MARINE ECOLOGY PROGRESS SERIES
  Vol. 138: 219-231.1996                                           Published July 25
                             Mar Ecol Prog Ser




   Seagrass responses to long-term light reduction
   by brown tide in upper Laguna Madre, Texas:
      distribution and biomass patterns
                          Christopher P. Onuf*
     National Biological Service, Southern Science Center, 6300 Ocean Drive, Corpus Christi, Texas 78412, USA




       ABSTRACT- A brown tide caused by a very dense bloom of an as yet undescribed species of the new
       class Pelagophyceae was first reported in upper Laguna Madre, Texas, USA, in June 1990 and has
       been there continuously through December 1995. No change in response to reduced light was evident
       in the distribution of the seagrass Halodule wrightii along transects sampled before the brown tide in
       1988 and resampled after initiation of the brown tide in 1991 and 1992; however, in winter 1993-94
       losses were documented over 2.6 km2 of bottom and by winter 1994-95 the area of vegetation lost had
       more than tripled to 9.4 km2 Changes in biomass presaged the changes in distribution. Decreases in
       biomass at depths >1.4 m were evident 2 yr before bare areas were detected. Reductions in biomass
       were more pronounced toward the south, in keeping with a gradient of increasing light attenuation
       from north to south. Support of a hminishing number of new shoots by reclamation of nutrients and
       stored reserves from senescing shoots and rhizomes may allow H. wrightii to persist under conditions
       of insufficient light for periods greatly in excess of the life span of any one shoot. This postulated capa-
       bility would account for the pattern of diminishing biomass over time where the seagrass persists in
       deeper areas and the long lag between light reduction and change in distribution where the seagrass
       succumbed.

       KEY WORDS: Distribution . Biomass . Seagrass . Halodule wrightii . Light . Irradiance . PAR . Brown
       tide . Subtrop~cal Texas



            INTRODUCTION                  tions, has occurred gradually over an extended period,
                                   has been accompanied by many structural and hydro-
 Clear water is increasingly recognized as a key req-        logic changes of the coastal environment, and has
uisite for the development and maintenance of healthy         occurred with little or no documentation of conditions
seagrass meadows, and conversely, reductions in            before losses were noticed. Consequently, the connec-
water clarity have been implicated in large-scale           tion between seagrass loss and water clarity can be dif-
losses of seagrass (Kenworthy & Haunert 1991). The          ficult to document.
causes of reduced water clarity range from nutrient           In contrast to a gradual, anthropogenically driven
enrichment (Costa 1988, Lewis 1989, Pulich & White          change, the advent of a brown tide in upper Laguna
1991, Batiuk et al. 1992, Dennison et al. 1993), to          Madre, Texas, USA, in June 1990 resulted in almost
increased suspended loads resulting from hydrological         instantaneous light reduction that has persisted to
alteration (Giesen et al. 1990) and frequent resuspen-        December 1995. Also, unlike many locations suffering
sion of dredge deposits (Onuf 1994).In most cases, the        diminished water clarity and seagrass loss, antecedent
process of water clarity loss and seagrass decline has        conditions were well documented. Seagrass distribu-
been the result of anthropogenic inputs and modifica-         tion and biomass had been assessed in 1988 (Quam-
                                   men & Onuf 1993),and a multidisciplinary study of the
'Present address: National Biological Service, Midwest Sci-
                                   upper lagoon had been under way for a year when the
ence Center. 6300 Ocean Drive, Corpus Christi, Texas         brown tide began, and was continued for 3 yr after
78412, USA. E-mail: chris-onuf@nbs.gov                (Stockwell et al. 1993, Dunton 1994). These unusual

Q lnter-Research 1996
Resale o f full article not permitted
                      Mar Ecol Prog Ser 138: 219-231, 1996




circumstances lend themselves to a particularly strong
assessment of effects of reduced light on seagrass
meadows. The abrupt and persistent reduction in light
by the phytoplankton bloom is more akin to the manip-
ulative field experiments of Backman & Barilotti (1976)
and Dennison & Alberte (1982) than to the inferred re-
constructions necessary in most trend analyses. How-
ever, the change of the light regime is on the scale of
the whole ecosystem, not a tiny fragment.
  The effect of the brown tide on the light regime of La-
guna Madre was abrupt and large and of unprece-
dented persistence [Stockwell et al. 1993). Prior to the
initiation of the brown tide, upper Laguna Madre was
renowned for the clarity of its waters (Pulich 1980). In
the 13 mo leading up to the beginning of the brown tide
in June 1990, chlorophyll concentrations never
reached as high as 20 pg I-'. In the next 11 mo, chloro-
phyll concentrations reached 90 pg 1-' and seldom fell
as low as 20 pg I-' (Stockwell et al. 1993, their Fig. 2).
The brown tide alga, an undescribed species in the
newly recognized class Pelagophyceae (DeYoe & Suttle
1994) was not seen before June 1990 but exceeded 106
cells ml-' thereafter. Light transmission through the top
1 m of the water column dropped from a mean of 47 %
the year before the brown tide to 19% the first year of
the brown tide (calculated from Stockwell et al. 1993,
their Fig. 2). Continued sampling at one site documents
that the influence of the brown tide persists. Annual to-
tal irradiance reaching the seagrass canopy in the 5 yr
since the start of the brown tide has ranged from 33 to    Fig. 1 Map of south Texas coastal region showing location of
                                study area in the northern part of upper Laguna Madre (USA)
54 % of what it had been the year before the brown tide
began (Dunton 1994, pers. comm.).That the brown tide
is largely responsible for the light reduction is indicated   Laguna Madre of Texas north of Baffin Bay (Fig. l ) ,the
by a highly significant ( p < 0.001, r2 = 0.60) relationship  part of the lagoon in which the brown tide was most
between monthly measures of diffuse attenuation coef-      prevalent. A survey used to determine the status of sea-
ficient and chlorophyll concentration (Dunton 1994).      grasses in Laguna Madre in 1988 (Quammen & Onuf
  Here, I report an assessment of the spatial pattern     1993, Onuf 1996) provided an assessment of seagrass
and time course of effects of light attenuation by the     distribution and biomass-depth relations before the
brown tide on seagrass distribution and biomass         brown tide. Sampling transects generally ran perpen-
afforded by resampling seagrasses in 1991, 1992, 1993     dicular from shore either west or east to the Gulf Intra-
and 1994 at the same time of year along the same tran-     coastal Waterway (Fig. 2). Dredge deposits on one side
sects as were sampled in 1988. In addition, I predict the   of the waterway or the other prevented continuous
ultimate extent of seagrass loss owing to light reduc-     transects across the whole lagoon. Intervals between
tion by brown tide by integrating reports of minimum      transects averaged 5 km. Sampling stations were l 0 0 to
light requirements for Halodule wrightii (Kenworthy et     400 m apart, depending on location and proximity to a
al. 1991, Onuf 1991, Dunton 1994, this study) with       boundary, along 17 transects. Positions were deter-
measurements of the underwater light regime and        mined by LORAN C or by dead reckoning in 1988, by
depth in different parts of the lagoon.            LORAN C in 1991 and by Global Positioning System
                                (GPS) in 1992, 1993, and 1994. Two transects were
                                added to the sampling array in 1991 to provide more
            METHODS                 detailed coverage of deeper parts of the lagoon, where
                                effects of llght reduction by brown tide were expected
 Distribution. Observations to detect effects of light    to be most strongly expressed. All sampling was carried
attenuation by brown tide on a seagrass meadow dom-      out in October and November, except that the 1992
inated by Halodule wrightii were made in the upper       sampling was not completed until 8 January 1993.
                   Onuf. Seagrass loss in response to llght reduction                    221




 Four 80 cm2 by 15 cm deep cores with plants were       middle of the study area (Fig 3). The difference
collected at each station 2.5 m apart along the port      between the mean depth of all stations on a transect
side of the boat. The time and depth were recorded at      in 1988, before installation of the tide gauge, and the
each, and depths for 1991, 1992, 1993 and 1994 sur-       mean of the depths corrected to MSL for the same
veys were standardized by adjusting measured depth       LORAN coordinates in 1991 were used to refer 1988
by the deviation from mean sea level (MSL) at sam-       depths to MSL.
pling time for the Texas Coastal Ocean Observation
Network tide gauge at Bird Island, located near the




                                      SEAGRASS LOST1993           WLAND


    -   TRANSECTS SAMPLED 1991-94
    IIII~II~~


        TRANSECTS SAMPLED ALL YEARS
                                 m     SEAGRASS LOST 1994
                                                    W
    ----  GULF !NTRACOASTAL WATERWAY            R g 3. Map s h o w ~ n g location of light monitors, tide gauge and
                                areas of seagrass cover lost durlng the brown tlde Light mon-
                                itors are designated as in the text and Fig 6 Areas a r e num-
Fig 2 Map of study area showlng location of transects sam-   bered ( d l 4 4 ) as in the text and in Table I Dashed line indi-
         pled ~n different years               cates the course of the Gulf Intracoastal Waterway
222                    Mar Ecol Prog Ser 138: 219-231, 1996




  Cores were washed on 1 mm screens, the retained      1991 vs 1993 and 1992 vs 1993 for each depth class to
plant material identified, and the dominant and other    determine whether there was a cumulative effect over
contributors to cover recorded. Occurrence data were     the whole period of the brown tide and whether effects
plotted on maps to depict the distribution of sea-      could be discriminated over shorter periods, up to the
grasses.                           last year for which biomass determinations were avail-
  In 1993 and 1994, the edges of bare areas were      able. The expectation was that if light attenuation
defined to <0.01' of longitude or latitude by repeatedly   resulting from brown tide is affecting biomass, it will
halving the interval between the last station where     be manifested in reduced biomass in later years in the
seagrass was encountered and the first station along     deeper depth classes. Other differences might suggest
the same transect that was bare (4 bare core samples     other causes.
and no seagrass rooted material pulled up on the        Light. Underwater photosynthetically active radia-
anchor at that location). When vegetated and bare      tion (PAR, 400 to 700 nm) was measured at 3 locations
samples were 0.01' or less apart, a stake was driven at   (Fig. 3): Stn L1,just inside the outer boundary of a
the outermost vegetated station. These locations were    meadow toward the south end of the study area
also marked with a plastic line-float attached by a     (1.66 m MSL, 27" 21.80' N, 97" 22.10' W); Stn L2, 200 m
stainless steel cable secured to a screw-in anchor in    shoreward of the boundary location (1.52 m MSL, 27"
some cases, because stakes sometimes disappeared       21.80' N, 97" 21.96' W); and Stn L3, in a deep, continu-
between visits. Similar sampling was conducted be-      ously vegetated area near the middle of the study area
tween the regularly sampled transects and along the     (1.91 m MSL, 27" 30.93' N, 97" 19.53' W). Underwater
long axis of the bare areas to delineate the bare areas   PAR measurements were made at 1 min intervals and
more closely. Differences in the location of the outer    integrated every hour on a continuous basis using an
boundary between observations were determined by       LI-193SA spherical quantum sensor inputting to an LI-
plotting on maps or were measured with a fiberglass     1000 datalogger (LI-COR, Lincoln, NE, USA). The sen-
tape. In January and February 1995, the locations of all   sor was positioned at canopy level, the top of the sen-
surviving boundary markers were determined using       sor 25 cm above the bottom. The sensor was wrapped
differential GPS. In most cases, there was no ambigu-    in transparent plastic wrap that was replaced at 1 or
ity as to what was meadow and what was not. All       4 wk intervals, depending on season, to minimize foul-
samples at a station were either vegetated or bare.     ing. The periods of record were May 1993 to August
Patchy stations were mostly limited to a 20 m band at    1994 for Stns L1 and L2 and October 1993 to August
the outer edge.                       1994 for Stn L3. Daily total fluxes of underwater PAR
  Biomass. The retained material from 2 of the 4 cores   were referred to daily total fluxes of incident PAR as
from each station, randomly chosen by coin toss, was     measured with a LI-19OSA 2rc sensor mounted on top of
placed in plastic bags and returned to the laboratory     a building at Port Aransas, Texas (27" 52' N, 97" 03' W)
on ice, where the samples were frozen until processed.    by K. Dunton, University of Texas.
Processing consisted of thawing and separating into       The spatial pattern of light attenuation in the lagoon
live (turgid green and white to beige structures) and    was evaluated at approximately monthly intervals
dead (flaccid brown to washed-out maroon) fractions.     from March 1992 to November 1994 with a 20 cm
The live fraction was sorted further according to spe-    diameter Secchi disc. Measurements were made and
cies and into aboveground (green portions of shoots)     depth recorded at stations -100 m from the eastern and
and belowground (root, rhizome, and unpigmented       western shores of the lagoon and at the midpoint on
portions of shoots) fractions. The sample fractions were   east-west transects at 27" 204,22', 26', 30', 34', 38', and
dried to constant weight at 60°C (72 h), weighed,      40'. All Secchi depth determinations were made by the
ashed at 530°C for 3 h, and weighed again. Dry weight    same observer outside the shadow of the boat and
and ash-free dry weight were calculated for all plant    were the means of the depths of disappearance of the
parts and dead material and expressed on a per m2      disk on descent and reappearance on ascent. Secchi
basis.                            depths were related to PAR at depth by simultaneously
  Biomass samples were separated into depth classes     measuring Secchi depths and determining the percent
to determine whether light attenuation resulting from    of surface irradiance (SI) reaching Secchi depth with
the brown tide affected biomass. Depth classes were     an LI-193SA spherical quantum sensor mounted on a
defined to yield a sample size of at least 10 in any year  lowering frame inputting to an LI-1000 datalogger on
for statistical comparisons between years: <85, 85-1 15,   22 June, 12, 13, 31 October, and 2, 3, 4, 7, 8 November
115-130, 130-140, and 2140 cm depths. Variances       1994. Hourly wind data were obtained from Blucher
were not equal between years regardless of transfor-     Institute, Texas A&M University, Corpus Christi,
mation. Consequently, Mann-Whitney U tests were       Texas, for the Bird Island station of the Texas Coas-
performed on pair-wise comparisons for 1988 vs 1993,     tal Ocean Observation Network (Fig. 3) to interpret
                   Onuf: Seagrass loss in response to light reduction                 223




large differences in light attenuation for small Secchi     depths were measured was then conlputed as the long-
depths. Conditions were classified as calm for winds      term measure of available light at different depths in
c24 km h-' (15 miles h-') at the time of light and Secchi    different parts of the lagoon. An estimate of 15% of
measurements and for protected locations (within        surface light reaching canopy level, near the midpoint
200 m of shore on the lee side with respect to prevail-     of the published range for the minimum light require-
ing wind) regardless of wind speed. Conditions were       ment of Halodule wrjghtii (Kenworthy et al. 1991, Onuf
classified as rough at exposed locations when wind       1991, Dunton 1994), was then used to predict the ulti-
speed was >24 km h-'                      mate extent of loss of seagrass likely to result from the
  The frequency of hourly observations of winds        prolonged occurrence of the brown tide.
>24 km h-' from 1 October 1993 to 17 October 1995
was assessed to determine whether high light attenua-
tion associated with rough water was likely to differ                   RESULTS
between the November to April period of frequent
frontal passage and the May to October period of pre-                   Distribution
vailing southeasterly breezes. Winds >24 km h-' were
further categorized by direction according to 90" sec-         No change in seagrass distribution was evident
tors centered on the long axis of upper Laguna Madre        between surveys of 1988 and 1991 or 1992, despite
or at right angles to the long axis. The fetch of the        large reductions in light reaching the bottom in upper
winds aligned with the long axis was greater than for        Laguna Madre after initiation of the brown tide in
winds oriented cross-wise and presumably promoted          June 1990 (Stockwell et al. 1993). These conditions
the development of rougher seas.                  have persisted at least through December 1995 (Dun-
  These relations of % S1 reaching Secchi depth were        ton 1994, pers. comm.). The first evidence of distribu-
then used to compute diffuse attenuation coefficients        tional change came from installation of a light moni-
corresponding with Secchi depths. The attenuation          tor just inside the boundary of the seagrass meadow
coefficients were applied to bathymetric profiles at        near the south end of the study area in May 1993. In
intervals of 0.1' longitude along transects at intervals of     November 1993, the outer boundary was 30 m land-
1' latitude to generate estimates of the proportion of       ward of the monitor (Fig. 3: Area #3). Elsewhere, bare
surface light reaching the bottom according to the         areas were encountered in November 1993 on 3 tran-
Beer's law relation:                        sects at stations that had been vegetated in 1992
                                  (Fig. 3: Areas # l and #2).In aggregate, 2.6 km2 of sea-
              Iz/Io = e-kz
                                  grass meadow had been lost between observations
where I, is photon flux density (pm01 photons m-' S-')       (Table 1).
at depth z, I. is photon flux density at the surface, k is       Boundary locations marked in November and
diffuse attenuation coefficient (In m-'), and z is depth      December 1993 were reexamined in December 1994
(m).The mean of these values for all dates that Secchi       and January-February 1995. Boundaries had receded
                                           from 50 to 800 m . In January 1995,
Table 1. Statistics on extent of loss of seagrass cover in upper Laguna Madre    Area   in the       the lagoon
(Texas, USA) since the advent of the brown tide. Area numbers ( # l 4 4 ) are as   was 8 km long and on average 0.8 km
                in the text and Fig. 3                wide (Fig. 3). On the other side of the
                                           Gulf Intracoastal Waterway, Area #2
Area    Width of meadow lost ( m )    Length Area    Number of       extended 5 km, constricted by dredge
     Mean M~nimum Maximum         (m)  (km2) determinations of    disposal areas. The outer boundaries
                               outer boundary
                                           for Areas #3 and #4 In the south had
 November 1992 or May 1993 to November 1993                     retreated 140 m on average (Fig. 3).
 #l   330    260      550    5100   1.7     11        Over the whole period, 9.4 km2 of sea-
 #2   560     -       -     1450   0.8      1       grass has been lost, more than a 3-fold
 #3    30     30       30    3000   01      2        increase since winter 1993 (Table 1).
#4 not surveyed
Total                      2.6
November 1993 to January 1995
                                                  Biomass
#l  770    220    1340     8100   6.2
#2  430    220     800     5400   2.3
#3  180    150     210     2700   05                Tiends in biomass over time differed
#4  140    80     220     2900   0.4               according to depth (Fig. 4, Table 2). In
Total                      9.4               the 2 shallowest depth classes, there
                                         was no change over time. In the 115-
224                     Mar Ecol Prog Ser 138: 219-231. 1996




130 cm depth class, the main difference
was that biomass was >30% higher In
1991 than other years. The significant
reduction in biomass between 1992 and
1993 is consistent with a brown tide ef-
fect; however, the lack of a significant
difference between the pre-brown tide
year and 1993 argues against this inter-
pretation.
  In the 130-140 cm depth class, bio-
mass was elevated in 1991 also (Fig. 4).
However, in this case, there was a sig-
nificant reduction in biomass between
the pre-brown tide year and 1993, the
last year for which biomass data are
available. The reduction from 1992 to
                                85    85-115    115-130   130- 140    > 140
1993 was not significant (Table 2).               DEPTH CLASS (CM) WITH RESPECTTO MEAN SEA LEVEL
  The strongest indication of a cumula-
tive effect of brown-tide-caused light
                                      m
                                     1988   1991  m 1992 0 1993

attenuation on seagrass biomass is the      Fig. 4. Mean biomass in 5 depth classes over 4 yr. 1988, before the advent of
monotonic decrease of biomass over        the brown tide; and 1991, 1992, 1993, under the influence of the brown tide.
                                  See Table 2 for statistical comparisons
time in the 2140 cm depth class (Fig. 4 ) .
Over the whole period, biomass diminished by >60%.
The reductions were significant from 1988 to 1993 and
from 1991 to 1993 but not from 1992 to 1993 (Table 2).
  For the 1140 cm depth class, spatial differentiation
also was evident (Fig. 5). Biomass in the southern half
of the study area was less than in the north in 1991 and
1992 but not in 1993 (Table 3).



Table 2. Mann-Whitney U tests for reductions In biomass in
different depth classes for 3 time periods: 1988 vs 1993, 1991
vs 1993 and 1992 vs 1993. U test statistic; z: standardized
normal deviate; N: sample size earlier year, later year;
             p: probability
                                                                 l
                                    1991             19m            1993
Depth class Time period    U    z   N    P                     YEAR
                                              ,  north +south
< 85     1988 VS 1993   164  -0.18 20, 17   0.43    Fig. 5. Biomass In the >140 cm depth class In northern vs
       1991 vs 1993   148  -0.43 19, 17   0.33    southern parts of the study area from 1991 to 1993. See Table 3
       1992 vs 1993   209  -0.68 28, 17   0 25             for statistical comparisons



                                 Table 3. Mann-Whltney U tests for differences ~n biomass in
                                 the > l 4 0 cm depth class in the northern (less affected by
                                 brown tide) and southern (more affected by brown tide) parts
                                 of the study area In different years. U: test statistic; z: stan-
                                 dardized normal deviate; N: sample slze north, sample
                                          size south; p: probability

                                 I  year      U      z      N      P
                    Onuf: Seagrass loss in response to light reduction                  225




          Light

 In May 1993, continuously recording
underwater light monitors were in-
stalled at canopy height at the outer
boundary of a seagrass meadow (Stn
L1) and 200 m into the meadow (Stn L2)
to document with precis~onn ~ i n i m u n ~
and sufficient levels of PAR to sustain
established seagrass meadows. In Oc-
tober 1993 a third monitor was installed
17 km to the north in a deep site with
continuous seagrass cover (Stn L3),
with the intent of documenting the light
environment at a clearer location. By
December 1993, the outer boundary                                               I
                          May-93     Aug-93      Nov-93    Mar-94    Jun-94   Sep-94
had receded 30 m landward from Stn                             DATE
L1 (Fig. 3). By January 1995, the outer                  ,site   L1 ++ site L2 -site  L3
boundary was within 30 m of Stn L2
and had receded past Stn L3 (Fig. 3).      Fig. 6. Weekly mean percentage incident PAR reaching canopy level at 3 sta-
Over the period with records from all 3     tions in upper Laguna Madre. See Fig. 2 for locations of monitors In relation to
statlons (10 October 1993 to 21 August                    shifts in seagrass boundaries
1994), 9 % of incident PAR reached
canopy level at Stn L1, 14% at Stn L2, and 16% at         (28 vs 18%),but the relationship was reversed the fol-
Stn L3; however, the temporal distribution of percent       lowing spring and summer (6% of incident PAR reach-
of surface PAR reaching seagrass canopy level was         ing canopy level at Stn L3 vs 12% at Stn L 2 ) . By No-
highly variable and differed between locations (Fig. 6).      vember 1995, seagrass had disappeared at Stn L2 as
A higher percentage of incident PAR reached the sea-        well.
grasses in winter (November 1993 to March 1994) than         Periodic Secchi disk measurements at stations
in the spring-summer period of active growth (April to       throughout the study area revealed a north-south gra-
August 1994) at all stations. Much more light pene-        dient in light attenuation (Fig. 7). Based on pooled data
trated to canopy level at Stn L3 than at Stn L2 in winter     for 20 sampling dates and 1 to 3 stations on a latitude
                                           transect of sufficient depth to measure
                                           Secchi depths, the percent frequency of
                                           Secchi depths <60 cm (relatively high
                                           light attenuation) increased from 15 to 55
                                           from the north end of the study area to the
                                           south, while the percent frequency of
                                           Secchi readings > 100 cm (relatively clear
                                           water) decreased from 50 to 15. This in-
                                           crease in light attenuation from north to
                                           south is consistent with the higher biomass
                                           seen in the 2140 cm depth range in the
                                           northern half of the study area than in the
                                           southern half in 1991 and 1992 (Fig. 5).
                                             In order to apply this north-south gra-
                                           dient in Secchi depths to predictions of
                                           the area of seagrass likely to be lost
                                           in different parts of the study area as a
      40&38     34      30      26     22&20        result of brown tide shading, a corre-
           MINUTES NORTH OF 27 DEGREES NORTH
                                           spondence had to be established be-
      CM a 6 0 - S O C M 6 0 - 1 0 0 ~~ ~> ~ O O C M               tween Secchi depth and light attenua-
Fig. 7 Percentage frequency of observations in different Secchi depth cate-
                                           tion. The % S1 reaching Secchi depth
gories along a latitudinal gradient in upper Laguna Madre, April 1992 to       proved to be extremely variable, ranging
               September 1994                     from 15 to 40 (Fig. 8). For Secchi depths
226                        Mar Ecol Prog Ser 138: 219-231, 1996




>60,% S1 reaching Secchi depth tended to decrease as          equation for the 'calm' array of points in Flg. 8 ( A and +
Secchi depth increased. For Secchi depths <60 cm,%           symbols). Short Secchi depths in November to March
S1 tended to be lower when winds exceeded 24 km h-'           were assumed to be the result of episodes of sediment
at exposed locations ( X = 24, SE = 2.1) than for all loca-       resuspension associated with winter storms. Conse-
tlons when winds were <24 km h-' (57 = 30, SE = 1.3)          quently, the mean % S1 for the 'rough' array in Fig. 8
and for protected locations when winds exceeded 24            was used for Secchi values <60 cm in November to
km h-' ( X = 31, SE = 1.8).                       April. The relationship for the calm array was used for
  The difference in % S1 for Secchi depths <60 cm            Secchi depths >60 cm.
between rough water conditions (stiff breeze, exposed
locations) and calrn (moderate breeze or protected
location) was significant ( t = 3.14, df = 22). Therefore,
the mean of the 9 observations for exposed locations
with winds >24 km h-' was taken as representative for
rough conditions (24 % S1 reaching Secchi depth). For
calm conditions, estimates of % S1 were generated
from the linear regression equation for all other points
in Fig. 8: % SIsD= 35.1 - 0.0698 SD (r2= 0.37, df = 39),
where SD is Secchi depth.
  Winds exceeded 24 km h-' 39% of the time in the
November to April period of frequent frontal passage
compared to 15 % of the time in May to October, based
on the 2 yr of records analyzed for the monitoring sta-
tion near Bird Island (Fig. 3). The difference was more
pronounced for winds with long fetch, oriented along
the long axis of the lagoon. They prevailed 17 % of the
time in November to April compared to 3 % of the time
in May to October.
  The geographic survey of light attenuation by Secchi
depth, the light versus Secchi depth relations and a
bathymetric survey (Fig. 9) were then integrated to
depict % S1 at canopy height over the study area.
  Because of the low frequency of winds r 2 4 km h-'
from May to October, especially oriented along the
long axis of the lagoon, estimates of light at depth for
that period were derived from the linear regression




101                                 I
  0     50      100     150     200     S O
              SECCHI DEPTH (CM)
     A calm     X  windy, exposed  + windy, protected
Fig. 8. Relationship between Secchi depth and percentage of       Fig. 9. Bathyrnetric map of study area Dashed line marks the
incident PAR reaching Secchi depth under calm and rough         course of the Gulf Intracoastal Waterway Small channels and
             conditions                         emergent or shoal areas are not depicted
                   Onuf. Seagrass loss in response to light reduction                227




                    BARE         VEGETATED          UPLAND

Fig. 10.Bare areas in upper Laguna Madre (a) predicted based on measured hght attenuation, depth and assumption that c15%
of incident PAR reaching canopy level is limiting to meadow development. (b) determined by survey October-November 1988,
before advent of the brown tide; (c) determined by survey October-November 1994, after 4 growing seasons of brown tide
               Dashed line indicates the course of the Gulf Intracoastal Waterway

 Applying the criterion that long-term mean light       ity of light is governing distribution in this system, a
reaching canopy level must exceed 15% of incident        seagrass meadow should survive there, regardless of
PAR to sustain Halodule wrightiimeadows (Kenworthy       how long the brown tide persists. To the south, increas-
et al. 1991, Onuf 1991, this study) to the Secchi depth     ing light attenuation and deeper water yield predic-
and light data of this study, the predicted maximum       tions of larger expanses of bare bottom (Fig. 10a). In
depth of seagrasses varied from 180 cm at 27' 38-41'      all, on the basls of measured light attenuation, 24 % of
N to 170 cm at 27" 34-37' N, 160 cm at 27" 30-33' N,      the study area is predicted to be too deep to support
150 cm at 27" 26-29' N, and 140 cm at 27" 20-25' N.       seagrass meadow. In contrast, only 6 5 of the study site
                                                     %
The northern part of the lagoon is mostly shallow (82 %     was bare before the advent of the brown tide
< 1 m deep north of 27" 37' N compared to 22 % < 1 m      (Fig. l o b ) . The greatest change in cover between pre-
deep south of 27" 30' N; Fig. 9 ) .Therefore, i availabil-
                       f         brown tide conditions and that predicted based on
228                      Mar Ecol Prog Ser 138: 219-231. 1996




Table 4. Final % of study area predicted to go bare if brown    tion. First, much of the lagoon is so shallow that even
tide persists long enough for distribution of seagrasses to    drastic light reduction would have no effect on distrib-
reach steady state with the light regime for different assump-
tions about minimum light requirements and relations
                                  ution or biomass over much of the area. Almost 50% of
     between light attenuation and Secchi depth        the study area is <1.0 m deep, while the Halodule
                                  wrightii meadow extended at least to 1.8 m before the
 %  S1 at Secchi depth     Minimum l ~ g h requirement
                         t
                                  brown tide began. Second, there was a d~stinct   gradi-
                   for Halodule wrightii     ent in light attenuation increasing from north to south.
                   15% S1     18% S1    Since the long-term light record for the upper lagoon
                                  (Dunton 1994) is from the south, much of the lagoon
 Varies with season and wind     18       24
                                  was not subject to such severe light deprivation as
 Does not vary systematically     20       27
 (use mean for all conditions)
                                  measured there. Third, the resolution of the initial
                                  sampl~ng  program in 1988 was so coarse that substan-
                                  tial changes in distribution could have occurred with-
                                  out being detected. The original sampling design was
available llght with brown tide is in the middle of the      patterned after an earlier survey of the lagoon
study area (Fig. 10a, b). Documented losses also are        (Merkord 1978) to maximize the power of the analysis
concentrated in the middle of the study area (Fig. 10c);      for trends between studies (Quammen & Onuf 1993).
however, as yet, the area pred.icted to go bare from        This meant that relatively little effort was expended in
measurements of the underwater light regime is con-        the most critical areas for detecting possible effects of
siderably larger than what is bare (Fig. 10a, c).         light limitation: deep areas with vegetation and the
  Because the assumptions about the seasonality of        zone where vegetation terminated in deep water.
light attenuation versus Secchi depth and the mini-        Fourth, the morphology of the lagoon is such that the
mum light requirement for Halodule wrightii are sub-        middle region is relatively flat, while the slope is rela-
ject to question, losses were estimated for 2 other        tively steep toward the edge. In the one part of the
assumptions. In one case, no systematic variation of %       lagoon where the seagrass meadow terminated in
S1 with respect to Secchi depth was assumed, and the        deep, bare bottom, the outer boundary lay in this
mean for all 50 observations (27.8% S1 reaching Secchi       region of steeper slope. Therefore, any lateral shift in
depth) was used to estimate '10 S1 reaching canopy         outer boundary corresponding to a decrease in the
level (25 cm above bottom) under all conditions. In the      compensation depth for the seagrasses was relatively
other case, 18% S1 was assumed to be the minimum          small.
necessary to support a seagrass meadow as reported          Regardless of the characteristics of the sampling
by Dunton (1994), rather than the 15% suggested in        program diminishing its sensitivity to detect change
this study. Both alternative assumptions lead to some-       resulting from light reduction, the area of bottom expe-
what higher estimates of bare bottom at steady state       riencing light reduction below that required to sustain
with the brown-tide-influenced light regime than as        a seagrass meadow was far in excess of the detect~on
described above (Table 4).                    limits of the sampling program. One possible explana-
                                 tion for the persistence of an established seagrass
                                 meadow under conditions of limiting light is that sur-
              DISCUSSION               viving shoots cannibalize the resources of adjacent
                                 shoots as they succumb to light limitation. According to
  The depth limit of seagrass meadows is commonly        this conceptual model, an established meadow might
assumed to be set by light attenuation underwater         be able to survive much longer under insufficient light
(Bulthuis 1983, Orth & Moore 1983, Iverson & Bittaker       than the life span of individual shoots would suggest
1986, Dennison 1987, Duarte 1991, Dennison et al.         by translocation of reserves from dying parts to rhi-
1993).In this study, >50% reduction of light caused by      zomes, analogous to the process of reclamation of
a dense phytoplankton bloom compared to pre-bloom         nutrients and presumably other materials from senes-
conditions had no discernible effect on distribution       cent leaves to support new growth in Zostera manna
until after the fourth growing season under reduced        (Pederson & Borum 1993) These resources might then
light. However, an effect on biomass was seen sooner.       subsidize survival of existing shoots and even develop-
Biomass at depths > l 4 0 cm was less in the first sam-      ment of new shoots. This progressive pooling of
pling after the initiation of the brown tide, after 2       resources from a formerly larger population to support
growing seasons of reduced light, than before.          new growth in a progressively smaller population
 Four factors contribute to the apparent discordance       operating at a deficit would seem necessary to account
between the magnitude of the environmental change         for the persistence over years of a species in which the
and the expression of an effect on seagrass distribu-       mean life span of individual shoots is 110 d (Gallegos et
                   Onuf: Seagrass loss in response to light reduction                229




al. 1994). Alternatively, the life span of individual      to occur under calmer conditions than previously
shoots may be longer under conditions of light limita-     (Ward et al. 1984) a n d more frequently. An indirect
tion than under the conditions assessed by Gallegos       effect may be the efflux of nutrients from the sedi-
et al. (1994).                         ments a s the recently dead seagrasses a r e remineral-
  No data a r e available to evaluate the responses of     ized, enhancing the growth of the brown tide organ-
populations of shoots; however, the gradual decrease      ism.
in biomass in d e e p areas where Halodule wrightii        Obviously, there is a limit to how long this holding
persists is consistent with this proposed mechanism. If     action by seagrasses can go on, if indeed light has been
reclamation of nutrients and stored reserves is respon-     reduced below the ecological compensation point
sible for the persistence of seagrasses in Laguna        (sensu Kenworthy et al. 1991). That limit was sur-
Madre under conditions of light limitation caused by      passed in some parts of the lagoon in 1993. Approxi-
the brown tide, then a reduction in seagrass biomass      mately 3 km2 of seagrass meadow went bare between
over time should be evident in deeper parts of the       distributional surveys made in fall 1992 a n d fall 1993,
lagoon where light is now limiting, compared to shal-      and the process of loss of seagrass cover has acceler-
lower areas where light remains sufficient. This trend     ated through fall 1994 (Fig. 3).
was apparent. While there was no downward trend          Predictions of how much further the losses might
over time in seagrass biomass in depths up to 115 cm      proceed a r e difficult to make because the light regime
and equivocal changes between 115 a n d 140 cm, bio-      of the lagoon is not uniform and no determination of
mass diminished by >60% in the 2140 cm depth range       minimum light requirements was made before the
by the end of the 1993 growing season (Fig. 4 ) . The fact   advent of the brown tide. Therefore, it is necessary to
that the reduction from 1992 to 1993 was not signifi-      use determinations made elsewhere of minimum light
cant may signal that shoot density in deep areas has      requirements to support development of continuous
equilibrated with the low light conditions of the brown     meadows of Halodule wrightii and evaluate them in
tide and that no more losses will occur. An alternative     terms of the measurements made in this study, when
explanation is that the process of biomass loss contin-     the outer boundaries were not fixed. Kenworthy et al.
ues, but the mean for the depth class has not changed,     (1991), working in Hobe Sound, Florida, USA, and
because some of the lowest biomass sites of 1992 had      Onuf (1991), in lower Laguna Madre, calculated from
gone bare by 1993 and are not represented in the 1993      long-term monitoring of light along transects crossing
determination of mean biomass for vegetated samples.      the outer boundary of meadows at many locations that
  Detailed observations by Dunton (1996) at one site      the ecological compensation point for the species was
where he had also collected continuous data on light      where 12 to 20% of surface light reached canopy level.
reaching the bottom are consistent with this interpreta-    In this study, sites where 9 a n d 16% of incident PAR
tion of persistence accomplished by reclamation of       reached to the depth of the seagrass canopy over the
nutrients and other resources from dying parts. Peak      10 mo period of record had gone bare by December
biomass of rhizomes and roots based on quarterly        1994. The remaining site where 1 4 % of surface light
determinations had diminished every year since the       reached canopy level had gone bare by November
beginning of the brown tide, from >500 g mW2 1989 in      1995. Two other studies from Texas closely bracket the
to <200 g m-2 in 1993.                     minimum light requirement for H. wrightii. In a shad-
  The difference in biomass in d e e p water in 1991 and    ing experiment in eastern Corpus Christi Bay, Texas,
1992 between the northern and southern parts of the       H. wnghtii was eliminated within 9 mo when receiving
study area (Fig. 5) is consistent with the gradient seen    16% S1 (Czerny & Dunton 1995). In upper Laguna
in water clarity (Fig 7). If, as hypothesized, the light    Madre, H. wrightii persists at a site receiving a n aver-
regime of the Laguna Madre is driving the changes in      a g e of 18 % S1 since the advent of the brown tide (Dun-
biomass and distribution observed over the last 6 yr,      ton 1994). These results indicate that there is a region
then the diminution of the north-south contrast in bio-     of uncertainty in the determination of minimum trans-
mass in 1993 suggests that the latitudinal gradient in     mission of light required to sustain a seagrass meadow,
light has broken down. This is suggested by the con-      but that 15% of incident PAR reaching canopy level is
tinuous monitoring records for light at Stns L1 and L2     in the middle of that range. The difference in the sea-
near the south e n d of the study area a n d Stn L3 near    sonal patterns of light availability between Stns L2 a n d
the middle of the study area (Fig. 6). The probable       L3 (Fig. 6) may explain the anomaly of longer persis-
cause for the deterioration of water clarity at Stn L3 is    tence of seagrass at the site with less light. Perfor-
that the bottom has gone bare around it (Fig. 3). With-     mance of the seagrasses is likely to be governed more
out an intact seagrass meadow to buffer the action of      strongly by light availability in the growing season
waves and the fabric of rhizomes and roots to bind the     than by availability over the whole year. Between April
sediments, resuspension of bottom sediments is likely      and August 1994, half as much light reached canopy
230                    Mar Ecol Prog Ser 138: 219-231, 1996




level at Stn L3 as at Stn L2, even though more llght got   ditlonal North American wintering areas such as
to canopy level at Stn L3 over the whole period of      Chesapeake Bay, Pamlico Sound and Galveston Bay
record from October 1993 to August 1994.           have been abandoned already (midwinter waterfowl
  These findings generally validate the estimate of     survey compilations, Office of Migratory Bird Manage-
minimum light necessary to maintain the seagrass       ment Files, U.S. Fish and Wildlife Service, Laurel, MD)
meadow that was used in this study to project the ulti-   and major modifications are proposed for the Laguna
mate extent of seagrass loss caused by the persistent    Madre de Tamaulipas, just across the delta of the Rio
brown tide. Therefore, the difference between the      Grande in Mexico, the second most important redhead
extent of bare bottom measured so far (Fig. 10c) and     wintering area.
that expected on the basis of where llght at canopy       This study sheds no light on the critical question of
level drops below 15% of what reaches the surface of     how long the brown tide may last. Stockwell et al.
the water (Fig. 10a) suggests that considerably more     (1993) reasonably speculated that regional drought
seagrass will be lost before seagrass meadows of upper    and hypersalinity established conditions that favored
Laguna Madre come to equilibrium with the brown-       the brown tide organism. Then a freeze-caused fish
tide-influenced light regime. This interpretation is     kill conceivably provided the limiting organic or inor-
least reliable for the northern part of the study area.   ganic compounds necessary to promote rapid growth.
where continuous records of underwater light are not     Limited water exchange and reduced grazing pressure
available and where incursions of the brown tide are     undoubtedly contribute to unprecedented persistence
shorter and more sporadic than to the south. Here, the    of the brown tide (Stockwell et al. 1993); however,
1 to 2 mo intervals between sampling in the Secchi disc   some additional source of nutrients also seems neces-
survey may not have been sufficient to represent the     sary (T.Whitledge pers. comm.),and ammonium is the
light regime, or there may have been episodes of clear    most likely candidate, since the brown tide alga is not
water during the growing season sufficient to sustain    able to use nitrate (DeYoe & Suttle 1994).One possible
seagrasses, despite low light for the year as a whole.    source could be ammonium regenerated from dying
  The weakest assumptions used in predicting the ulti-   seagrasses. If this is the case, the brown tide might be
mate extent of seagrass cover to be lost as a result of   expected to persist as long as the seagrass meadows
brown tide shading are the choice of 15% of incident     continue to recede. However, possible contributions
PAR reaching canopy level as the minimum light        from watershed sources cannot be discounted.
required by Halodule wrightii and the attribution of
different Secchi depth versus PAR attenuation rela-     Acknowledgements. J . J Ingold assisted in all phases of the
tionships (Fig. 8) to winter and summer periods based    study. L. J. Hyde assisted in the laboratory. K. H. Dunton
on their different wind regimes. Results using Dunton's   kindly supplied data on incident PAR. Data on water level and
                               wind speed and direction were kindly supplied by the Texas
(1994)estimate of 18 % S1 as the minimum requirement    Coastal Ocean Observation Network, operated by the Conrad
of H. wrightii and attenuation based on the mean of all   Blucher Institute for Surveying and Science at Texas A&M
observations of % S1 yielded somewhat higher esti-     University, Corpus Christi. D. W. Hicks and B. B. Hardegree
mates of area of seagrass lost (Table 4 ) . Since H.     prepared final versions of maps The manuscript has bene-
                               fited from the comments of E. J Buskey, K H. Dunton, J. J .
wrightii still survives at Dunton's (1994) site and has   Ingold and 2 anonymous reviewers.
succumbed at the 3 stations with continuous light mon-
itoring records in this study, the actual limit may lie
between. I have no independent evidence to evaluate                LITERATURE CITED
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This article was presented by G. W. Thayer (Senior Editorial     Manuscript first received: A p r ~ 25, 1995
                                                    l
Advisor), Beaufort, North Carolina, USA               Revised version accepted: January 24, 1996