an analysis of factors influencing the primary production of the benthic microflora in a southern...

Netherlands Journal of Sea Research 17 (1)." 126-144 (1983)

AN A N A L Y S I S O F F A C T O R S I N F L U E N C I N G T H E P R I M A R Y P R O D U C T I O N O F T H E B E N T H I C

M I C R O F L O R A IN A S O U T H E R N C A L I F O R N I A L A G O O N

by

G.P. SHAFFER* andC.P. ONUF Marine Science Institute, University of California, Santa Barbara CA 93106, USA

C O N T E N T S

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . 126 2. Materials and Methods . . . . . . . . . . . . . . . . . . . . . . 127

2.1. The study site . . . . . . . . . . . . . . . . . . . . . . 127 2.2. Hourly gross primary productivity . . . . . . . . . . . . . . 130 2.3. Chlorophyll, light and grain size . . . . . . . . . . . . . . . 131 2.4. Statistical analyses . . . . . . . . . . . . . . . . . . . . . 132

3. Results and Discussion . . . . . . . . . . . . . . . . . . . . . 133 3.1. Yearly patterns of the measured variables . . . . . . . . . . . 133 3.2. Statistical analyses . . . . . . . . . . . . . . . . . . . . . 135 3.3. The determinants of primary production and its distribution . . . . 139

4. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . 142 5. References . . . . . . . . . . . . . . . . . . . . . . . . . . . 143

1. I N T R O D U C T I O N

There is wide recognit ion that the p r imary product ion of benthic microflora is impor tant in shallow-water and periodically flooded habitats. Repor ts are available for Arctic subtidal m u d bot tom (MATHEKE & HORNER, 1974), north temperate lake shores and bot- toms (WETzEL, 1964; HARGRAVE, 1969; HUNDING, 1971), intertidal flats (PAMATMAT, 1968; LEACH,1970; MARSHALL, OVIATT • SKAUEN, 1971; CADI~E t~Z HEGEMAN, 1974, 1977; RIZNYK, EDDENS ~Z LIBBY, 1978), salt marshes (POMEROY, 1959; GALLAGHER & DAIBER, 1974; VAN RAALTE, VALIELA • TEAL, 1976; ZEDLER, 1980), subtropical and tropical subtidal sediments (BUNT, LEE & LEE, 1972). A great deal of variability occurs, e.g. the data of MARSHALL el al. (1973) show coeffi- cients of variat ion of ~ 100 in measurements of hourly productivi ty, while annual estimates differed as much as fourfold for the same shoal habitats in ne ighbour ing estuaries of New England, U .S .A. Also,

* Present address: Center tor Wetland Resources, Louisiana State University, Baton Rouge LA 70803, USA.

PRIMARY PRODUCTION IN A LAGOON 127

there is great variety in the factors suggested to be important in deter- mining the level of primary productivity, ranging from light availabili- ty through temperature of the water, chlorophyll concentration, nutrients, to grain size (POMEROY, 1959; WILLIAMS, 1962; PAMATMAT, 1968; MARGRAVE, 1969; HICKMAN & ROUND, 1970; LEACH, 1970; MARSHALL, OVIATT ~Z SKAUEN, 1971; RIZNYK ~Z PHINNEY, 1972; CADI~E • HEGEMAN, 1974, 1977; VAN RAALTE, VALIELA & TEAL, 1976; RIZNYK, EDDENS & LIBBY, 1978; ZEDLER, 1980).

The aim of the research reported here was to add to an explanation of the great variation in measurements of primary production by quantifying features of the heterogeneity of physiographic units that might influence primary production. This was accomplished by sampling frequently at a wide variety of spatial scales within and between substrate types, and measuring light, temperature, pigment concentration, grain size and community respiration coincident with the determinations of productivity. These data were subjected to analysis of variance to identify spatial patterns, the auto-regressive moving average (ARMA) process to trace temporal patterns, and multiple linear regression to find which variables explained most of the variance.

Acknowledgements.--We thank Commander, U.S. Naval Air Sta- tion, Pt Mugu, California, for permission to conduct research in the lagoon, and base biologist Ron now and meteorologist Bob DeViolini for providing essential support data. Peter Cahoon, Michael Caponigro, Jill Cermak, and Millicent Quammen assisted with different aspects of the research. Peter Cahoon, Robert Holmes, John Melack and Barbara Pr6zelin commented on earlier versions. This research was sponsored in part by NOAA, National Sea Grant Col- lege Program, Department of Commerce, under Grants # 04-7-158-44121 and NA80AA-D-00120 Projects # R/CZ33A and 52 through the California Sea Grant College Program, and the California State Resources Agency.

2. M A T E R I A L S A N D M E T H O D S

2. 1. THE STUDY SITE

The study was conducted in the eastern part of Mugu Lagoon (34 ° 06' N, 119 ° 05'W) which is an ecological reserve; access is limited primarily to researchers. The eastern arm (WARME, 1971) of the lagoon comprises approximately 50 ha of the 300 ha wetland expanse

128 G . p . S H A F F E R & C . P . O N U F

Fig. 1. Map of Mugu Lagoon indicating areas that are always submerged (black), submerged by neap high tides (dark stippling), submerged by spring high tides (light stippling) and never submerged (no stippling), b. The eastern arm of the lagoon with

the sampling sites and the area covered by salt marsh.

(Fig. 1). One half of the eastern a rm is emergent salt marsh domina ted by Salicornia virginica, one quar te r is intert idal sand and m u d flats, and one quar te r is pe rmanen t ly subtidal. T h e lagoon m o u th is open to the ocean year round. Tidal flushing occurs to vary ing degrees daily but not all tides affect the lagoon because of the mixed semidiurnal tidal regime in the adjacent Pacific Ocean and a sill in the mou th at about M e a n Sea Level. The m a x i m u m tidal ampl i tude is - 3 m outside the lagoon and half that inside. Fresh water input is low except following heavy precipitat ion. The only pe rmanen t fresh water input is f rom Calleguas Creek (Fig. 1) discharging into the western part . Conse- quent ly , the salinity of the water within the eastern part approximates that of the open ocean (i.e. 33.8; MAcGImTIE & MAcG1NITIE, 1969) almost all of the time.

A total of 17 stations located along 6 transects (Fig. 1) encompassed both intertidal and subtidal areas, as well as the lagoon 's full comple- ment of sediment composit ions. General ly , sediments become finer grained f rom west to east (away from the mouth) and from south to north (away from the sandspit). Pr ior to February , 1978, even the

P R I M A R Y P R O D U C T I O N I N A L A G O O N 199

finest g ra ined sed iments in the eas te rn a r m were mos t ly sand, with only a small m u d fract ion. H o w e v e r , torrent ia l ra in s torms du r ing the win te r of 1978 (the second wettest season in 113 years of local meteoro logica l records) caused a deposi t ion of up to 50 cm of ex- clusively silt and clay in the deepest par t s of the lagoon. T h e stations included in the s tudy were affected differential ly by the deposi t ion. Al though a fivefold increase in silt and clay occur red at Stat ions 1 to 4 (Fig. 2b), the change to f iner sediments was short-l ived. Wi th in 3

% I00"

50

I00"

/,_...": :. / / /

c

15 d5 0125 0125 (~b6;

b . . ,

.: ' / , / : .: / . /

,:- /

f/ / /

J f , , f

d

I0 05 0.'25 0.1~25 o;B2rnm

Fig. 2. Cumulative percentage of sediment size fractions before (solid), during (dash- ed) and after (dotted) the major storms (J.P. CERMAK, unpublished results), a. For stations which changed from coarse- to fine-grained sediment (Stations 5 and 6). b, For stations which changed from coarse- to intermediate- and again coarse-grained sediment (Stations 1 to 4). c. For stations which changed from intermediate- to fine- grained sediment (Stations 8 to 15). d. For stations which experienced little to no sedi-

ment deposition (Stations 7, 16 and 17).

mon ths the a rea rever ted back to a p r e d o m i n a n t l y sandy condi t ion (Fig. 2b). O n l y a par t ia l revers ion to the p re - s to rm state occur red at Stat ions 5 and 6 (Fig. 2a), while Stat ions 8 to 15 r ema ined covered with a b lanket of fine part icle sed iments (Fig. 2c). Little to no deposi- t ion occur red at Stat ions 7, 16, and 17 (Fig. 2d) which were located at l andward extremit ies .

130 G . P . S H A F F E R & C . P . O N U F

2. 2. H O U R L Y G R O S S P R I M A R Y P R O D U C T I V I T Y

The hourly gross primary productivity of the benthic microflora was estimated by following changes in dissolved oxygen concentrations in transparent and opaque chambers, using a modification of the Winkler technique (STRICKLAND & PARSONS, 1968). The experiments were conducted between 09.30 and 15.30 hours local time. The measurements were thus made under a variety of conditions as the measurement dates were scheduled a month in advance.

Sediment samples in plastic Petri dishes, 19.3 cm diameter, were placed in 2 incubation chambers constructed from transparent polycarbonate cylinders (Nalgene Ecochambers cut in half, 16.4 cm inner diameter, 11.7 cm height). Dark chambers were made by wrap- ping with black vinyl tape over a coat of black paint. Temperatures in light and dark chambers were equalized to within 1 o C by empirically adjusting the proportion of white and black on the outer surfaces of the dark chambers.

During incubation, chambers were placed in the water of the lagoon at or near the sample site to simulate natural conditions. Every 15 minutes the water was mixed by slowly moving a rod attached through the top of each chamber to a transparent plate inside, as some water movement always was evident near the bottom of the lagoon, even on calm days under slack water conditions, and in preliminary experiments production was 25% less in chambers not stirred. The depth of water above the chambers varied according to tidal pattern, but never exceeded 25 cm.

Along with each set of incubation chambers, three 300 ml BOD bottles were filled with sea water from the container used to fill the chambers. One of the bottles was immediately fixed to ascertain the initial dissolved oxygen concentration (one determination of initial dissolved oxygen sufficed as multiple samples proved to be uniform). The other BOD bottles (1 light and 1 dark, the dark bottle covered with aluminum foil) were incubated alongside the chambers as con- trols to determine oxygen production and consumption by residual phytoplankton in the filtered sea water.

At the termination of incubation, the temperature of the water next to the sediment core was measured and two 300 ml samples were removed from each chamber using a Mityvac hand vacuum pump. The samples were immediately fixed and placed in the dark until titrated in the laboratory. The sediment cores were taken to the laboratory for analysis of plant pigments and sediment composition.

Early in the study large gas bubbles sometimes were present in chambers at the end of incubation. Microgasometric analyses

P R I M A R Y P R O D U C T I O N IN A L A G O O N 131

( S c H O L A N D E R a al., 1955) indicated that the bubbles were only 22% oxygen (SHAFFER, 1982). They appeared to result from seepage of air trapped in pockets either between the sediment core and the Petri dish or within the sediment core. After the source of the bubbles was discovered, they were dislodged before incubation by gently tapping the sample-plus-dish on a hard object, and it was concluded that no important loss of oxygen from water due to supersaturation did occur.

2. 3. C H L O R O P H Y L L , L I G H T A N D G R A I N S I Z E

Sediment samples were collected for pigment analysis from each sediment core used in the primary production measurements. From March 1977 through January 1978, duplicate samples were collected using a plexiglass dish (5.0 cm inside diameter, 0.5 cm depth, 0.002 m 2 area) pressed into the sediment, inverted, levelled and washed in- to test tubes. From February 1978 through June 1978, a sampling device was used which simultaneously removed 13 subsamples (each 1.4 cm inside diameter, 0.5 cm depth, 0.002 m 2 pooled area) from each sediment core. All samples were frozen ( -14°C) .

For pigment extraction, samples were thawed, the overlying water drawn off, and the sediment ground twice with magnesium carbonate buffered 90% acetone for 3 minutes in a Waring blender with an Eberbach Semi-micro Container. The blending container was placed into an ice bath prior to each grinding to minimize temperature rise generated by friction. The pigment extract was brought to 200 ml with additional buffered acetone, and absorbance measured at 750, 663, 645, and 630 nm using a Bausch and Lomb Spectronic 70 in 1 or 10 cm path-length cuvettes. After acidification with 1 N HC1 (50 #1 for 1 cm cells, 150 #1 for 10 cm cells), second measurements were made at 750 and 663 nm to distinguish between chlorophyll a and phaeophytin a.

REIMANN (1978) found that acidification to more than 3 x 10 -3 tool. 1-1 can cause changes in absorbance between 600 and 750 nm due to spectral changes in carotenoids (primarily fucoxanthin), resulting in significant error. In this study, 1.7 x 10 -2 mol • 1-1 HC1 was used, probably resulting in less than 10% error (REIMANN, 1978: table 1).

Preliminary analysis indicated that two grindings extracted 91% of the pigment. Pigment concentrations were calculated according to the formulas of STRICKLAND ~Z: PARSONS (1968) and LORENZEN (1967), ad- justed for extraction efficiency.

Light was measured either with a LI -COR Model 185-A quantum meter or with an Eppley 8-48 pyranometer. The two instruments were


intercalibrated by taking simultaneous readings of sun plus sky on 10 occasions. The empirically determined conversion factor was 1 W - m -~ (pyranometer) = 2.25 /xE. m -2 • s -I (quantum meter). This agrees well with the theoretically derived values of McCREE (1972) and HANSEN & BRINGS (1979) of 1 W - m - 2 = 4 . 5 7 and 4.6 #E. m -2 • s -1, respectively, since half of the irradiance measured by the pyranometer corresponds to the photosynthetically active region (RvTHER, 1956) measured by the quantum meter.

Sediment grain size distributions were determined by wet sieving through a graded series of screens, drying and weighing the fractions. For the initial characterization of sites, 75 cm 2 x 1.5 cm deep samples were separated into fractions of 1 ~ ranging from < -2 cI, to > 4 cI, using United States Standard Sieves. Subsamples of incubated cores similar to those used for pigment analyses (20 cmZx 0.5 cm deep) were wet-sieved through Mechanical Soil Analysis Sieves to determine changes in sediment characteristics during the course of the study.

2. 4. S T A T I S T I C A L A N A L Y S E S

Several stepwise linear regressions were performed (Dixon & B~OWN, 1979: B M D P 2 R program) to determine the relative importance of 6 independent variables in explaining the variation in the hourly productivity of the benthic microflora; viz. chlorophyll a, solar radiation, water temperature, sediment composition (% coarse grain, or that re- tained by a 0.25 mm mesh sieve), benthic community respiration and initial dissolved oxygen. The coefficient of multiple determination (R 2) is the statistic that estimates the cumulative proportion of the variability in the dependent variable explained by the independent variables.

First, the stepwise regression was performed using all measurements from each station pooled together. Then, to determine whether the independent variables affected the dependent variable differently for the benthic microflora inhabiting different types of areas, stations which experienced similar changes in sediment composition during the study were categorized together (Fig. 2a to d). Three categories were established according to the proportion of silt and clay ( < 63/xm; FOLK, 1968: 25) in a sample: (1) coarse, < 10% silt and clay, (2) intermediate, 10% to 30% silt and clay, (3) fine, > 3 0 % silt and clay. To determine whether the independent variables changed in relative importance through time, samples were grouped by month, and each month analyzed separately. Since standard transformations on the data did not better meet the assumptions of the analysis (for instance normality), all analyses were carried out on untransformed data.

P R I M A R Y P R O D U C T I O N IN A LAGOON 133

To provide information on the extent and scale of patchiness of the benthic microflora, analyses of variance were performed on chlorophyll concentration between subsamples (centimetres), between samples (decimetres), between stations (metres to tens of metres), and within and between substrate types. To investigate temporal variation in the standing crop of the benthic microflora, the chlorophyll data were grouped by month and also subjected to analysis of variance. In addition, the standing crop data and each independent variable were subjected to a multi-channel autoregressive moving average (ARMA) process (ULRYCH • BISHOP, 1975; ULRYCH & CLAYTON, 1976). This procedure was used to determine the optimum amount of previous data necessary to accurately track the standing crop through time, resulting in an indication of how often measurements need be obtain- ed temporally. See SHAFFER (1982) for a more detailed description of methods and results.

3. RESULTS AND DISCUSSION

3. 1. YEARLY P A T T E R N S OF THE M E A S U R E D V A R I A B L E S

Distinct temporal patterns in gross production are apparent (Fig. 3a). Generally, temporal fluctuations in chlorophyll a levels resemble those of production (r = 0.48, p<0 .001 , n = 316) in having highest values in spring and summer and lowest during the winter (Fig. 3a and d). Although chlorophylls b and c cannot be determined reliably in sediments by the procedure used (because they cannot be distinguish- ed from pigment degradation products probably present), the abrupt, large and persistent change in the ratio of chlorophyll a to chlorophylls b and c between January and February suggests a change in com- munities, reflecting an increased blue-green component (PARSONS & TAKAHASm, 1973). This change coincided with the storm-caused alteration of lagoon sediments to finer grain size (Section 2.1).

Sediment types were significantly different in chlorophyll a content (Tables 1 and 2). In spite of the large differences in chlorophyll a con- tents between sediments, productivities were identical when all data were included. For the period that all sediment types were present simultaneously (February to July 1978), the trend in productivity ac- tually was opposite that of chlorophyll (Table 1).

Respiration of the benthic community (macroinvertebrates and fish only rarely present), was measured from June 1977 through July 1978, by following changes in dissolved oxygen in dark chambers. Besides following the same general temporal patterns as hourly pro-

134 G . P . S H A F F E R & C , P . O N U F

duct ivi ty ( r = 0 . 3 9 , p < 0 . 0 0 1 , n = 3 4 8 ) , hour ly respira t ion also cor- related highly significantly with t e m p e r a t u r e of the wa te r (r = 0.43, p < 0 . 0 0 1 , n = 3 4 8 , Fig. 3a, c and e). O x y g e n consumpt ion rates g rouped by sediment type show a p r o n o u n c e d grada t ion in respira t ion f rom high in fine sediments to low in coarse sediments (Table 1); however , they tended to follow the same t empora l pa t te rn . T h e ap- pea rance of the m u d c o m m u n i t y and absence of the sand c o m m u n i t y in F e b r u a r y 1978 is a consequence of the m a j o r s to rm-re la ted sedi- men t deposi t ion. T h e m u c h higher respira t ion measu red in J u n e and

mg m'Z-h I

50 //

25

O

C °C I

15] • ~ug.g "1

0 .I) mg m'2-h 1

e

2

mg V

J J A S O N D J F M A M J J -

Fig. 3. Temporal variations measured; averages with 1 x standard error (bars) over all stations, a. Hourly gross carbon productivity (rag-m -2. h-~). b. Photosyn- thetically active radiation (#E - m ~ - s-~). c. Temperature of the water next to the sediment core (°C). d. Chlorophyll a (with standard error, left axis, #g. g-~) and the ratio of chlorophyll a to chlorophyll b and c (without standard error, right axis), e. Benthic community respiration of carbon (rag-m -~- h-~). f. Initial dissolved oxygen

concentration (rag. 1-~).


TABLE 1

Mean (~) and standard error (se) of carbon and chlorophyll values grouped by season and sediment type of gross productivity (rag. m -2 - h-l), chlorophyll a (/~g- (g dry sediment)-l), benthic community respiration and net benthic community productivi-

ty (mg- m -2 • h -l)

Period Sediment n Gross Chloro- Community Net community type production phyll respiration production

(rag" m -2" h -1) (#g. g- l ) (rag' m -z" h -1) (rag rn -2" h -1)

se ~ se ~ se ~ se

Summer (J, J, A) all 70-78 81 7.2 29 4.9 20 3.0 61 6.9 Autumn (S, O, N) all 76 59 5.4 13 1.8 14 2.3 45 5.2 Winter (D, J, F) all 64-66 33 4.5 10 2.0 15 2.5 18 4.7 Spring (M, A, M) all 72-82 86 8.2 26 4.7 30 3.1 56 8.6 Summer (J, j) all 24-44 99 17.4 17 4.0 46 7.0 53 17.2

Jun 77-Jul 78

Feb-Jul 78

coarse 102-110 73 5.2 11 1.2 13 1.9 60 4.0 medium 158-172 70 2.5 20 1.6 24 1.1 44 3.0

fine 56-66 63 4.0 32 3.7 40 2.3 23 4.1 coarse 24-30 116 9.7 9 0.5 27 6.0 89 5.3

medium 42-52 82 5.1 18 1.7 27 1.5 55 3.7 fine 56-66 63 4.0 32 3.7 40 2.3 23 4.1

J u l y 1978 than in the same months of 1977 (Fig. 3e) presumably is a residual effect at most sites of the storm-caused deposition of fine sediments in February 1978.

T hough net productivi ty of the benthic microflora was not measurable, net p r imary product ivi ty for the benthic communi ty as a whole is. Over the entire year, the net benthic communi ty product ion in coarse-grained sediments averaged twice as high as in fine-grained sediments, and was even greater for post-deposition months (Table 1). For the daylight hours, net benthic communi ty product ion was 83 % of gross benthic microfloral product ion in the coarse-grained areas, 64% in the areas with intermediate sediments, and 42% in the fine sediments.

3, 2. S T A T I S T I C A L A N A L Y S E S

When the data from all stations were pooled, the l inear regression of hour ly productivi ty on 6 independent variables (Table 3) accounted for only 38% of the variat ion in the dependent variable. All the independent variables excluding initial dissolved oxygen concentrat ion were highly significant ( p < 0.01) in the equation. Chlorophyll a was the most impor tant variable affecting hour ly productivity, explaining 23 % of the variability. Al though the individual correlations between product ion and solar radiat ion and water temperature were highly significant, account ing for 16 % and 18 % of the variability respective-

136 G.P. SHAFFER & C.P. ONUF

TABLE 2 Analyses of variance on chlorophyll a content grouped in the following entries: (1) between months, (2) between all stations, (3) between different sediment types, (4) between stations with coarse sediments, (5) between stations with intermediate sediments, (6) between stations with fine sediments, (7) between replicate cores from stations with coarse sediments, (8) between replicate cores from stations with intermediate sediments, (9) between replicate cores from stations with fine sediments, (10) between replicate subsamples from sediment cores randomly chosen from all sediment types or from intermediate sediments. Significance levels p< 0.05 (*), p <

0.01 (**), p<0.001 (***).

Variation between: df F

(1) Months 12, 136 2.31"* (2) Stations 16, 132 5.80*** (3) Sediment types 2, 146 5.33** (4) Stations (coarse sediment) 5, 41 7.57*** (5) Stations (intermediate sediment) 9, 61 3.65** (6) Stations (fine sediment) 6, 20 2.83* (7) Replicate cores (coarse) 3, 123 0.47 (8) Replicate cores (intermediate) 3, 183 4.33" * (9) Replicate cores (fine) 3, 60 1.49

(10) Replicate subsamples (all) l, 30 0 15 (all) 1, 30 0.01 (all) 1, 30 0.00 (intermediate) 1, 30 0.00 (intermediate) 1, 30 0.11

ly, together they explain only 12% of the var ia t ion in product iv i ty . This suggests a large covar iance be tween the two factors, which was borne out in a cluster analysis on the independen t var iables (D ixon & BROWN, 1979: p r o g r a m B M D P I M ) . Solar radia t ion and water t e m p e r a t u r e fo rm the t ightest cluster a m o n g all the var iables (r = 0.73, p < 0 . 0 0 1 ) .

O n the a s sumpt ion that the l um p i ng of sites with different characteris t ics migh t be part ial ly responsible for the low resolut ion of the mult iple regression pe r fo rmed on pooled data , stepwise regressions were pe r fo rmed on stations g rouped by history of changes in sediment compos i t ion (Table 3). Solar radia t ion was the mos t impor - tant var iable affecting product iv i ty for stations which were least affected by sediment deposi t ion and those which were affected most drastically (coarse to fine stations). Al though in bo th groups solar radia t ion accounted for more than half of the total expla ined var ia t ion, chlorophyll a, water t empe ra tu r e , and benthic c o m m u n i t y respi ra t ion were a lmost as highly corre la ted with the dependen t var iable . As in the pooled regression analysis, the relat ively small cont r ibut ions of these latter 3 var iables to the total expla ined var iance is indicat ive of an in te rdependence a m o n g the " i n d e p e n d e n t " variables.


T A B L E 3

Corre la t ion coefficient (r), F value and cont r ibut ion of 6 independent variables to the coefficient of mult iple de te rmina t ion (R 2) for explaining the variat ion in gross productivi ty of the benthic microflora; all data pooled and data g rouped for areas with the same his tory of changes in sediment type after s torm. Significance levels p < 0.05

(*), p < 0 . 0 1 ( * ' ) , p<O.O01 (***).

Variables Correlation coefficient (r) Contribution to R 2 F value

All data pooled (n = 316) Chlorophyl l a 0.48" * * 0.23 94.1 * * Solar radiat ion 0.40 * * * 0.08 34.7 * * T e m p e r a t u r e 0.43"** 0.04 19.0"* Sediment type 0.00 0.01 5.1 * * Respi ra t ion 0.29"** 0..01 5.2"* Initial dissolved oxygen - 0 . 0 6 0.00 2.2* Total 0.38

Area with coarse changing to fine sediment (n = 50) Solar radia t ion 0.66" * * 0.44 33.1 * * Chlorophyl l a 0.63"** 0.19 21.6"* T e m p e r a t u r e 0.62"** 0.04 5.6"* Respi ra t ion 0.59"** 0.04 4.9"* Initial dissolved oxygen - 0.09 0.03 4.5" * Sediment type - 0.13 - - Total 0.74

Area with coarse, changing to intermediate , back to coarse sediment (n = 76) Respi ra t ion 0.78"** 0.61 117.2"* T e m p e r a t u r e 0.47*** 0.05 10.5"* Solar radiat ion 0.30** 0.01 1.6 Initial dissolved oxygen - 0.16 0.01 3.1 * Sediment type - 0.12 0.01 2.1 Chlorophyl l a 0.24 - - Total 0.69

Area with intermediate sediment du r i ng the whole s tudy (n = 66) Solar radiat ion 0.59*** 0.35 34.6** Respi ra t ion 0.57 * * * 0.14 1 7 . 6 " *

T e m p e r a t u r e 0.56"** 0.02 2.4 Chlorophyl l a 0.47 * * * 0.04 6.1 * * Sediment type - 0.21 0.03 3.8" * Initial dissolved oxygen 0.04 0.03 3.8** Total 0.60

Area with in termedia te changing to fine sediment (n = 124) Chlorophyl l a 0.57" * * 0.33 58.9" * T e m p e r a t u r e 0.38" * * 0.05 9.1 ** Solar radiat ion 0.32" * * - - Resp i ra t ion 0.15 - - Sediment type 0.07 - - Initial dissolved oxygen - 0 . 0 8 - - Total 0.37


For the coarsest gra ined sediments which increased fivefold in silt and clay content and rever ted back to the pre-depos i t ion condit ion within 3 mon ths (Fig. 2b), the d o m i n a n t por t ion of the total expla ined var ia t ion (61 out of 6 9 % , T a b l e 3) was a t t r ibutable to benthic com- m u n i t y respirat ion. In contrast , benthic c o m m u n i t y respira t ion does not enter the equa t ion for the stations with the finest gra ined sediments (Fig. 2c, Tab l e 3) where chlorophyll a accounted for 33 out of 37 % of the total expla ined var ia t ion in hour ly p roduc t ion (and does not enter the equa t ion for the coarsest gra ined stations).

W h e n t empora l var ia t ion was min imized by g roup ing the da ta by mon th , the expla ined var ia t ion in hour ly produc t iv i ty was general ly high (between 50% and 93% for 11 of 14 months ; Tab l e 4). Chlorophyl l a was indicated to be the most consistently impor t an t var iable inf luencing hour ly product iv i ty (first to enter the regression for 4 out of 13 months , and high individual correlat ion for mos t months) , but each of the independen t var iables was most impor t an t dur ing at least one m o n t h (Table 4).

Several analyses of var iance on chlorophyll a content of the sediments were p e r f o r m e d (using B M D P 2 V , D i x o n & BROWN, 1979). T h e analyses showed highly significant differences in t empora l (between months) and spatial (be tween stations) var ia t ion (Table 2).

Significant differences also resulted f rom a compar i son of the var ia-

T A B L E 4

The first independent variable to enter, its correlation coefficient, the coefficient of multiple determination (Total R 2) and the F value of multiple linear regression of 6 independent variables on gross productivity for data grouped by month (no chlorophyll a data were collected during July 1978). Significance levels p < 0.05 (*),

p<O.O1 (**), p x 0.001 (***).

Month Independent variable Correlation Total F value coefficient R:'

Jun Chlorophyll a 0.67 0.93 11.6* * Jul Initial dissolved oxygen -0.45 0.54 3.2* Aug Water temperature 0.41 0.22 1.1 Sep Water temperature 0.44 0.78 14.6" * * Oct Water temperature 0.70 0.76 9.1 * ** Nov Community respiration 0.31 0.39 1.4 Dec Chlorophyll a 0.58 0.56 3.6* J an Chlorophyll a 0.51 0.72 6.4" * Feb Community respiration 0.55 0.85 10.7" * * Mar Chlorophyll a 0.46 0.50 3.5* Apr Community respiration 0.37 0.17 0.7 May Solar radiation 0.54 0.68 5.5" * Jun Sediment type 0.52 0.65 4.7 * * Jul Sediment type 0.71 0.69 5.7" *

P R I M A R Y P R O D U C T I O N IN A LAGOON 139

tion in chlorophyll a content between different sediments (Table 2). The between-stations variation within each sediment type diminished from coarse to intermediate to fine sediments (Table 2). The variation in chlorophyll a content between replicate cores taken within 1 m was significant for intermediate sediments, but not for coarse or fine sediments (Table 2). Finally, no significant differences were found in the variation of chlorophyll a content between subsamples from sediment cores taken within 5 cm of one another for 3 trials of 10 randomly chosen stations (4 cores per station, 2 replicates per core, and for 2 similar trials of 80 cores of intermediate sediment composition, Table 2).

A phase lag of one resulted in all cases when the A R M A process (ULRYCH • BISHOP, 1975; ULRYCH & CLAYTON, 1976) was performed on the standing crop (and productivity) data coupled with each independent variable measured. Thus the relationship between the independent variables and the abundance and productivity of the benthic microflora appears to be Markovian (due to the large gap between sample dates), since the only useful prediction window encompasses measurements during the same day. Consequently, a monthly sampling frequency for each station is probably insufficient to track all temporal patterns. Therefore, unmeasured peaks and troughs in benthic microfloral abundance and productivity may have occurred during this study.

3. 3. THE D E T E R M I N A N T S OF P R I M A R Y P R O D U C T I O N AND ITS

D I S T R I B U T I O N

The results of this study indicate that any of a wide variety of factors can become most important in explaining primary production, depending on time of year and other conditions. Consequently, when data were pooled and a stepwise regression was performed, an undif- ferentiated blend resulted. This occurred because a small contribution to the total explained variation in productivity for one area or time was averaged with a large contribution for the same independent variable in another area or at a different time.

The differences in factors controlling production among sites, in some cases corresponded to obvious environmental differences. For example, heterotrophic bacterial and meiofaunal populations tend to increase with an increasing silt and clay fraction (RIZNYK & PnINNEV, 1972; RHEINHEIMER, 1977). Thus, the benthic microflora will com- prise a decreasing proportion of the total benthic community as sediments become finer, and the lowest correlations between productivity and benthic community respiration would be expected and were

140 G.P. SHAFFER & C.P. ONUF

observed in the finest sediments. We speculate that the unmeasured activities of the heterotrophic fraction of the benthic community also account for the low total explained variation (37%) in the finest sediments.

Analogously, the responses of the benthic microflora to incident radiation might be different between locations because light is less like- ly to be limiting in coarse-grained intertidal and subtidal areas with typically clear overlying water than in areas of fine-grained sediments where even slight turbulence leads to high turbidity. In the latter case, the benthic microflora might compensate for the lower levels of light reaching the sediment surface by incorporating higher concentrations of pigments into the light harvesting complexes, i.e. higher chlorophyll a per cell content (HALLDAL & FRENCH, 1958; BRODY ~1; EMERSON, 1959; BROWN ~; RICHARDSON, 1968; HALLDAL, 1970; JORGENSEN, 1970, 1972; MANDELLI, 1972; PRI~ZELIN, 1976). Consistent with this interpretation, we found chlorophyll a concentrations in fine sediments to be double those in intermediate sediments and triple those in coarse sediments while the opposite was true for productivity during the period that all sediment types were present simultaneously (February to Ju ly 1978, Table 1).

The effects of water temperature on benthic microfloral production were similar for the different sediment types. This is a result of the oc- currence at Mugu Lagoon of all sediment types in similar proportions from highest to lowest elevations. Regardless of sediment type, water temperature will be highest in shallow areas and lowest in deep areas when ambient air temperature and insolation are high, and the opposite will be true for low ambient air temperature and insolation.

Nutrients were not measured in this study but have been shown rarely if ever to limit benthic microfloral production in areas free of vascular plants (WILLIAMS, 1962; VAN RAALTE, VALIELA • TEAL, 1976). In the presence of marsh plants, nutrients have been shown to limit benthic microfloral production, but only when the vascular plants are growing rapidly.

When temporal variation was minimized by grouping the data by month, the total explained variation in hourly productivity usually was quite high. Each of the 6 independent variables used in the analysis explained most of the variation during at least one month. This suggests that different factors are important at different times as well as at different locations and further explains why the analysis on the pooled data for the whole year is so uninformative. These temporal changes are consistent with the potential for rapid turnover in benthic microfloral populations, increasing the chance of changes in community composition. In this study, the most obvious change in corn-

P R I M A R Y P R O D U C T I O N I N A L A G O O N 141

munity composition coincided with the deposition of silts and clays, whereupon organisms containing chlorophylls b and c become scarce, suggesting a benthic microflora dominated by blue-green algae.

One of the major problems of accurately estimating the total productivity of the benthic microflora, and not addressed explicitly in previous studies, deals with the great heterogeneity in space and in time of the benthic microfloral standing crop. Spatially, the within substrate, between station variation in standing crop decreased from coarse to intermediate to fine sediments. Two factors may account for this gradient. Firstly, predictable (incoming and outgoing) tidal cur- rents predominate over coarse sediments whereas t u r b u l e n t water movements generated by variable breezes predominate in areas of fine sediments. Secondly, the fine sediments are much more easily disturb- ed. Apparently the combination of turbulent water m o v e m e n t and easily suspended sediments leads to much more homogeneously distributed microflora than the regime of faster but more predictable water movements, presumably allowing the microflora to migrate into the harder to suspend sediments.

The within sediment, between replicate sample variation in chlorophyll a content was only significant for intermediate grained sediments. This was expected since the greatest within station topographical relief occurs in these areas. Characteristic mounds and troughs occur with the troughs containing a visibly denser microfloral film. Significant spatial patchiness never occurred in the within core, between subsamples comparisons.

This analysis in space suggests that it is important to carry out regular measurements from several sample sites within each sediment type, since significant variation in microfloral standing crop occurred both between and within sediment types. Since the variation was never significant for samples taken with a 15 cm core, and since only rarely were samples within 1 m significantly different from one another, it is of greater importance to sample from a large area within each sediment type.

Unlike the spatial sampling protocol, information is not available on the frequency at which measurements need be carried out to observe all temporal patterns in productivity. The A R M A process revealed that samples were not collected often enough during this study. The only data that could accurately track productivity on any one day, were data measured during the day in question (i. e. the opt imum window region was one, and all measurements were made in duplicate). Consequently, unobserved trends could have occurred in the productivity of the benthic microflora.

In conclusion, benthic microfloral production is highly variable in


large part because different factors can be most important in deter- mining the levels of production in different locations and at different times. By dint of extensive and systematic sampling, we have been able to explain the majority of the observed variability in terms of these locational and temporal differences. Pooling data to obtain whole area or annual estimates destroys much of the power to discriminate the sources of variation.

4. SUMMARY

From June 1977 through July 1978 duplicate monthly determinations of benthic microfloral production were made at different locations along 6 parallel transects located at different distances from the mouth of Mugu Lagoon, California, so that locational as well as sediment and tidal height relationships could be examined. Multiple regression analysis performed on the entire data set showed that the independent variables chlorophyll a, solar radiation, water temperature, community respiration, sediment composition, and initial dissolved oxygen accounted for remarkably little of the observed variation (38%). In separate analyses the data set was decomposed by month and by sediment history (a major storm completely changed the bottom characteristics of the lagoon about half way through the study) to elucidate the apparent failure of intuitively important factors in deter- mining the level of production. For the individual categories, the variance explained was generally much higher (mean 60%), and, of particular significance, different independent variables were most important for different categories, thus accounting for the poor resolu- tion of the multiple regression analysis on pooled data. In the monthly categorization, each of the 6 independent variables was most important during at least one month. Light or chlorophyll was most important only in 5 of 14 months.

Comparisons between subsamples (centimetres), samples (decimetres), stations (metres to tens of metres) and within and between sediment types were used to investigate the spatial distribution of benthic microflora as measured by pigment concentrations. Significant variability never occurred in samples collected within 1 m of one another. Spatial heterogeneity was greater as the sediments became coarser. Chlorophyll concentrations were lower in coarser sediments; however, gross primary production did not vary according to sediment type. Communi ty respiration was half as much in coarse as in fine sediment.

PRIMARY PRODUCTION IN A LAGOON 143

5. R E F E R E N C E S

BRODY, M. & R. EMERSON, 1959. The effect of wavelength and intensity of light on the proportion of pigments in Porphyridium cruentum.--Amer. J. Bot. 45: 433-440.

BROWN, T.E. & F.L. RmHARDSON, 1968. The effect of growth environment on the physiology of algae: light intensity.--J. Phycol. (U.S.) 4: 38-55.

BUNT, J.S., C.C. LEE & E. LEE. 1972. Primary productivity and related data from tropical and subtropical marine sediments.--Mar. Biol. 16: 28-36.

CADGE, G.C. &J. HEOEMAN, 1974. Primary production of the benthic microflora liv- ing on tidal flats in the Dutch Wadden Sea.--Neth. J. Sea Res. 8: 260-291.

- - - - , 1977. Distribution of primary production of the benthic microflora and ac- cumulation of organic matter on a tidal flat area, Balgzand, Dutch Wadden Sea.--Neth. J. Sea Res. 11: 24-41.

DIXON, W.J. & M.B. BROWN, 1979. BMDP biomedical computer programs P-series 1979. Univ. of Calif. Press, Los Angeles: 1-880.

FOLK, R.L., 1968. Petrology of sedimentary rocks. Hemphills, Austin: 1-170. GALLAGHER, J.T. & F.C. DAIBER, 1974. Primary productivity of edaphic algal com-

munities in a Delaware salt marsh.--Limnol. Oceanogr. 19: 390-395. HALLDAL, P., 1970. The photosynthetic apparatus in microalgae and its adaptation

to environmental factors. In: P. HALLDALL. Photobiology of microbiology. Wiley Interscience, New York: 17-56.

HALLDAL, P. & C.S. FRENCH, 1958. Pigment formation and growth in blue-green algae in crossed gradients of light intensity and temperature.--Physiologia P1. 11: 401-420.

HANSEN, M.C. & W.W. BRIGGS, 1979. LI-COR brochure DS-1180. LI-COR, Box 4425., Lincoln, Nebraska 68504, U.S.A.

HARGRAVE, B.T., 1969. Epibenthic algal production and community respiration in the sediments of Marion Lake.--J. Fish. Res. Bd Can. 26: 2003-2026.

HICKMAN, M. & F.E. ROUND, 1970. Primary productivity and standing crops of epipsammic and epipelic algae.--J. Phycol. (U.S.) 5 (2): 247-255.

HUNDINO, C., 1971. Production of benthic microalgae in the littoral zone of a eutrophic lake.--Oikos 22: 389-397.

JORGENSEN, E.G., 1970. The adaptation of planktonic algae: IV. Light adaptation in different algal species.--Physiologia P1. 22: 1307-1315.

- - - - , 1972. The adaptation of planktonic algae: V. Variation in photosynthetic characteristics of Skeletonema costatum cells grown at low light intensity.-- Physiologia Pl. 23: 11-17.

LEACH, J.H., 1970. Epibenthic algal production in an intertidal mudflat.--Limnol. Oceanogr. 15: 514-521.

LORENZEN, C., 1967. Determination of chlorophyll and pheo-pigments: spectrophotometric equations.--Limnol. Oceanogr. 12: 343-346.

MAcGINITIE, G.E. & N.L. MACGINITIE, 1969. A report on Mugu Lagoon.-- Tabulata 2: 15-24.

MANDELLI, E.F., 1972. The effect of growth illumination on the pigmentation of a marine dinoflagellate.--J, Phycol. (U.S.)8: 367-369.

MARSHALL, N., C.A. OVIATT & D.M. SKAUEN, 1971. Productivity of the benthic microflora of shoal estuarine environments in southern New England.--Int. Revue ges. Hydrobiol. 56: 947-956.

MARSHALL, N., D.M. SKAUEN, H.C. LAMPE & C.A. OVIATT, 1973. Primary production of benthic microflora. In: A guide to measurement of marine primary production under some special conditions. Unesco Monogr. Oceanogr. Methodol. 3: 37-44.

144 G.P. SHAFFER & C,P, ONUF

MATHEKE, G.E.M. & R. HORNER, 1974. Productivity of the benthic micro-algae in the Chukchi Sea near Barrow, Alaska.---J. Fish. Res. Bd Can. 31: 1779-1786.

McCREE, K.J., 1972. Test of current definitions of photosynthetically active radiation against leaf photosynthesis data.--Agric. Met. 10: 443-453.

PAMATMAT, M.M., 1968. Ecology and metabolism of a benthic community on an intertidal sand flat.--Int. Revue ges. Hydrobiol. 53: 211-298.

PARSONS, T. & M. TAKAHASHI, 1973. Biological oceanographic process. Pergamon Press, New York: 1-186.

POMEROV, L.R., 1959. Algal productivity in salt marshes of Georgia.--IAmnol. Oceanogr. 4" 386-397.

PR~Z~L1N, B.B., 1976. The role of peridinin-chlorophyll a - proteins in the photosynthetic light adaptation of the marine dinoflagellate Glenodinium sp.--Planta 130: 225-233.

RAALTE, C.D. VAN, I. VALIELA & J 'M" TEAL, 1976. Production of benthic salt marsh algae: light and nutrient limitation.--Limnol. Oceanogr. 21: 862-872.

REIMANN, B., 1978. Carotenoid interference in the spectrophotometric determination of chlorophyll degradation products from natural populations of phytoplankton.--Limnol. Oceanogr. 23:1059-1066.

RHEINHEIMER, G., 1977. Aquatic microbiology. John Wiley, New York: 1-184. RIZNVK, R., J.I. EDDENS & R.C. LIBBV, t978. Production of epibenthic diatoms in

a southern California impounded estuary.--J. Phycol. (U.S.) 14: 273-279. RlZNYK, R. & H.K. PrtINNEY. 1972. Manometric assessment of interstitial microalgae

production in two estuarine sediments.--Oecologia 10: 193-203. RVTUER, J .H. , 1956. Photosynthesis in the ocean as a function of light intensity.--

Limnol. Oceanogr. 1: 61-70. SCHOLANDER, P.F., L. VAN DAM, C.L. CLAFF &J.W. KANW1SHER, 1955. Microgaso-

metric determination of dissolved oxygen and nitrogen.--Biol. Bull. mar. biol. Lab., Woods Hole 109: 328-334.

SHAFFER, G.P., 1982. Primary production of the benthic microflora in a southern California estuary. M.A. thesis, University of California, Santa Barbara: 1-135.

STRmKI.ANn, J.D. & T.R. PARSONS, 1968. A practical handbook for seawater analysis.--Bull. Fish. Res. Bd Can. 167:1-311.

ULRVCH, T.J. & T.N. BISHOP, 1975. Maximum entropy spectral analysis and autoregressive decomposition.--Rev. Geophys. 13: 183-200.

UI.RYCH, T.J. & R.W. CLAYTON, 1976. Time series modelling and maximum entropy.--Phys, earth planet. Interiors 12: 188-200.

WARME, J.E., 1971. Paleoecological aspects of a modern coastal lagoon.--Univ, of California Publs in Geological Sciences 87: 1-131.

WETZEI., R.G., 1964. A comparative study of the primary productivity of higher aquatic plants, periphyton, and phytoplankton in a large, shallow lake.--Int. Revue ges. Hydrobiol. 49: 1-61.

WILLIAMS, R.B., 1962. The ecology of diatom populations in a Georgia salt marsh. Ph.D. thesis, Harvard Univ.: 1-143.

ZEDLER, J.B., 1980. Algal mat productivity: comparisons in a salt marsh.--Estuaries 2: 122-131.

an analysis of factors influencing the primary production of the benthic microflora in a southern...

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