337Q 2001 Estuarine Research Federation

Estuaries Vol. 24, No. 3, p. 337–346 June 2001

The Decline and Recovery of a Persistent Texas Brown Tide Algal

Bloom in the Laguna Madre (Texas, USA)

EDWARD J. BUSKEY*, HONGBIN LIU1, CHRISTOPHER COLLUMB2, and JOSE GUILHERME F.BERSANO3

University of Texas Marine Science Institute, 750 Channelview Drive, Port Aransas, Texas 78373

ABSTRACT: The Laguna Madre has experienced a persistent bloom of Aureoumbra lagunensis for over eight years. Thepersistence of this bloom may be due in part to the often hypersaline conditions in Laguna Madre (40–60 psu) thatfavor the growth of A. lagunensis. Above-normal rainfall in the fall of 1997 reduced the salinities in Baffin Bay from .40 to , 20 psu. A. lagunensis cell densities dropped from . 106 cells ml21 in July 1997 to c. 200 cells ml21 in January1998. During this time of low brown tide density, phytoplankton biomass generally remained high and the Laguna Madreexperienced successive blooms of diatoms (Rhizosolenia spp.) and cyanobacteria. Hypersaline conditions returned in1998 and brown tide densities increased to . 0.5 3 106 cells ml21 by summer. The extraordinary persistence of thebrown tide and the unusual sequence of intense blooms may be related in part to the reduction of zooplankton popu-lations. Microzooplankton populations declined following the above-normal rain in the fall of 1997; populations did notrecover until fall 1998. Copepod populations also declined sharply and remained low in Laguna Madre, but recoveredby summer 1998 in Baffin Bay. Dilution experiments indicated that microzooplankton grazing and phytoplankton growthwere usually balanced when measured during our cruises. The rapid recovery of the A. lagunensis bloom suggests thatthis alga may be a more resilient component of the Laguna Madre flora than previously suspected.

IntroductionThe Laguna Madre of Texas is a large, shallow,

and often hypersaline subtropical lagoon. A bloomof the alga Aureoumbra lagunensis persisted withoutinterruption in the Laguna Madre from December1989 through October 1997. This species had notbeen described prior to this bloom (DeYoe et al.1997) although subsequent investigations haveshown that this species was present in small num-bers before the bloom (Buskey et al. 1999). This isthe longest uninterrupted phytoplankton bloom ofwhich we are aware. The bloom began in late fallof 1989 in three small embayments within BaffinBay, following a prolonged period of drought inTexas (Buskey et al. 1997). The collapse of grazerpopulations prior to the initiation of the bloom(Buskey et al. 1997) along with the ability of A.lagunensis to grow at maximum rates under hyper-saline conditions (Buskey et al. 1998) may havebeen important factors in bloom initiation, whilea nutrient pulse released by the decomposition offish killed in a severe freeze may have served to

* Corresponding author: tele: 361/749-6794;fax: 361/749-6777; e-mail: buskey@utmsi.utexas.edu.

1 Present address: Louisiana Universities Marine Consortium,8124 Highway 56, Chauvin, Louisiana 70344.

2 Present address: Boston University, College of General Stud-ies, 871 Commonwealth Avenue, Boston, Massachusetts 02215.

3 Present address: Nuleo de Estudos do Mar, Centro de Cien-cias Biologicas, Universidade Federal de Santa Catarina, Cam-pus Trindade, Florianopolis, SC 88040-900, Brazil.

intensify the growth phase of the existing bloom(Whitledge 1993; DeYoe and Suttle 1994).

The reasons for the extraordinary persistence ofthis bloom are less apparent. The Laguna Madrehas limited water exchange with the Gulf of Mex-ico, so the prolonged residence time of its waters,thought to be in excess of one year (Shormann1992), may reduce potential losses of brown tidecells through advection from the system. Field data(Buskey and Stockwell 1993) and laboratory stud-ies (Buskey and Hyatt 1995) have documented thatA. lagunensis is poor food for planktonic grazers,and this reduced planktonic grazing pressure mayalso contribute to the persistence of the bloom.Hypersaline conditions also promote the produc-tion of extracellular polymeric substances (EPS) bythis alga (Liu and Buskey 2000a) and high levelsof EPS inhibit the growth and grazing of protozoaon A. lagunensis (Liu and Buskey 2000b). A. lagu-nensis does not appear to be toxic to adult fish orbenthic invertebrates (Montagna et al. 1993; Bus-key et al. 1996). High cell densities decreased lighttransmission to the bottom and reduced the dis-tribution and biomass of seagrasses in Laguna Ma-dre (Dunton 1994; Onuf 1996).

The purpose of this study was to examine thebalance between populations of brown tide andplanktonic grazers over a gradient from highbrown tide concentrations to low concentrationduring an annual cycle. We hypothesized that highdensities of brown tide inhibited the growth and

338 E. J. Buskey et al.

Fig. 1. Location of major sampling stations in Baffin Bay(BB), Laguna Madre (LM), and Corpus Christi Bay (CC).

grazing of microzooplankton populations. Basedon our experience with the seven-year bloom, apattern of brown tide gradients has typically beenobserved between Baffin Bay, where brown tideconcentrations are typically highest, and CorpusChristi Bay, where the alga is typically at back-ground levels. Abundance of A. lagunensis, phyto-plankton biomass, zooplankton abundance, andmicrozooplankton grazing rates were measured atthree stations in Corpus Christi Bay, Upper LagunaMadre, and Baffin Bay at 3-mo intervals over a pe-riod of 15 mo. Although it was not anticipatedwhen this study was planned, the decline and re-covery of an A. lagunensis bloom was documentedwhen heavy rains flushed the brown tide from La-guna Madre in the fall of 1997, and drought leadto rapid recovery of hypersaline conditions in1998.

Materials and MethodsThe field work was carried out using the R/V

Longhorn as a base of operations and by deployingsmall boats to make collections in the shallow wa-ters of Laguna Madre and Corpus Christi Bay.Based on historical distributions and a survey of A.lagunensis distributions a few days prior to the firstcruise, station locations were chosen in CorpusChristi Bay, Laguna Madre, and Baffin Bay (Fig. 1).Baffin Bay has historically been the area with thehighest concentrations of A. lagunensis, while La-guna Madre has substantial but usually lower con-centrations and Corpus Christi Bay typically hasonly trace amounts (Buskey et al. 1996).

Temperature and salinity were measured nearthe surface and bottom at each station (Fig. 1) us-

ing a YSI Model 30 temperature and salinity meter.Triplicate, subsurface whole water samples werecollected at 3 stations. Samples were preserved in2% formaldehyde for enumeration of A. lagunensisdensities using an immunofluorescence assay (Lo-pez-Barreiro et al. 1998; Buskey et al. 1999). Mi-crozooplankton samples were preserved with c. 5%acid Lugol’s iodine, and were enumerated fromwhole water samples using the Utermohl methodwith 5–20 ml of sample (depending on planktondensity) settled in a well slide and counted usingan inverted microscope. Sample preservation withLugol’s iodine made it impossible to distinguishbetween autotrophic and heterotrophic dinofla-gellates based on chlorophyll autofluorescence.Samples for flow cytometric analysis were pre-served with formaldehyde (0.2% final concentra-tion), quick frozen in dry ice, and stored at 2808Cuntil analysis. A FACSCaliber flow cytometerequipped with a 15-mW laser exciting at 488 nmwas used to enumerate the picoplankton and na-noplankton. At least 10,000 events were countedfor each sample. Forward and right angle lightscatters and green, orange, and red fluorescencewere collected, saved, and analyzed with Cytowinsoftware (Vaulot 1989). The detection limit wastriggered by chlorophyll fluorescence to eliminatesignals from numerous detritus particles. Severalmajor groups of picoplankton and nanoplanktonwere distinguished based on their light scatter andautofluorescence properties. Whole water sampleswere collected for measurement of phytoplanktonbiomass as chlorophyll a (chl a). Triplicate samplesof between 10 and 50 ml of water were filteredonto GF/F glass fiber filters, wrapped in aluminumfoil, and frozen. On return to the laboratory, sam-ples were extracted for 24 h in 90% acetone andchlorophyll fluorescence was measured with aTurner Designs TD-700 fluorometer.

Mesozooplankton samples were collected in trip-licate tows at three stations using a 30-cm diam,153-mm mesh plankton net. The net was towed be-low the surface for 5 min, and the volume of watersampled was quantified using a General Oceanicsflowmeter mounted in the mouth of the net. Sam-ples were preserved in 5% buffered formaldehydefor species enumeration. To get a better estimateof abundance of copepod nauplii, triplicate netsamples were also collected at each station with a30-cm diam, 64-mm mesh plankton net equippedwith a low-speed General Oceanics flowmeter.

The dilution method (Landry and Hassett 1982)was used to assess the growth of phytoplanktonpopulations and microzooplankton grazing im-pact. Brown tide impacted waters have proved tobe very difficult to filter for dilution experiments,probably due to the large amounts of EPS on the

Texas Brown Tide Decline and Recovery 339

Fig. 2. Long-term average salinity in Baffin Bay, from Janu-ary 1995 through December 1998, based on data collected dur-ing the Texas Parks and Wildlife Department fish census (un-published data) and average monthly rainfall from several lo-cations near the shores of Baffin Bay during 1997 and 1998(King Ranch unpublished data).

Fig. 3. Temperature and salinity conditions at the three ma-jor sampling stations during the 6 cruises from July 1997through October 1998.

cell surface (Liu and Buskey 2000a) that quicklyclog even glass fiber filters. In order to producethe volume of filtered seawater needed for dilutionexperiments, brown-tide impacted waters were firstprefiltered through a series of cartridge filters ofdecreasing porosity, and finally through a 0.45-mmporosity capsule filter. Triplicate 500-ml polycar-bonate bottles were prepared for dilutions of100%, 50%, 25%, 10%, and 5% whole seawater ateach site. Chlorophyll samples for each dilutionreplicate were collected on GF/F glass fiber filtersat the beginning and end of the experiment. Bot-tles were incubated for 24 h in a 30-cm deep deckincubator with a continuous flow of seawater fromthe Laguna Madre. Light levels in the deck incu-bator were comparable to those in the Laguna Ma-dre where average depth is , 1 m. We decided notto add nutrients to dilution incubations because ofthe unknown effects of added nutrients on proto-zoa (Gifford 1988) and because dissolved inorgan-ic nitrogen and phosphorous concentrations inthese shallow waters were only occasionally at levelsthat might be expected to limit phytoplanktongrowth based on past measurements (Whitledge1993; Buskey et al. 1996), especially for a slow-growing species like A. lagunensis (Stockwell et al.1993).

ResultsThe Laguna Madre is often hypersaline, since

evaporation normally exceeds precipitation insemi-arid South Texas, and there are no perma-nent rivers entering the upper Laguna Madre.Data collected during the Texas Parks and WildlifeDepartment’s monthly fish surveys show the his-torical pattern of hypersaline conditions in Baffin

Bay from 1995 through 1998 (Fig. 2). Samplinglocations in the survey were randomly chosen froma grid of c. 350 potential sampling locations in theupper Laguna Madre, so the sample locations varyeach month and only those locations from BaffinBay were averaged to produce Fig. 2. In spite ofthe spatial variability of collection sites, a clear pat-tern of generally hypersaline conditions is evidentin Baffin Bay during 1995 and 1996. There was anextended period of extreme hypersaline condi-tions (. 45 psu) from summer 1996 throughspring 1997, during which the brown tide flour-ished. Above-normal rainfall in spring of 1997 (Fig.2) dropped salinities to near 35 psu for severalmonths before Baffin Bay became hypersalineagain in late summer 1997. Salinities climbed tonearly 50 psu in September of 1997 before plum-meting to c. 15 psu in November of 1997, followingextensive rains in October 1997. Salinities in-creased in Baffin Bay steadily during a drought pe-riod through the next year, returning to nearly 50psu by September 1998. Salinities again fell to ,20 psu in November 1998 following extensive rainsin the fall of 1998, including those associated withtropical storm Frances.

Water temperatures at our three stations rangedfrom a high of 308C during July cruises in 1997and 1998 to a low of 188C during October 1997(Fig. 3). Water temperatures were within 18C at all

340 E. J. Buskey et al.

Fig. 4. Chlorophyll a concentrations (top) and Aureoumbralagunensis cell concentrations (bottom) at the three major sam-pling stations from July 1997 through October 1998.

three stations on each cruise, but since stationswere visited in succession at approximately 3-h in-tervals (0900, 1200, 1500), water temperaturestended to increase slightly as the day progressed,so mean temperatures for all three stations are pre-sented. There was no indication of stratification inthe shallow waters of these stations so only surfacetemperatures are reported. There has historicallybeen a salinity gradient between the three stationsin our study, with highest salinities often in BaffinBay (making it a reverse estuary), somewhat lowersalinities in Laguna Madre, and lowest salinities inCorpus Christi Bay, which receives freshwater in-flow from the Nueces River (Buskey et al. 1996;Buskey unpublished data). During the first cruisein July 1997, salinities were similar at all three sta-tion (c. 35 psu; Fig. 3). Following the heavy rainsin October 1997, Baffin Bay acquired a salinity dis-tribution similar to a normal estuary, as dry creekbeds filled and carried enormous amounts offreshwater into Baffin Bay. Even though CorpusChristi Bay also had high freshwater inflow, thesesalinities were modified by tidal exchange with theGulf of Mexico. During the severe drought of the

following year, salinities increased faster in theshallow Laguna Madre, which had the highest sa-linities during the April 1998 and July 1998 cruises.It was not until the final cruise in October 1998that the typical gradient of salinity from high inBaffin Bay to low in Corpus Christi Bay had beenre-established.

Phytoplankton biomass, estimated as concentra-tion of chl a, varied from a high of 49 mg chl am23 to as low as c. 1 mg chl a m23 at the threemajor stations over the course of this study (Fig.4). The samples taken from Baffin Bay in July 1997(49 mg chl a m23) represented the end of the near-ly 8-yr, uninterrupted brown tide bloom that hadbegun in December 1989. Phytoplankton biomassremained high in Baffin Bay in October 1997 (40mg chl a m23), but in this case the biomass wasdominated by the diatom Rhizosolenia. Phytoplank-ton biomass in Baffin Bay fell to 4 mg chl a m23 inJanuary 1998, but recovered to 47 mg chl a m23 byJuly of 1998 with the return of the brown tidebloom. In Laguna Madre, phytoplankton biomasswas lower than in Baffin Bay from July 1997through January 1998. In April 1998, Laguna Ma-dre experienced a cyanobacterial bloom that in-creased phytoplankton biomass to 37 mg chl a m23.Phytoplankton biomass climbed to 45 mg chl a m23

in October of 1998 with the return of the browntide bloom. Phytoplankton biomass in CorpusChristi Bay was typically lower than that found inLaguna Madre or Baffin Bay (Fig. 4).

At the beginning of this study, the brown tidealga was still at bloom concentrations in Baffin Baywith 14 3 105 cells ml21 (Fig. 4). Cell densities de-clined to less than 200 cells ml21 in Baffin Bay inJanuary 1998 (near background level, Buskey et al.1999). Brown tide populations increased steadilyover the next nine months, recovering to 1.4 3 105

cells ml21 by October 1998. A. lagunensis popula-tions were initially lower in Laguna Madre than inBaffin Bay, but remained higher throughout therest of the study, declining to only 1,100 cells ml21

in January 1998 but recovering to 3.6 3 105 cellsml21 by October 1998. A. lagunensis populations re-mained below 0.06 3 105 cells ml21 throughoutthis study in Corpus Christi Bay, except in April1998 when they reached 0.8 3 105 cells ml21 as A.lagunensis cells from Baffin Bay and Laguna Madrewere advected into Corpus Christi Bay by the largeinput of freshwater into the Laguna Madre. Therewas a strong positive correlation between salinityand A. lagunensis densities at all three stations (Fig.5).

In addition to the bloom of A. lagunensis, whichwas the initial focus of this study, two other majorphytoplankton blooms were observed. In Octoberof 1997 a dense diatom bloom occurred in the

Texas Brown Tide Decline and Recovery 341

Fig. 5. Relationship between Aureoumbra lagunensis densityand salinity for the three major stations from July 1997 throughOctober 1998.

Fig. 6. Flow cytometer counts of abundance of 2 unidenti-fied species of cyanobacteria and the brown tide alga Aureoumbralagunensis during a bloom in April 1998.

study area, centering in Baffin Bay. The dominantspecies in the bloom, Rhizosolenia punctiger, reacheddensities of 7,800 cells ml21 at Station 3 in BaffinBay, but were only present at densities of 1,100cells ml21 in Laguna Madre and c. 30 cells ml21 inCorpus Christi Bay. Diatom blooms had not beenobserved in the Laguna Madre since before theonset of brown tide in December 1989. In April1998, a dense cyanobacterial bloom was observedin the study area, centered in the Laguna Madre.Based on flow cytometry, two species of small coc-coid Synechococcus-like cyanobacteria were enumer-ated. Cyanobacteria species 1 was a phycocyanin-rich cell that lacked orange fluorescence under488-nm excitation, whereas species 2 was a phyco-erythrin-rich cell with fluorescence characteristicssimilar to open-ocean Synechococcus spp. (Fig. 6).Cell densities exceeded 13 3 106 cells ml21 in theLaguna Madre, but were only c. 1 3 106 cells ml21

in Corpus Christi Bay and Baffin Bay.Microzooplankton samples were numerically

dominated by ciliates; dinoflagellates were alsoabundant in some samples but autotrophic andheterotrophic forms could not be distinguishedbased on chlorophyll autofluorescence in our Lu-gol’s iodine preserved samples. In Baffin Bay, cili-ate abundance was initially quite low (, 20 cellsml21) during the end of the brown tide bloom inJuly 1997, but increased in October 1997 as thebrown tide waned following abundant rainfall (Fig.7). In the winter and spring of 1998 ciliate abun-dances decline again before increasing in the sum-mer and fall of 1998. Ciliate populations followeda similar pattern in Laguna Madre, except thatthey were consistently lower than those from BaffinBay. Populations in Corpus Christi Bay were ini-tially highest, but then went through a similar pat-

tern of decline and recovery. The pattern of ciliateabundance was quite complex, and there was littleindication of the inverse relationship to brown tideabundance that had been found in past studies;populations of both A. lagunensis and ciliates in-creased in the Laguna Madre and Baffin Bay fromApril to August 1998 (Figs. 4 and 7).

Samples collected with the 64-mm mesh net re-veal an initial gradient of decreasing abundance ofcopepod nauplii from Corpus Christi Bay to BaffinBay in July 1997 (Fig. 7). Abundance of nauplii waslow at all three stations during the next two cruisesin October 1997 and January 1998. Populationshad increased rapidly in Baffin Bay and CorpusChristi Bay by the April 1998 cruise, but declinedsomewhat over the next two cruises. Populationsof adult copepods were dominated by Acartia tonsaand showed few clear trends over the period of thisstudy. Copepods were initially most abundant inLaguna Madre, but then populations remained lowfor the rest of the study at this station (Fig. 7).Populations in Baffin Bay fluctuate widely betweenthe six cruises, with peaks of abundance duringOctober 1997 and July 1998. Populations of cope-pods were consistently abundant in Corpus ChristiBay, except for October 1997, following abnormal-ly high rainfall (Fig. 2).

Estimates of microzooplankton grazing impact,

342 E. J. Buskey et al.

Fig. 7. Zooplankton abundances at the three major sam-pling stations from July 1997 through October 1998; ciliateabundance based on whole water samples (top), abundance ofcopepods nauplii collected with tows of a 64-mm mesh net (mid-dle), and abundance of copepods (adults and copepodites) col-lected with tows of a 153-mm mesh net (bottom).

TABLE 1. Results of dilution experiments to estimate micro-zooplankton grazing coefficients g per day and phytoplanktongrowth coefficients k per day at stations in Corpus Christi Bay(CC), Laguna Madre (LM), and Baffin Bay (BB) during eachof six cruises. The correlation coefficient (r) between the frac-tion of undiluted seawater and the apparent phytoplanktongrowth is also presented. An asterisk indicates a significant cor-relation (a 5 0.05).

Cruise Location g (d21) k (d21) r

July 1997

Oct 1997

CCLMBBCCLMBB

0.880.400.380.181.030.31

0.350.430.390.270.770.32

0.84*0.76*0.95*0.66*0.85*0.61*

Jan 1998

April 1998

CCLMBBCCLMBB

0.650.200.620.780.750.05

0.880.12

20.051.120.460.11

0.93*0.87*0.89*0.97*0.95*0.24

July 1998

Oct 1998

CCLMBBCCLMBB

0.920.530.040.020.400.13

0.820.38

20.210.870.020.24

0.97*0.88*0.200.230.86*0.65*

expressed as the grazing coefficient g (d21), variedconsiderably between location and cruise (Table1). During the first cruise ( July 1997), when highconcentrations of A. lagunensis still persisted in Baf-fin Bay, microzooplankton grazing was lower inBaffin Bay and Laguna Madre than in CorpusChristi Bay. During October 1997 when a diatombloom existed in Baffin Bay, grazing impact wasgreatest in the Laguna Madre. Microzooplanktongrazing declined in Laguna Madre but increasedat the other two stations in January 1998 when phy-toplankton biomass was generally low. Grazing in-creased in Laguna Madre during the April and July1998 cruises, but could not be determined in Baf-fin Bay due to failed dilution experiments. Duringthe last cruise in October 1998, grazing was higherin Laguna Madre than Baffin Bay. The growth ofphytoplankton populations k can also be estimated

from these dilution experiments (Landry and Has-sett 1982). When growth (k) and grazing (g) weresimilar, little change in phytoplankton biomasswould be expected; when they do not balance, phy-toplankton biomass would be expected to increaseor decrease over time. At all three stations, bothgrowth and grazing estimates were either similaror grazing exceeded growth, suggesting that phy-toplankton biomass should not be expected to in-crease (Fig. 8).

DiscussionPhytoplankton bloom formation requires that

growth of the algal species exceed the sum of allloss processes, including losses to sinking, mixing,advection, disease, grazing, and other sources ofmortality. Several factors may allow A. lagunensis togrow faster than other phytoplankton species inthe often hypersaline Laguna Madre. A. lagunensiscan maintain maximum growth rates at salinitiesof up to 50 psu, and growth rates of more thanone half its maximum over a range of 15–80 psu(Buskey et al. 1998). There have been few labora-tory studies of the growth of other phytoplanktonunder hypersaline conditions, but those that havebeen studied often show reduced growth under hy-persaline conditions (e.g., Kain and Fogg 1958;Brand 1984). In a field study of the Laguna Madre,Cornelius (1984) found only 15 species of phyto-plankton at salinities from 41–50 psu, compared to90 species of phytoplankton at salinities of 21 to30 psu. At high salinities A. lagunensis produces

Texas Brown Tide Decline and Recovery 343

Fig. 8. The grazing coefficient, g, of microzooplankton pop-ulations plotted against the growth, k, of phytoplankton popu-lations, for the six cruises in this study, based on the results ofdilution experiments (see Table 1).

more EPS, a thick extracellular mucus layer thatmay help buffer the cell from harsh environmentalconditions while also inhibiting grazing on A. la-gunensis by protozoa (Liu and Buskey 2000a,b). Inaddition, there is evidence that A. lagunensis has avery low phosphorus requirement compared tomost other phytoplankton species (Villareal et al.1998; Liu et al. in press) which would give it a com-petitive advantage in a potentially phosphorus-lim-ited hypersaline coastal lagoon like the Laguna Ma-dre (Smith and Atkinson 1984, 1994).

The Laguna Madre is a shallow system (averagedepth c. 1 m) with little water exchange with theGulf of Mexico, so losses of phytoplankton due tophysical effects of sinking, mixing, and advectionare extremely small under most circumstances (thetwo periods of intense rain during this study areclear exceptions). Preliminary estimates of the res-idence time of water in the upper Laguna Madrerange from 300 d to several years, based on gagedinflows, evaporation rates, and water exchangerates through the ‘‘land cut’’ to the south and theKennedy Causeway to the north (Shormann 1992).Although viruses have the potential to affect pop-ulation dynamics of phytoplankton under certaincircumstances (Suttle 1994) there is only limitedevidence of viral inclusions in A. lagunensis from asingle collection (DeYoe et al. 1997). The mostlikely source of mortality of A. lagunensis would ap-pear to be through grazing. Although microzoo-plankton grazers have the greatest impact on pop-

ulations of small phytoplankton (Hansen et al.1994), previous studies have shown that there isoften a decline in microzooplankton abundancewhen A. lagunensis is present at bloom concentra-tions (Buskey and Stockwell 1993; Buskey et al.1998), and laboratory studies have demonstratedthat several species of protozoa will not grow on adiet of A. lagunensis, even though other similarlysized phytoplankton species support their growth(Buskey and Hyatt 1995). During the six cruises ofthis study, there was only one sample with A. la-gunensis populations at previous bloom levels (i.e.,. 106 cells ml21), so it was impossible to discernany relationship between protozoan abundanceand A. lagunensis bloom densities (Figs. 4 and 7).

The unusually intense rains of October 1997dropped salinities by over 30 psu on average inBaffin Bay (Fig. 2) and by 17 psu at station 3 ofour study (Fig. 3). Brown tide populations werecertainly substantially reduced by this massive ad-vection of water from Baffin Bay and the LagunaMadre. If advection were the only factor affectingbrown tide populations, it would be expected thatsalinity and A. lagunensis abundance would act sim-ilarly as passive tracers of freshwater dilution. How-ever, the relationship between A. lagunensis celldensity and salinity shows an exponential declinein brown tide with decreasing salinity (Fig. 5).While salinity declined from 36 to 20 psu from Julyto October 1997 in Baffin Bay, A. lagunensis pop-ulations declined from 14 to 0.016 3 105 cells ml21.The additional decline in A. lagunensis populationsmust have been caused by reduced growth and/orincreased cell mortality. Previous studies haveshown that A. lagunensis grows at reduced rates insalinities below 20 psu (Buskey et al. 1998) but con-tinues to grow at even the lowest salinity tested (10psu). However, cultures in these studies wereadapted to low salinities for extended periods oftime; nothing is known about the effects of rapidchanges in salinity on the survival and growth ofA. lagunensis.

The extensive input of freshwater in the fall of1997 appears to have stimulated a succession ofphytoplankton blooms in the Laguna Madre. Be-fore the initiation of the brown tide, the LagunaMadre was a relatively clear subtropical lagoon,characterized by relatively low phytoplankton bio-mass and extensive seagrass beds. Chlorophyll aconcentrations were typically , 20 mg l21 beforethe onset of the brown tide in 1990 (Stockwell etal. 1993). The decline of the A. lagunensis bloomwas quickly followed by a diatom bloom in BaffinBay (Rhizosolenia spp.) with chl a concentrations of40 mg l21(Fig. 4). Following a period of low phy-toplankton biomass in January 1998 (, 5 mg l21

chl a), the brown tide began to recover in Baffin

344 E. J. Buskey et al.

Bay and the Laguna Madre in April 1998, alongwith a cyanobacterial bloom that was particularlysevere in Laguna Madre and phytoplankton bio-mass increased again. There appears to have beena basic shift in the Laguna Madre ecosystem thatnow favors phytoplankton blooms and high phy-toplankton biomass, compared to the conditionsprior to the initiation of the extended A. lagunensisbloom. In this system with limited seawater ex-change, perhaps the nutrient load tied up in biotaremains high following the large nutrient input re-sulting from the extensive fish kill caused by a se-vere freeze in December 1989 (Whitledge 1993;DeYoe and Suttle 1994; Buskey et al. 1997).

The intense freshwater inflow event in the La-guna Madre appeared to have complex effects onzooplankton grazer populations. Hypersaline con-ditions generally have adverse effects on bothmetazoan grazers such as copepods and on pro-tozoan grazers (Buskey and Stockwell 1993; Buskeyet al. 1998) so the decline in salinities in BaffinBay and Laguna Madre to the 20–30 psu range atthe three stations of this study from October 1997through April 1998 (Fig. 3) might be expected tohave positive effects on grazer populations. How-ever there was only a temporary increase in micro-zooplankton populations, followed by a decline atour stations during this period (Fig. 7) and a dras-tic decline in abundance of copepod nauplii dur-ing October 1997 and January 1998, followed bypronounced increase in abundance in April 1998(Fig. 7). Although populations of adult and juve-nile (copepodite) copepods were generally low inOctober 1997 and January 1998, this would notseem to explain the drastic decline in abundanceof nauplii. One possible explanation is that the di-atom bloom in October 1997 (long, thin Rhizoso-lenia spp.), were not suitable food for the cope-pods, and egg production rates dropped. Bothphytoplankton biomass (Fig. 4) and microzoo-plankton abundance (Fig. 7) were low in January1998, also suggesting a poor food supply for co-pepods. The correlation between adequate foodsupply and egg production in copepods has beenwell established (e.g., Checkley 1980; Ambler1986).

The original goal of this study was to examinethe population dynamics of A. lagunensis and theirplanktonic grazers, and the balance betweengrowth of the brown tide and grazing pressure inareas severely impacted by the brown tide, in ad-jacent unimpacted areas, and in transition areasbetween the two extremes. If A. lagunensis inhibit-ed the growth and grazing of protozoans at highbrown tide concentrations, brown tide growthshould have exceeded zooplankton grazing in ar-eas impacted by the brown tide, while grazing on

brown tide may have exceeded its growth in tran-sition waters not severely impacted by the browntide. We anticipated a gradient of increased micro-zooplankton biomass and total community grazingimpact as we moved through the transition zonefrom areas heavily impacted by the brown tide toareas that were unaffected. This pattern existedonly during the first cruise in July 1997. However,heavy rains in October 1997 broke down the browntide gradient that had persisted for much of theprevious 8 yr, and no clear relationship was foundbetween brown tide density (Fig. 4) and microzoo-plankton grazing (Table 1) at the lower brown tidedensities found through most of this study. Duringall dilution experiments phytoplankton growthand grazing were either nearly in balance, or graz-ing exceeded growth (Fig. 8). However, our esti-mates of phytoplankton growth from dilution ex-periments may have been too low if nutrients be-came limiting at higher dilutions due to reducednutrient regeneration by microzooplankton. TheLaguna Madre experienced a series of blooms ofother phytoplankton species during our study, sug-gesting that grazing was not always an effective con-trol of phytoplankton populations in the LagunaMadre during this year of rapidly changing salini-ties.

It has generally been accepted that it was an un-usual combination of events that lead to the initi-ation of the extraordinarily persistent brown tidebloom, and therefore it was thought that once thebloom disappeared, it would not easily return. Itwas originally hypothesized that the initiation ofthe A. lagunensis bloom in January 1990 was dueto the combination of an extended period ofdrought leading to severe hypersalinity in the La-guna Madre and a severe freeze and resulting fishkill that released a large pulse of nutrients (Whit-ledge 1993; DeYoe and Suttle 1994). Subsequentanalysis of archived samples with an immunofluo-rescence assay suggest that disruption of grazerpopulations induced by hypersalinity may have al-lowed the bloom to initiate before the freeze (Bus-key et al. 1999), although the nutrient pulse re-sulting from the fish kill certainly may have accel-erated growth. When the bloom was flushed fromthe Laguna Madre in the fall of 1997, and popu-lations of A. lagunensis declined to backgrounddensities (Buskey et al. 1999), it was not expectedto return. As salinities slowly increased in the fol-lowing year, so did brown tide populations. Dis-rupted grazer populations may again partly explainthe increase in brown tide population (Buskey etal. 1997), but the steady increase in brown tidepopulations through a series of blooms of otherphytoplankton species and fluctuations in grazerpopulations, suggests that other factors might be

Texas Brown Tide Decline and Recovery 345

contributing to the resilience of this bloom. Al-though nothing is known about the life cycle ofthis alga, if a resting stage did exist, it could bepresent in immense numbers in the Laguna Madrefollowing the eight-year bloom. A reservoir of rest-ing cells in the sediment could make the recoveryof the brown tide almost inevitable. Research onthe life history of A. lagunensis is needed to addressthis question.

ACKNOWLEDGMENTS

This work was supported by the Texas Higher Education Co-ordinating Board under grant 003658-019, and by the NationalScience Foundation under grant OCE-9529750. Technical assis-tance was provided by Brian Wysor during the first cruise. DeanStockwell and Terry Whitledge collected water samples prior tothe first cruise for determining brown tide distribution. TracyVillareal assisted with identification of species from the diatombloom. We thank Texas Parks and Wildlife Department for shar-ing their salinity data from Baffin Bay, the King Ranch for rain-fall data, and Lisa Campbell for use of her flow-cytometer. Thisis University of Texas Marine Science Institute contributionnumber 1172.

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Received for consideration, March 13, 2000Accepted for publication, December 20, 2000