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Planktonic Standing Crop and Nutrients in a Saltern Ecosystem Author(s): Barbara J. Javor Source: Limnology and Oceanography, Vol. 28, No. 1 (Jan., 1983), pp. 153-159 Published by: American Society of Limnology and Oceanography Stable URL: http://www.jstor.org/stable/2836155 . Accessed: 14/06/2014 23:18 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. . American Society of Limnology and Oceanography is collaborating with JSTOR to digitize, preserve and extend access to Limnology and Oceanography. http://www.jstor.org This content downloaded from 195.34.79.20 on Sat, 14 Jun 2014 23:18:34 PM All use subject to JSTOR Terms and Conditions

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Page 1: Planktonic Standing Crop and Nutrients in a Saltern Ecosystem

Planktonic Standing Crop and Nutrients in a Saltern EcosystemAuthor(s): Barbara J. JavorSource: Limnology and Oceanography, Vol. 28, No. 1 (Jan., 1983), pp. 153-159Published by: American Society of Limnology and OceanographyStable URL: http://www.jstor.org/stable/2836155 .

Accessed: 14/06/2014 23:18

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

American Society of Limnology and Oceanography is collaborating with JSTOR to digitize, preserve andextend access to Limnology and Oceanography.

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Page 2: Planktonic Standing Crop and Nutrients in a Saltern Ecosystem

Notes 153

Limnol. Oceanogr., 28(1), 1983, 153-159 ? 1983, by the American Society of Limnology and Oceanography, Inc.

Planktonic standing crop and nutrients in a saltern ecosystem'

Abstract-The brines in the seawater con- centrating ponds and NaCl crystallizing ponds of the Exportadora de Sal saltern contain little dissolved nitrate, ammonia, and phosphate. The phytoplanktonic standing crop in the con- centrators is relatively low and kept in check by brine shrimp grazing. The concentration of red halophilic bacteria in the crystallizers is dependent on brine density. Bacteriorhodop- sin is present. Bitterns ponds are relatively nutrient-rich but apparently are devoid of life.

The seawater flow-through systems of many commercial salterns include a wide gradient of habitats, ranging from sea- water of brackish or normal composition to highly concentrated brines in which no organisms can be detected. The species of some salterns have been iden- tified (Carpelan 1957; Davis 1978), but although seasonal changes in productiv- ity and nutrient levels in a narrow range of salinities in a saltern were document- ed by Carpelan, data integrating the whole system are scarce.

In the halite crystallizing ponds, the fi- nal downstream communities are com- posed of halophilic bacteria which derive nutrients that pass through all the up- stream stages from the seawater source. Although these bacteria have been exten- sively investigated in the laboratory (see reviews by Dundas 1977; Kushner 1978; Stoeckenius 1978; Lanyi 1979), field studies have been relatively rare. This study is a preliminary investigation of some of the relationships between stand- ing crop, nutrients, and productivity through the planktonic habitat gradients of the Exportadora de Sal, S.A. (ESSA) saltern.

I thank W. Stoeckenius for reading the manuscript.

Ionic analyses of the brines were pro-

'Research was conducted while B.J.J. was a con- sultant for Exportadora de Sal, S.A.

vided by ESSA. Reactive phosphate, re- active nitrate, nitrite (Strickland and Par- sons 1972), and ammonia (Solorzano 1969) were analyzed. For these analyses, con- centrated brines were diluted with dis- tilled water before the addition of re- agents. For phosphate, nitrate, and nitrite analyses, crystallizer and bitterns brines were diluted by a factor of 11/2-3. For am- monia analyses, all brines were diluted to 12.50 Be. Samples were read in a spec- trophotometer (Bausch and Lomb Spec- tronic 20).

For chlorophyll a measurements, sam- ples were filtered onto GF/C glass-fiber filters (Whatman) and extracted in the dark at 40C in methanol saturated with MgCO3. Extracts were read at 667 nm, using an extinction coefficient of 75.0 li- ters mol-h cm-' (Lenz and Zeitzschel 1968).

Oxygen was measured by the azide modification of the Winkler method (Strickland and Parsons 1972). Brine den- sities were measured with Baume (Be) scale hydrometers, and all readings were corrected to 15.50C.

Enrichments for bacteria in the crys- tallizer and bitterns brines were made in the complex medium of Oesterhelt and Stoeckenius (1974). Brines were also streaked directly on agar plates with the medium of Sehgal and Gibbons (1960) or an equivalent medium substituting 5 g liter-' tryptone (Bacto) for the casami- no acids. All enrichments were incubated at 370C under a tungsten or fluorescent light. The liquid enrichments were main- tained on a rotary shaker (125 rpm). In- ocula for the enrichments were collected from both the NaCl crystallizer brines and the bitterns brines.

Cells were counted in a Levy im- proved Neubauer counting chamber. For particulate protein measurements, brines were centrifuged at 39,000 x g for 30 min at 40C. For the crystallizer and bitterns

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Page 3: Planktonic Standing Crop and Nutrients in a Saltern Ecosystem

154 Notes

80 K+

zo 0 0 ~ ~ ~ ~ ~~~-5 - + 2 0No

4 12 20 28 36 Brine density (?Be)

Fig. 1. Concentrations of dissolved ions in ESSA brines. Calcium was not analyzed. Curve for cal- cium was calculated from data of Herrmann et al. (1973).

brines, the pellet was washed once in a basal salt solution consisting of (per liter distilled water): 250 g NaCl, 20 g MgSO4 7H2O, 2 g KCl, and 2 g Na citrate, pH 7.4. The pellets were solubilized in 1 ml of 1% sodium dodecylsulfate (SDS). Protein was determined according to Lowry et al. (1951) with the modification of the addi- tion of SDS to a final concentration of 1% in solution A. A bovine serum albumin standard was used.

For bacteriorhodopsin determinations, samples were prepared by centrifuging 4 liters of each brine sample at 39,000 x g for 30 min at 4?C and washing the pellet in basal salt solution. The pellets were thoroughly drained and dissolved in 5 ml of distilled water plus ca. 0.1 mg of DNase (Sigma). To prevent bacterial contami- nation of the lysates during preparation, I added a 2% NaN3 solution to a final con- centration of 0.02%, and the samples were stored at 4?C. The lysates were centri- fuged at 480 x g for 15 min at 4?C to re- move the inorganic precipitates.

The bacteriorhodopsin concentrations in the lysates were determined by light- adapted vs. dark-adapted difference spectra on a Cary 14R or a Beckman MVI spectrophotometer (Bogomolni et al. 1980). The extinction coefficient of the maximum difference in absorbance near 580 nm was calculated to be 12,000 li- ters mol-l cmn-.

The ESSA saltern is on the Pacific coast in Guerrero Negro, Baja California Sur, Mexico (28?N, 114?W). Seawater is pumped into the system from Laguna Ojo de Liebre. The ESSA saltern con- sists of a series of 13 interconnected seawater concentrating ponds (19,627 ha),

- 20 _o0 0 0

-D 10-

I600 U) 0 @

50 *-

c 60

i3 0 0 ZC 60 .-

4 40 - ;

260 2.

O ~~~~ *

10 15 0 5 30 BO

010 2 03 0 10 30 5O MMg

Brine concentration

Fig. 2. Bacteriorhodopsin, cell counts, and par- ticulate protein in ESSA brines. Bacteriorhodopsin (bR) was measured in March (0) and June (0) 1981. Cell count data are for October 1980. Only cells in the crystallizer and bitterns brines were counted. Particulate protein data are for June 1981 (except for the open circle at 33.20 Be, which was measured in March 1981).

over 40 crystallizing ponds for halite pro- duction (2,465 ha), and several bitterns ponds for the recovery of magnesium and potassium salts (347 ha). Ponds are usu- ally -1 m deep. The major ions of the brines are shown in Fig. 1. Baume scale values of seawater density approximately equal percent dissolved solids until the stage of NaCl saturation is reached (25.50 Be; abscissa in Fig. 2 shows comparison with Mg2+ concentrations). By the time the brines have reached this stage (nearly 11/2 years in passage), almost all calcium has precipitated, primarily as gypsum. NaCl of >99.8% purity precipitates in the density range of about 26?-290 Be. As sea- water concentrates further, potassium and magnesium salts coprecipitate with the halite. By the time the brines reach a density of about 310 Be, they are pumped to the bitterns ponds.

The climate is arid, with rainfall gen- erally averaging <5 cm yr-'. The tem- peratures are mild; brine temperatures vary between 190 and 300C (midmorning) during the year. Strong offshore winds as

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Page 4: Planktonic Standing Crop and Nutrients in a Saltern Ecosystem

Notes 155

v/ 0 Artemia

Fabrea

> Trichocorixa c

k Aphanothece (benthic) ] Oscillatoriaceans (benthic)

Navicula (benthic)

a) Striatella

Grammatophora

Licmophora

Enteromorpha

o I IV V Vl VIII IX X

5? 10? 15? 20?

Brine density ('Be')

Fig. 3. Distribution of important algal and in- vertebrate species in saltern concentrating ponds. Roman numerals refer to concentrator number.

well as morning and afternoon fog tend to lessen the effects of the seasonal changes in temperatures.

The important algae and invertebrates of the concentrating ponds are listed in Fig. 3. The fauna and flora of the first con- centrating pond, especially near the pumps from the lagoon, largely resem- bled those of Laguna Ojo de Liebre: a variety of fish, red and green algae, and the ditch weed Ruppia. Most of the pond floor was dominated by the green alga Enteromorpha and Ruppia. Diatoms oc- curred in the plankton, as epiphytes, and as a film on the sediment: Licmophora, Navicula, Grammatophora, and Striatel- la. Seawater in the pond was 4o-50 Be. Planktonic chlorophyll a concentrations ranged from 0.7-4.5 ,ug liter-l, both in July 1979 (Fig. 4). Because the ponds were about 1 m deep, these data repre- sent chlorophyll a concentrations per 0.1 cm2 and can thus be compared with the benthic chlorophyll a concentrations in the same figure.

The fourth and fifth concentrators (brines ca. 6?-10? Be) were characterized by firm bottom mats consisting primarily of several species of Oscillatoriaceae and one chroococcalean, Aphanothece halo- phytica. A film of diatoms (Navicula) cov- ered the mats. The planktonic chloro- phyll a concentrations ranged from 2.3

c 20

_~~~ ~ ~ A_ E 1

Q_ _

_' A o I

4? 6? 8? 10? 12? Brine density (?Be)

Fig. 4. Chlorophyll a in the plankton and ben- thic mats in concentrating ponds. Points represent plankton collected between June 1979 and January 1980. June *; July-O; October-A; November- A; December-U; January-O. Roman numerals refer to concentrator number, boxes represent range of chlorophyll a concentrations measured in the mats (May 1979) and approximate range of seawater den- sities in each pond.

,ug liter-1 in June 1979 to 16.1 in January 1980. The fauna consisted primarily of a ciliate (Fabrea salina), waterboatmen (Trichocorixa; Corixidae), and occasional fish.

The bottom mats were very similar in composition until the ninth concentrator (:13' Be), where gypsum cement floors the ponds. No bottom mat occurred in ponds of higher brine densities although A. halophytica colonized some of the gypsum.

Brine shrimp (Artemia salina) were found in the concentrators in the density range of about 10?-20? Be (concentrators 6 through 10, 11, or 12, depending on the season). The animals were rarely found in concentrations higher than about one per liter, except on the leeward shores of the ponds. They reproduced by bearing live young all year. Egg production was uncommon.

Primary productivity of the plankton in the concentrators was low (Table 1). Planktonic chlorophyll a was essentially zero in concentrator 6 (the first pond with Artemia) and in all later concentrators and crystallizers. In July 1979, the productiv- ity of the mats in ponds 5 and 6 (mea- sured in their respective brines) was 0.08 and 0.05 mg 02 *g Chl a-' h-', rates sim- ilar to those of the plankton in ponds 1 through 5 during June.

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Page 5: Planktonic Standing Crop and Nutrients in a Saltern Ecosystem

156 Notes

Table 1. Planktonic productivity in ESSA seawater concentrators expressed as mg 02 liter-'* h-'. Val- ues for June are also expressed as mg O2 ,ug Chl a-' h-' (Chl a). Assay was performed by the light and dark bottle technique with four replicates of each. Samples were incubated in several centimeters of water in the concentrators from which they came. Incubation period was 1 or 2 h near midday. Incubation temperatures ranged from a low of 17?C (pond 6 in May) to a high of 300C (ponds 5, 6, and 9 in October).

Concentrating ? Be May Jun Jun Jul Oct pond Avg (Chl a)

1 entrance 4.7 0.08 0.15 0.07 0.06 0.04 1 exit 5.4 0.49 0.12 0.04 0.06 0.03 4 exit 7.4 0.15 0.19 0.06 0.05 0.04 5 exit 9.5 0 0.02 0.04 0.06 0.07 6 exit 11.8 -0.08 0 0 -0.05 0 9 exit 14.2 -0.13 -0.06 0 -0.02 0

Between the densities of about 220 and 310 Be, red halophilic bacteria dominated the ecosystem. The halophilic green alga, Dunaliella, was virtually absent. Obser- vations of the field material, of the en- richments, and of the colonies on agar plates showed that the dominant bacteria were rods (up to ca. 10 ,m long) that re- semble Halobacterium (Gibbons 1974). The species were not determined. The square bacteria noted by Walsby (1980) were also present. Other square bacteria have been isolated (Javor et al. 1982). SrSO4 (determined by X-ray diffraction) precipitated around the rods, especially in the more concentrated NaCl crystalliz- er brines. The precipitate occurred as bi- lobate or dumbbell-shaped bundles of crystals up to about 10 ,tm long. Cell counts (including cells with the precipi- tate) for October 1980 are given in Fig. 2.

Particulate planktonic protein concen- trations for the whole saltern system in June 1981 are also shown in Fig. 2. The suspended organic material in the first concentrating pond (50 Be) did not form a compact pellet upon centrifugation, and it was therefore not amenable to analysis by the method used. Visually, the floc that did pellet seemed quite sparse. The high particulate protein concentration at about 7.50 Be was due to a bloom of Fabrea sa- lina. The peak between about 270 and 300 Be was attributable to halophilic bacte- ria.

Bacteriorhodopsin concentrations in distilled water lysates of cells from the crystallizer brines were determined in March and June 1981 (Fig. 2). Spectra of

the lysates had absorption peaks at 540, 503, 475, and 390 nm. These peaks are identical to those of bacterioruberin, the dominant carotenoid of halobacteria.

Analyses of the brines over the course of a year show that in the concentrating ponds there was no measurable phos- phate in the system and combined nitro- gen was present in low concentrations (Fig. 5). Reactive nitrate was always pres- ent in low concentrations at the seawater inlet but was typically absent in the rest of the system until the crystallizer stage. Nitrite was never present. Ammonia was generally present in low concentrations throughout the concentrators. Between 40 and about 260 Be, although there was sea- sonal variability in planktonic chloro- phyll a, no seasonal variability in phos- phate and combined nitrogen was detected.

In the NaCl crystallizers (260-30 or 310 Be), which were colored pink by halo- bacteria, phosphate, nitrate, and ammo- nia concentrations increased over those in the seawater concentrating ponds. Oxygen was absent or nearly absent (use of the analytical method was difficult in solutions of such high salinity). As the brines further concentrate and the bac- teria die, the color of the brine changes from turbid pink to clear green (the nat- ural color of the brine in the absence of bacteria). At 320 Be and higher densities, brines are green. In these brines (bit- terns), phosphate, nitrate, and ammonia concentrations increased dramatically. Although the greatest values were re- corded in winter, they were not consis-

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Page 6: Planktonic Standing Crop and Nutrients in a Saltern Ecosystem

Notes 157

JM 10.0 000

8.0 0 0

6.0 0 0 o 0~~~~~~~~~~~~~~~~~~~~~~~~~C

L 4.0

2.0 800o o

c o? o

3 0 o000

20 0

Z 10 0 ? o

o9i 0 0

~p0~P. ~ Q x,~b 0 0 _~~~~~~~~~~ o* ob 000 06

40 0

z I 0 0

0 0 0 0

Z 20 0 0

00 0 0

0 00 0o o

oQO 00 0 0 0 0 0

0O0cr 00,%g0 0 O00OeO,

40 80 120 160 200 240 280 320 360

B r i n e d e n s i t y ( 0 B 'e) Fig. 5. Reactive phosphate, reactive nitrate, and ammonia concentrations in ESSA brines. Data were

collected monthly for 1 year during 1979 and 1980, and all months are represented.

tently high nor were summer values all low.

No bacteria grew in the enrichments nor on the agar plates with inocula from the bittems. Little or no particulate pro- tein was detected. The "cells" that were counted were the SrSO4 crystals that had previously precipitated around rods. The bitterns were apparently devoid of life.

The fauna and flora of the ESSA saltern is typical for salterns and hypersaline bodies (Carpelan 1957; Nissenbaum 1975; Post 1977; Davis 1978). It is noteworthy that Dunaliella was absent from the crys- tallizers although it was occasionally found in ponds peripheral to the saltern system.

None of the studies cited describes standing crop or productivity per unit chlorophyll a. In a San Francisco saltern,

measurements of productivity in terms of mg 02 liter-' h-' were generally much higher than those of the ESSA saltern, with values ranging up to about lOx (Carpelan 1957). Combined nitrogen and reactive phosphate were similarly much higher in that saltern. Some error in the ESSA study may have arisen from the method of 02 measurement (Walker et al. 1970).

Brine shrimp populations, planktonic chlorophyll a, and dissolved nutrients are relatively low in comparison to those in a saltern in Chula Vista, California, where brine shrimp are commercially harvested (Javor unpubl.). Brine shrimp popula- tions are also dense enough to be com- mercially harvested in the saltern de- scribed by Carpelan (1957). The phytoplankton of the ESSA saltern ap-

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Page 7: Planktonic Standing Crop and Nutrients in a Saltern Ecosystem

158 Notes

pear to be nutrient-limited until the brines reach the stage of halite precipitation. The brine shrimp in turn are limited by the phytoplankton since they are filter feed- ers and do not graze the algal mats. The virtual absence of planktonic chlorophyll a in the concentrators where Artemia thrives suggests that the brine shrimp keep the phytoplankton completely in check.

Nutrient depletion by the algal mats must be at least partially responsible for the relatively low productivity of the phytoplankton. Because the mats accrete, nutrients would be permanently trapped. However, if the benthic mats were the only sink of dissolved nutrients in the con- centrators, then there probably could not be high populations of bacteria in the crystallizers.

The increase in concentrations of phos- phate, nitrate, and ammonia in the crys- tallizer and bitterns brines is due to de- composition of the bacteria and further brine concentration. Although halobac- teria do produce ammonia (Dundas and Halvorson 1966), the pathways that might produce nitrate in the system have not been explored.

Changes in brine density affect the ap- parent standing crop of halobacterial populations. The bacteriorhodopsin data do not fit as neat a curve as the cell count and protein data (Fig. 2) because the low concentrations of the pigment are near the limit of detection by the analytical meth- od. The greatest concentration of bacte- riorhodopsin was 2.2 nM, which is more than three times the concentration mea- sured in the Dead Sea (Oren and Shilo 1981). This peak occurs in brines of slightly lower density (28?-29? Be) than those for protein and cell counts (290-30O Be). A study of the productivity of these bacteria would determine whether the cells in the denser brines are viable. Halobacteria are primarily aerobic het- erotrophs and they use bacteriorhodop- sin for light-mediated ATP synthesis un- der conditions of low oxygen. The inability to maintain sufficiently high concentrations of this pigment may limit the success of the cells in :290 Be brines

where 02 iS virtually absent. The some- what higher cell counts and protein con- centrations in 29? and 30? Be brines may reflect passive concentration by evapo- ration, while further brine concentration promotes cellular breakdown or the pre- cipitation of dead cells encased in salt crystals.

The apparent inability of the bacteria to survive in the bitterns in spite of high nutrient concentrations is probably due to changes in various ion concentrations and to low water activity. Between 28? and 29? Be, Na+ concentration falls below 3.5 M, and at 320 Be, it is only 2.5 M. Between 28? and 290 Be, Mg2+ increases from 1.0 to 1.5 M, and at 320 Be, it is >2.5 M. An isolate from this saltern did not grow in medium with -2.5 M Na+ nor in medium with :2 M Mg2+ (Javor et al. 1982). The water activity at 250C de- creases from 0.72 to 0.69 between 280 and 290 Be, and it is only 0.63 at 320 Be (Roth- baum 1958). The previously reported low water activity limit for a microbe (a fun- gus) is 0.66 (Scott 1957). The calculated ionic strength increases from about 8.5 to about 10 between 280 and 300 Be, and it increases even more in the bitterns due to high concentrations of Mg2+ and S042-. In addition, detrimentally low or high concentrations of certain trace elements or growth factors may limit the bacteria.

This preliminary investigation pro- vides a basis for studies now underway concerning the chemistry and biology of halobacterial environments. An ecologi- cal study of the productivity of halobac- teria and the factors that enhance and limit their success in nature is needed to cor- roborate evidence from laboratory inves- tigations of the physiology of these mi- croorganisms.

Barbara J. Javor

Scripps Institution of Oceanography, A-002

University of California, San Diego La Jolla 92093

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W. STOECKENIUS. 1980. Action spectrum and

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Page 8: Planktonic Standing Crop and Nutrients in a Saltern Ecosystem

Notes 159

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Submitted: 18 February 1982 Accepted: 24 August 1982

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