and by 1986, the standing
nutrient additions (Fig. 5). After one year of fertilization,    crop of H. wrightii exceeded T. testudinum. In 1991, H.
the average mass of T. testudinum shoots doubled. As H.       wrightii made up 97% of the total seagrass standing crop.
wrightii became established at the FERT sites and began       In contrast, H. wrightii never comprised more than 2% of
replacing T. testudinum, the size of the remaining short      the standing crop at the control sites, and in 1991,99% of
shoots decreased.                          the total seagrass standing crop at the controls was T.
  The standing crop of Halodule wrightii was strongly       testudinum.
affected by the addition of nutrients in the form of bird
feces to the FERT sites (Fig. 6). Averaged across all the
years of the experiment, there were significant differ-       Discontinuedfertilization
ences between FERT and CONT treatments (ANOVA,
Treatment main effect, F,4 = 28.6, P < 0.01): in all        ANOVA indicated no statistically significant changes in
instances except for the beginning of the experiment, H.      seagrass standing crop and short shoot density between
wrightii standing crop was higher at the FERT sites than      years 1987, 1989, 1990 and 1991 at the DISC sites (Table


Table 1. Characteristics the seagrassbeds fromsites at whichfertilization discontinued 1983. Valuesare means? 1 SE.
           of                        was     in
ANOVAresultsare for repeated  measuresANOVAtestingfor differencesbetweenyears.
Year                 Standingcrop (g(dry)m-2)                Shortshoot density(m-2)
          Thalassia          Halodule       Total        Thalassia      Halodule
          testudinum          wrightii      seagrass      testudinum      wrightii
1987        31.9?16.2          61.2?14.7      93.2?21.3      156? 77       5287?1432
1989        73.6?16.1          47.8+ 5.4     121.4?14.2      380+ 99       3310? 377
1990        71.9?18.3          51.3+18.3     123.2? 8.1      440?128       4795?1483
1991        56.1?17.1          34.8+16.4      90.8? 7.9      460+124       3115? 998
ANOVA
 F2.3         1.6              1.3       16.0         0.5          4.0
 P          0.4              0.5       0.06         0.7          0.2

354                                                      OIKOS 72:3 (1995)
1). The total seagrass standing crop at these sites was    mand for P than H. wrightii; this agrees with the esti-
about equally divided among Thalassia testudinum (34%     mates based on the specific growth rates of the species
- 58% of total) and Halodule wrightii (40% - 66%).      (Fourqurean et al. 1992a). Therefore, T. testudinum
These proportions are similar to what was present at the   should be able to out-compete H. wrightii for nutrients in
FERT sites between 1985 and 1986 (Fig. 6). Assuming      a nutrient-limited environment, which explains why T.
that the 28 months of fertilization from July 1981 to     testudinum dominates the nutrient-limited seagrass beds
November 1983 had the same effect on the surrounding     of Florida Bay. Similarly, Williams (1987, 1990) found
seagrass beds as the fertilization from November 1983 to   that T. testudinum could out-compete Syringodium fil-
October 1986, the seagrass beds at the DISC sites did not   iforme for nutrients in seagrass beds in St Croix, U.S.V.I.
change appreciably between 1983 and 1991.            It is more difficult to explain the dominance of Halo-
                               dule wrightii over Thalassia testudinum under nutrient-
                               enriched conditions than to explain the dominance of T.
                               testudinumover H. wrightii under nutrient-limitedcondi-
                               tions. Once the nutrient limitation of H. wrightii was
Discussion                          released at the fertilized sites, H. wrightii was able to
The development of seagrass beds in south Florida and    colonize the fertilized areas. The decrease in T. testudi-
the Caribbeanis often nutrient, and specifically phospho-  num at the fertilized sites was directly related to the
rus, limited (Short et al. 1985, 1990, Williams 1987,     increase in H. wrightii (Fig. 2). There are at least three
1990, Powell et al. 1989, 1991, Fourqureanet al. 1992a,   possible reasons for the decline of T. testudinum at the
b). Not only is seagrass biomass controlled by nutrient   fertilized sites, including: 1) nutrient enrichment could
availability, but there are documented differences in the  directly inhibit the growth of T. testudinum and not of H.
nutrient availability in seagrass beds dominated by Tha-   wrightii; 2) H. wrightii could have an allelopathic effect
lassia testudinum and Halodule wrightii in Florida Bay   on T. testudinum, or 3) H. wrightii could, in the absence
(Fourqureanet al. 1992a). H. wrightii beds have higher    of nutrient limitation, out-compete T. testudinum for
concentrations of dissolved inorganic phosphorus in the    some other resource (e.g. light).
sediment porewater than T. testudinum beds. This ob-      It does not seem likely that nutrient enrichment di-
served correlation does not prove that H. wrightii beds   rectly suppressed Thalassia testudinum. In Florida Bay,
are restricted to areas of high P concentration, since the  the standing crop of T. testudinum is positively related to
elevated P concentrations may be a consequence of the    P availability (Fourqureanet al. 1992a, b), and in the first
presence of H. wrightii. The experiments described      two years of this experiment T. testudinum was sub-
herein, however, demonstrate that H. wrightii colonizes   stantially enhanced at the fertilized sites compared to the
T. testudinum-dominatedseagrass beds and out-competes    controls (Figs 4-6). T. testudinumdid not decrease at any
T. testudinum when nutrient availability is increased in  of the fertilized sites until after Halodule wrightii became
Florida Bay.                         well established (Fig. 2). Nutrient enrichment has been
  The dominance of Thalassia testudinum in the nutri-   cited as a factor in the decreased standing crop, produc-
ent-limited seagrass beds of Florida Bay can be explained  tivity and persistence of some seagrass beds, however.
by the relative nutrient demands of T. testudinum and    Nutrient availability has been correlated with epiphyte
Halodule wrightii. Using the relative growth rates and the  loads on seagrass leaves (e.g. Sand-Jensen 1977, Silber-
nutrient contents of the two species to estimate relative  stein et al. 1986, Tomasko and Lapointe 1991), and shad-
nutrient demands, Fourqureanet al. (1992a) have shown    ing of seagrasses by epiphytes has been implicated as one
that H. wrightii has a four-fold higher demand for phos-   of the most deleterious effects of eutrophication of sea-
phorus, the limiting nutrient, than T. testudinum.Another  grass habitats (e.g. Bulthuis and Woelkerling 1983, Cam-
method for assessing the relative nutrient demands is    bridge and McComb 1984). Since leaf turn-over is faster
estimating the equilibrium resource requirement, or R*,   for H. wrightii than T. testudinum(unpubl.), it is conceiv-
for each species (Tilman 1982). R* can be approximated    able that fouling of the longer-lived T. testudinum leaves
by the concentration of a resource in the environment    could cause the loss of T. testudinumfrom areas of nutri-
when population sizes reach equilibrium. Assuming that    ent enrichment, but this mechanism was probably not
populations reach equilibrium with respect to nutrient    operative in these experiments. While the epiphyte loads
supply when additional nutrient supply does not cause an   of the seagrasses at fertilized and control sites were not
increase in population size, R* for sediment nutrients in  quantified, there were no visual differences in macro-
Florida Bay seagrass beds can be estimated by the "sat-   phytic or microscopic epiphyte loads at control or fertil-
urating" porewater concentations of nutrients for each    ized sites.
seagrass species. In the case of sedimentary P supply, the    The initial response of T. testudinumto increased nutri-
limiting nutrient for seagrass growth in Florida Bay, R*   ent supply was an increase in the leaf biomass per short
for T. testudinum and H. wrightii are approximately 0.2   shoot (Fig. 5). Increased leafiness is a well-known plant
[M and 0.9 L[MP, respectively (Fourqureanet al 1992a).    response to shading, and there is some evidence that T.
Since R* for T. testudinum is substantially lower than R*  testudinummay respond to decreased light availability by
for H. wrightii, T. testudinum should have a lower de-    increasing shoot size (Dawes and Tomasko 1988). In our

23* OIKOS 72:3 (1995)                                                355
experiment, however, T. testudinum shoot size decreased    fertilization. The loss of nutrients from the system over 8
after 1984, as light availability continued to decrease    yr was not great enough to draw the availability below the
concomitantly with increases in H. wrightii biomass. This   threshold value for Halodule wrightii survival. Since sea-
suggests that the initial increase in T. testudinum shoot   grass beds do lose some nutrients due to diffusion from
size was a response to increased nutrient availability, not  the sediments and leaf loss, it is inevitable that this will
decreased light availability.                 eventually happen, however.
  Allelopathic effects have been documented as impor-      Succession can be viewed as the change in species
tant controls over interspecies interactions in some ter-   composition through time caused by changing resource
restrial environments (see Rice 1974). It is unlikely that   availabilities due to the impacts of organisms on the
Halodule wrightii has any allelopathic effect on Thalas-    environment (Pickett 1976, Tilman 1987), and the ability
sia testudinum, since there are many locations where H.    of an organism to utilize resources may in large part
wrightii exists as an understoryin predominantly T. testu-   determine its role in succession. In the original formula-
dinum seagrass beds (pers. obs.).               tion of the resource-ratio hypothesis, Tilman (1985,
  The most likely cause of the dominance of Halodule      1988) hypothesized that early successional species
wrightii over Thalassia testudinum at the fertilized sites   should have lower R* values for nutrients and be more
is direct competition for light between the two species.    competitive for nutrients than late successional species.
Under the fertilized treatment, H. wrightii developed a    This observation was directly at odds with many observa-
long and dense canopy, with numerous "aerial runners",     tions, however: one of the generalized patternsin changes
or apical rhizomes extending 20-30 cm into the water      in plant physiological ecology during succession is a
column. From distributionalevidence (Phillips 1960, Wi-    change from high to low resource demands (Bazzaz
ginton and McMillan 1979, Iverson and Bittaker 1986) it     1979). In later work, Tilman and Wedin (1991a, b) re-
is apparent that T. testudinum has a higher light require-   evaluated this facet of resource ratio theory and found
ment than H. wrightii. The dense canopy of H. wrightii at   that, contrary to earlier predictions, early successional
the fertilized sites probably interruptedsufficient light so  grasses have higher R* values than late successional
that T. testudinum could no longer maintain a positive     grasses. Tilman now considers early successional species
carbon balance, leading to the extirpation of T. testudi-   to have an edge over later successional species due to
num at those stations.                     their rapid colonizing rates (Gleeson and Tilman 1990,
  The resource-ratiotheory of plant community structure    Tilman and Wedin 1991a), which agrees with many other
(Tilman 1982, 1988) predicts that experimentally manip-    assessments of early successional dynamics (e.g. Platt
ulated plots that receive the same supply of limiting      1975, Connell and Slayter 1977, Bazzaz 1979). Early
resources should become similar in species compositon,     succession in Florida Bay seagrass beds also fits this
or converge on similar communities, through time. The     model. Halodule wrightii, the normal early successional
convergence of plant communities receiving the same      species, has a lower competitive ability for sediment
resource supplies is dependent on the historical composi-   nutrients than Thalassia testudinum, the later succes-
tion of the communities, however (Inouye and Tilman      sional species, but a potentially much faster colonization
1988). Similarly, the outcome of the manipulations      rate than T. testudinum. H. wrightii has a much higher
should depend on the availablity of propagules of species   vegetative reproduction rate than T. testudinum (Tom-
favored by the manipulation. In the fertilization experi-   linson 1974, Fonseca et al. 1987), and sexual reproduc-
ments presented here, Halodule wrightii was clearly fa-    tion is potentially more important in the spread of H.
vored by fertilization. Fertilized sites eventually con-    wrightii than T. testudinum (Williams 1990). H. wrightii
verged on similar, H. wrightii-dominated seagrass beds,    has a higher flowering rate than T. testudinum (Williams
but the trajectories of the individual sites was dependent   1990). H. wrightii seeds form a seed bank in sediments of
on the colonization of the sites by H. wrightii (Fig. 2). In  seagrass beds (McMillan 1981, 1983), and the seedling
the absence of H. wrightii, Thalassia testudinumbiomass    success of T. testudinum is very low (Williams and Adey
stayed elevated over control areas, but following the      1983).
eventual colonization of the sites by H. wrightii, T. testu-   The replacement of Thalassia testudinum by Halodule
dinum declined. The stochastic event of H. wrightii colo-   wrightii at the fertilized sites was in contrast to the nor-
nization therefore controlled the response of Florida Bay   mal successional sequence in seagrass beds in south Flor-
seagrass beds to manipulations in resource supply rates.    ida and the Caribbean.Under non-enriched conditions, H.
  The changes caused by fertilization of seagrass beds in   wrightii is commonly the early successional, colonizing
Florida Bay persisted for at least 8 yr after the fertil-   species and T. testudinum is the late-successional, "cli-
ization was discontinued (Table 1). The primarysource of    max" species (den Hartog 1971). Fertilization of other
nutrientsfor seagrass growth in unfertilized seagrass beds   plant communities can also lead to the establishment of
is the remineralization of organic matter in the sediments   communities resembling early successional states. For
(Patriquin 1972, Capone and Taylor 1980, Short 1987).     example, in an old-field fertilization experiment Carson
The lack of change at the sites where fertilization was    and Barrett (1988) found that nutrient enrichment of
discontinued suggests that seagrass beds are very effi-    late-successional fields led to the establishment of plant
cient at retaining and recycling nutrients acquired during   communities dominated by summer annuals with high

356                                                    OIKOS 72:3 (1995)
 photosynthetic rates and high relative growth rates. The     dependent on the duration of the fertilization of the sea-
resultant communities resembled earlier stages of sec-      grass beds. Increased nutrient availability caused a dou-
ondary succession. Similarly, McLendon and Redente        bling of the Thalassia testudinumleaf biomass over con-
(1991) noted that fertilization of a sagebrush steppe com-    trols for the first two years of this experiment; and were it
munity allowed early-successional annuals to persist as     to have ended at that time we would have concluded that
community dominants, and they concluded that the dom-      increased nutrient supply to Florida Bay seagrasses
inance of a site by annuals during the early stages of      would cause an increase in the biomass of the late succes-
secondary succession is related to high nutrient availabil-   sional seagrass T. testudinum.The true outcome of such a
ity. Succession in plant communities is dependent on the     change in nutrient supply rates was dependent on the
temporal pattern in the availability of nutrients. Increased   colonization of these fertilized, and therefore newly suit-
nutrientavailability may alter the trajectoryof succession    able, areas by the early successional seagrass Halodule
by allowing plant species adapted to high nutrient envi-     wrightii. This time-dependent result underscores the im-
ronments to displace established species (Grime 1979). In    portance of designing field experiments of the proper
areas of high nutrient availability in Florida Bay, H.      duration to capture the dynamics of the system being
wrightii will be the dominant late successional species,     studied.
while T. testudinum will be the dominant late-succes-
sional species in areas of low nutrient availability.                -
                                 Acknowledgements This researchwas fundedin partby the
  We propose that the change in species dominance from     JohnD. andCatherine MacArthur
                                            T.           and
                                                   Foundation, through a
Thalassia testudinum to Halodule wrightii was caused       cooperative agreement betweenthe U.S. NationalParkService
                                 and the Univ. of Virginia(CA-5280-0-9009).We thank H.
directly by a change in the supply rates of light and soil         L.
                                 McCurdy, Lagera,R. Zieman,K. Halamaand R. Bjorkfor
nutrients. This shifted the outcome of competition be-      help with the field work. We thank the administration and
tween the two seagrass species. We have interpretedthese     rangersof EvergladesNational Park for their toleranceand
results to be consistent with the resource ratio hypothesis   logisticalassistance
                                           withthis long-termstudywithinthepark.J.
                                 P. Grime,J. Dooley, R. Price, D. Tomaskoand R. Chambers
(Tilman 1982, 1985, 1987, 1988), which asserts that       providedcommentsthatgreatlyimproved paper.
                                                     this
competition is the main determinant of vegetation dom-
inance in both nutrient-rich and nutrient-poor environ-
ments. In contrast, the triangularmodel of plant strategies
(Grime 1974, 1977, 1979) holds that the relative impor-
tance of competition decreases in nutrient-poorenviron-     References
ments, where the ability of plant species to weather stress   Bazzaz,F. A. 1979.The physiological   ecology of plantsucces-
becomes the primary determinant of vegetation. Experi-        sion. - Annu.Rev. Ecol. Syst. 10: 351-371.
ments have shown that some aspects of competition do       Bulthuis,D. A. andWoelkerling, J. 1983. Effectsof in situ
                                                   W.
                                        and
                                   nitrogen phosphorus    enrichment the seagrass
                                                      of       Hetero-
indeed decrease in intensity with an increase in stress       zostera tasmanica(Martensex Aschers.) den Hartog in
(Campbell and Grime 1992), and a simulation model of        Western              -
                                        Port,Victoria,Australia. J. Exp. Mar.Biol. Ecol.
succession based on the triangularmodel has been shown        53: 193-207.
to produce results consistent with successional theory            M.
                                 Cambridge, L. and McComb,A. J. 1984. The loss of sea-
                                   grassesin Cockbur Sound,Western         I.
                                                      Australia. The time
(Colasanti and Grime 1993). An alternative interpretation      course and magnitudeof seagrass decline in relationto
of the results of these experiments, consistent with the      industrial        -
                                         development. Aquat.Bot. 20: 229-243.
triangularmodel, ascribes the dominance of T. testudinum     Campbell, D. andGrime,J. P. 1992.An experimental of
                                       B.                      test
over H. wrightii in oligotrophic Florida Bay to a conse-       plantstrategytheory.- Ecology 73: 15-29.
                                 Capone,D. G. and Taylor,B. F. 1980. Microbialnitrogency-
quence of the low nutrient demand of T. testudinum          cling in a seagrasscommuity.- In: Kennedy,V. S. (ed.),
caused by slow growth and efficient retention of retained      Estuarineperspectives.Academic Press, New York, pp.
nutrients compared to H. wrightii. In other words, T.         153-162.
testudinum is more tolerant of the stress of low nutrient     Carson,W. P. and Barrett, W. 1988. Successionin old-field
                                               G.
                                   plantcommunities:  effects of contrasting types of nutrient
availability than H. wrightii. The triangularmodel works              -
                                   enrichment. Ecology 69: 984-994.
well if we consider only one kind of stress, in this case     Chapin,F. S. III. 1980. The mineralnutrition wild plants.-
                                                         of
nutrient limitation; but becomes cumbersome once light        Annu.Rev. Ecol. Syst. 11: 233-260.
stress is also considered, because light stress and nutrient   Colasanti, L. andGrime,J. P. 1993. Resource
                                       R.                   dynamicsand
stress do not act in concert in aquatic environments.        vegetationprocesses:a deterministic   model using two-di-
                                   mensionsal  cellularautomata. - Funct.Ecol. 7: 169-176.
Often, light availability and nutrient availability are in-    Connell,J. H. and Slayter,R.O. 1977. Mechanisms succes-
                                                            of
versely correlated. For nutrients, T. testudinum is clearly     sion in naturalcommunitiesand their role in community
the better competitor; but it is also clear that H. wrightii is                 -
                                   stabilityand organization. Am. Nat. 111: 1119-1144.
a better competitor for light. In this case, the tradeoffs    Dawes, C. J. and Tomasko,D. A. 1988. Depthdistribution    of
                                   Thalassiatestudinum two meadowson the west coast of
                                              in
made between accumulation of light and accumulation of                                  -
                                   Florida;a differencein effect of light availability. Mar.
nutrients, as described by the resource ratio hypothesis,      Ecol. 9: 123-130.
determines the behavior of T. testudinum and H. wrightii     den Hartog,C. 1971. The dynamicaspect in the ecology of
                                               -
                                   seagrasscommunities. Thalassia    Jugosl.7: 101-112.
in Florida Bay.
                                 Fonseca,M. S., Thayer, W. andKenworthy, J. 1987.The
                                             G.           W.
  Interpretation of the results of this experiment was       use of ecological data in the implementation manage-
                                                          and

OIKOS 72:3 (1995)
                                                              357
   ment of seagrass restorations. - In: Durako, M. J., Phillips,    tropical estuary: observational and experimental evidence. -
   R. C. and Lewis, R. R. III (eds), Proceedings of the sympo-     Estuarine Coastal Shelf Sci. 32: 567-579.
   sium on subtropical seagrasses of the southeastern United    Rice, E. L. 1974. Allelopathy. - Academic Press, New York.
   States. Florida Marine Research Publications No. 42., Flor-   Sand-Jensen, K. 1977. Effect of epiphytes on eelgrass photosyn-
   ida Dept of Natural Resources, St. Petersburg, FL, pp. 175-     thesis. - Aquat. Bot. 3: 55-63.
   188.                              Short, F. T. 1987. Effects of sediment nutrients on seagrasses:
Fourqurean, J. W., Zieman, J. C. and Powell, G. V. N. 1992a.       literature review and mesocosm experiment. - Aquat. Bot.
   Relationships between porewater nutrients and seagrasses in     27: 51-57.
   a subtropical carbonate environment. - Mar. Biol. 114:      -, Davis, M. W., Gibson, R. A. and Zimmerman, C. F. 1985.
   57-65.                                Evidence for phosphorus limitation in carbonate sediments
 - , Zieman, J. C. and Powell, G. V. N. 1992b. Phosphorus        of the seagrass Syringodium filiforme. - Estuarine Coastal
   limitation of primary production in Florida Bay: evidence      Shelf Sci. 20: 419-430.
   from the C: N: P ratios of the dominant seagrass Thalassia    -, Dennison, W. C. and Capone, D. G. 1990. Phosphorus-
   testudinum. - Limnol. Oceanogr. 37: 162-171.             limited growth of the tropical seagrass Syringodium fil-
Gleeson, S. and Tilman, D. 1990. Allocation and the transient       iforme in carbonate sediments. - Mar. Ecol. Prog. Ser. 62:
   dynamics of succession on poor soils. - Ecology 71: 1144-       169-174.
   1155.                              Silberstein, K., Chiffings, A. W. and McComb, A. J. 1986. The
Grime, J. P. 1974. Vegetation classification by reference to       loss of seagrasses in Cockbum Sound, Western Australia.
   strategies. - Nature 250: 26-31.                   III. The effect of epiphytes on productivity of Posidonia
 - 1977. Evidence for the existence of three primary strategies     australis Hook. F. - Aquat. Bot. 24: 355-371.
   in plants and its relevance to ecological and evolutionary   Tilman, D. 1982. Resource competition and community struc-
   theory. - Am. Nat. 111: 1169-1194.                  ture. - Princeton Univ. Press, Princeton, NJ.
 - 1979. Plant strategies and vegetation processes. - Wiley,     - 1985. The resource ratio hypothesis of succession. - Am.
   New York.                              Nat. 125: 827-852.
Harper, J. L. 1977. Population biology of plants. - Academic      - 1987. On the meaning of competition and the mechanisms of
   Press, London.                            competitive superiority. - Funct. Ecol. 1: 304-315.
Inouye, R. S. and Tilman, D. 1988. Convergence and divergence     - 1988. Plant stategies and the dynamics and structureof plant
   of old-field plant communities along experimental nitrogen      commuities. - Princeton Univ. Press, Princeton, NJ.
  gradients. - Ecology 69: 995-1004.                 - and Wedin, D. 1991a. Dynamics of nitrogen competition
Iverson, R. L. and Bittaker, H. F. 1986. Seagrass distribution in     between successional grasses. - Ecology 72: 1038-1049.
  the eastern Gulf of Mexico. - Estuarine Coastal Shelf Sci.     - and Wedin, D. 1991b. Plant traits and resource reduction for
   22: 577-602.                             five grasses growing on a nitrogen gradient. - Ecology 72:
McLendon, T. and Redente, E. F. 1991. Nitrogen and phospho-        685-700.
  rus effects on secondary succession dynamics on a semi-arid   Tomasko, D. A. and Lapointe, B. E. 1991. Productivity and
  sagebrush site. - Ecology 72: 2016-2024.               biomass of Thalassia testudinum as related to water column
McMillan, C. 1981. Seed reserves and seed germination for two      nutrient availability and epiphyte levels: field observations
  seagrasses, Halodule wrightii and Syringodium filiforme       and experimental studies. - Mar. Ecol. Prog. Ser. 75: 9-17.
  from the western Atlantic. - Aquat. Bot. 11: 279-296.      Tomlinson, P. B. 1974. Vegetative morphology and meristem
- 1983. Seed germination in Halodule wrightii and Syringo-       dependence - the foundation of productivity in seagrasses. -
  dium filiforme from Texas and the U.S. Virgin Islands. -       Aquaculture 4: 107-130.
  Aquat. Bot. 15: 217-220.                     Wiginton, J. R., and McMillan, C. 1979. Chlorophyll composi-
Patriquin,D. G. 1972. The origin of nitrogen and phosphorus for     tion under controlled light conditions as related to the distri-
  the growth of the marine angiosperm Thalassia testudinum.      bution of seagrasses in Texas and the U.S. Virgin Islands. -
  - Mar. Biol. 15: 35-46.                       Aquat. Bot. 6: 171-184.
Phillips, R. C. 1960. Observation on the ecology and distribu-    Williams, S. L. 1987. Competition between the seagrasses Tha-
  tion of the Florida seagrasses. - Professional papers series     lassia testudinum and Syringodiumfiliforme in a Caribbean
  No. 2, Florida State Board of Conservation, Tallahassee, FL.     lagoon. - Mar. Ecol. Prog. Ser. 35: 91-98.
Pickett, S. T. A. 1976. Succession: an evolutionary interpreta-    - 1990. Experimental studies of Caribbeanseagrass bed devel-
  tion. - Am. Nat. 110: 107-119.                    opment. - Ecol. Monogr. 60: 449-469.
Platt, W. J. 1975. The colonization and formation of equilibrium   - and Adey, W. H. 1983. Thalassia testudinum Banks ex
  plant species associations on badger mounds in a tall-grass     Konig seedling success in a coral reef microcosm. - Aquat.
  prairie. - Ecol. Monogr. 45: 285-305.                Bot. 16: 181-188.
Powell, G. V. N. 1987. Habitat use by wading birds in a sub-     Winer, B. J. 1971. Statistical principles in experimental design,
  tropical estuary: implications of hydrography. - Auk 104:      2nd ed. - McGraw-Hill, New York.
  740-749.                             Zieman, J. C. 1982. The ecology of seagrasses of south Florida:
  , Kenworthy, W. J. and Fourqurean, J. W. 1989. Experi-        A community profile. - U.S. Fish and Wildlife Service Biol.
  mental evidence for nutrient limitation of seagrass growth in    Rep. OBS-82/25. U.S. Fish and Wildlife Service, Washing-
  a tropical estuary with restricted circulation. - Bull. Mar.     ton.
  Sci. 44: 324-340.                         - , Fourqurean,J. W. and Iverson, R. L. 1989. The distribution,
-, Fourqurean, J. W., Kenworthy, W. J. and Zieman, J. C.        abundance and productivity of seagrasses in Florida Bay. -
  1991. Bird colonies cause seagrass enrichment in a sub-       Bull. Mar. Sci. 44: 292-311.




358                                                          OIKOS 72:3 (1995)