Phytoplankton crops, bacterial metabolism and oxygen in saanich inlet, a fjord in Vancouver Island, British Columbia

Sedimentary Geology, 36 (1983) 117-130

I 17

Elsevier Science Publishers B.V., Amsterdam - Printed in The Netherlands

PHYTOPLANKTON CROPS, BACTERIAL METABOLISM AND OXYGEN IN SAANICH INLET, A FJORD IN VANCOUVER ISLAND, BRITISH COLUMBIA

LOUIS A. HOBSON

Department of Biology, University of Victoria, Victoria, B. C V8W 2 Y2 (Canada) (Accepted for publication May 16, 1983)

ABSTRACT Hobson, L.A., 1983. Phytoplankton crops, bacterial metabolism and oxygen in Saanich Inlet, a fjord in Vancouver Island, British Columbia. Sediment Geol., 36:117-130. Phytoplankton crops in Saanich Inlet were characterized by their content of photosynthetic pigments and by their taxonomic compositions, from early April to mid-December, 1981. Crop sizes were correlated to particle volumes , bacterial activities, and oxygen concentrations at all depths to test the hypothesis that the degradation of sinking phytoplankton debris by bacterial production results in anoxia. Particles produced during the spring bloom were rich in chlorophyll a and pheopigments, which disappeared as particles sank deeper in the water column. The volume of particles, with sizes ranging from 2.0 to 40 # m , was dominated by those with a mean size of about 32 #m. Qualitatively, m a n y of the particles were frustules of the two diatom genera, Thalassiosira and Chaetoceros, which dominated crops in the euphotic zone. No temporal changes in either qualities or quantities of photosynthetic pigments were observed in anoxic sediments. A positive correlation between particle volume and bacterial production was observed. However, no correlation between production and changes in dissolved 02 was seen in the deep water prior to mid-June. Further observations were masked by flushing that occurred in August and may have begun as early as mid-June.

INTRODUCTION

Most fjords in western Canada are oxygenated throughout the year (Pickard, 1975), a result of their river-driven turbulent circulation. However, waters below the sill in Saanich Inlet, a fjord with minimal river flow in southern Vancouver Island, may become anoxic at depths greater than 100 m. The fjord is long and narrow with a maximum depth of about 200 m separated from the Strait of Georgia by a sill at 75 m (Herlinveaux, 1962). Anoxia occurs because oxygen-consuming reactions exceed replacement of oxygen by turbulent diffusion. Consumption is due, in part, to animal respiration. Benthic animals are found down to a depth of 130 m (Tunnicliffe, 1981) and zooplankters to 150 m (Bary, 1966). However, zooplankton biomass is concentrated during the day in the oxycline, which usually occurs 0037-0738/83/$03.00

© 1983 Elsevier Science Publishers B.V.

lib

between 85 and 130 m (Bary, 1966). About 30% of oxygen consumption in the oxycline has been attributed to zooplankton respiration (Devol. 1981), while no estimates for benthic animal respiration are extant. In addition to respiration, Herlinveaux (1962) postulated that sinking organic debris, primarily from phytoplankton and benthic algae, led to anoxia, presumably caused by bacterial degradation of the debris (Richards, 1965). However, this postulate has never been tested. The purpose of the present study was to begin testing Herlinveaux's postulate by describing the particles resulting from phytoplankton production and by measuring the accompanying bacterial activity in Saanich Inlet. Particles larger than about 2 /zm were characterized by their content of photosynthetic pigment and degradation products of pigments, and by their volumes and size frequencies within the range from 2.0 to 40 /~m. Bacterial activity was assessed and correlated to variations in particles and oxygen concentrations. M ETHODS A N D MATERIALS

Cruises were carried out tri-weekly from early April to mid-December, 1981. Stations 1 and 2 were occupied at each end of the deep central trench, about 2 km long, in the inlet (Fig. 1). Water samples were collected by Niskin bottles at 0, 5, 25, 50, 100, 150 and 200 m, and samples of bottom sediments were taken by a Van Veen grab. Samples for chlorophyll a and pheopigment analyses were filtered through MgCO 3 treated Gelman type A glass-fiber filters, which were stored at - 2 0 ° C in a dark desiccator for a maximum of one week. Samples for the taxonomy and carbon content of phytoplankton were treated with Lugol's iodine solution. Samples for bacterial activity and particle volume and size frequency measurements were stored at 2°C in darkness until laboratory analyses were carried out either on the day of or day after each cruise. Sediments removed from the surface layer of mud captured by the Van Veen grab at the two stations were stored at - 2 0 ° C in the dark until being freeze-dried. Beginning in May, only one sample was taken from the central trench and another was taken (station 3) from sediments at 80 m (Fig. 1). Concentrations of chlorophyll a and pheopigments were determined with the spectrophotometric method and equations described by Lorenzen (1967). Phytoplankton taxonomy and cellular carbon contents were estimated with the aid of an inverted microscope by methods outlined in Hobson et al. (1973). Bacterial activity was assessed by a method using incorporation of (methyl-3H) thymidine (53 Ci m m o l - 1, ICN Corp.) as a tracer of D N A synthesis. Five ~1 of thymidine was added to each 20-ml seawater aliquot with a control treated by 0.7 I~M HgC12. Aliquots were incubated for 3 h in darkness at an average temperature for the upper 10 m of Saanich Inlet, characteristic for each cruise. All other manipulations followed the work of Fuhrman et al. (1980). Final results were reported as nmoles thymidine incorporated into D N A 1 - ~ h 1. Particle volume in the size range from 2.0 to 40 ~ m was measured by a Model T A I I Coulter Counter equipped with a 100-t~m aperature

119

"'~i"+i

/

,~rag'

123"30'

Fig. 1. Chart of Saanich Inlet with isobaths (m) showing positions of stations 1 and 2 over anoxic sediments and station 3 over oxygenated sediments.

120

tube. Volumes were separated into size ranges with mean diameters of 2.25, 2.85, 3.60, 5.70, 7.20, 9.00, 11.4, 14.4, 18.0, 22.5, 28.5 and 36.0/~m and percentages of the total volume were calculated. Particle sizes of sediments were also determined with the Coulter Counter by the above method. The identity and quantity of photosynthetic pigments in the sediments were determined. Lipid soluble pigments were extracted from freeze-dried sediments into 90% acetone/water, then concentrated into anhydrous diethyl ether and separated by two-dimensional chromatography following methods described by Jeffrey (1968). Spots on chromatograms were characterized by their positions relative to solvent fronts and by their absorption spectra, which were determined by a Beckman Model DU-8, UV-VIS, single-beam spectrophotometer. Oxygen concentrations in seawater were determined by the Winkler technique (e.g. Strickland and Parsons, 1968) rather than by the method of Broenkow and Cline (1969) because the odor of H2S was never detected in seawater from any depth during this study. The masking effect of horizontal spatial variations in particles on temporal and vertical variations had to be removed. To do this, data from stations 1 and 2 were considered to be simultaneous, and those from identical depths were used as duplicates. To determine confidence limits ( p = 0.05), values were selected from the two cruises for which maximum ranges in any variable over depth were observed. In all cases variances were related to means of data and this dependency was removed prior to analysis of variance by transformations based on a power function calculation (Taylor, 1961). Confidence limits were used to contour data over depth and time. RESULTS Phytoplankton chlorophyll a increased in early April, culminating in concentrations greater than 10/~g 1 ~ at 5 m in late April and May (Fig. 2). These crops were dominated by two genera of centric diatoms, Thalassiosira and Chaetoceros spp. (Table I). Thereafter, concentrations of pigment in the upper 10 m decreased. reaching 1.3/~g 1- i by mid-July and subsequently varied between 0.1 and 1.3/~g 1 These crops were dominated by dinoflagellates and nanoflagellates (Table I). Water below 25 m was characterized by pigment concentrations varying between 0.1 and 1.3/~g I i from early April to early June. By late June, levels became undetectable at depths greater than 150 m and remained so until late August (Fig. 2). Then, concentrations increased and varied between 0.1 and 1.3 /~g 1 ~ during the remainder of the year. Considerable numbers of chloroplast-bearing cells of the centric diatom genera, Melosira and Skeletonema, the pennate diatom genus, Nit~chia, and nano-flagellates as well as unidentified centric diatoms occurred in the deep water from early April to mid-August (Table II). Pheopigments were detected at most depths and times, and maximum concentrations occurred in the upper 10 m from mid-May to June, and again from late July to

121

A

M -

20"

40"

J

J

A

S

0

N

J

Io

0

60"

80"

OIO

I00"

120"

140"

/)

160'

180"

200"

Fig. 2. Temporal and spatial distributions of chlorophyll a (/.tg 1- I) in Saanich Inlet during 1981.

early August (Fig. 3). Largest concentrations occurred in the deep water from early April to mid-August, then declined and reached undetectable levels by mid-November. During the early period, pheopigments co-occurred in the deep water with many frustules of diatom genera found in the upper 10 m (Table III). Little information about temporal and vertical changes in pheopigments was obtained because horizontal variations in these pigments were very large. Insufficient quantities of pigments were collected from the seston for identification. Sediments from the trench were black, anoxic and probably very porous (p = 0.5 g cm-3), while those from the shallower station were green, oxygenated and more compact ( p = 1.7 g cm-3). Pigments in the anoxic sediments were dominated by pheophytin a and included either pheophorbides or chlorophyllides and unidentified xanthophylls and

122

TABLE 1 Taxonomic composition of phytoplankton and protozoan assemblages accounting for at least 90% of micro- and nanoplankton carbon (%): values are means of 0 and 5 m samples Time (months)

April 7

A rnphidinium spp. Chaetoceros concavicornis Mangin Chaetoceros debilis Cleve

27

May

June

20

10

July 6

17

29

3.2 13

21 7.2 32

6,(1 58

I0

Euglenoid flagellates

Unidentified pennate Diatoms

Sept.

18

Chaetoceros didyrnus Ehrenberg Chaetoceros difficilis Cleve Chaetoceros spp. Ciliata Dinophvsls spp. Gvmnodinium spp. nano-flagellates Nitzschia delicatissima Cleve Prorocentrum spp. Protoperidinium spp. Skeletonema costatum (Greville) Cleve Thalassiosira auguste - lineata (Schmidt) Fryxell el Hasle Thalassiosira decipiens (Grunow) Jorgensen Thalassiosira Nordenski61dii Cleve Thalassiosira rotula Meunier Thalassiosira spp. Unidentified Centric Diatoms

~0

Aug.

14 50

3.7 I1

7.0

6.0 4.8

4.3

53

31 12

27

6,5 10 4.8

6,5

7.4

11 68

4.1

2.6

16 90

46

4.3 16

18

24

12

3.3 2.4

5.0 2,7 6.4

carotenoids (Table IV). Oxygenated sediments had lower concentrations of pheophytin a and similar amounts of pheophorbide-chlorophyllide, xanthophylls and carotenoids. N o seasonal changes were readily apparent, therefore data were pooled and means and their standard errors calculated (Table IV). Maximum volumes of suspended particles occurred between the sea surface and 10 m from late April to late May (Fig. 4). Large volumes of particles at depths between 25 and 150 m co-occurred with the near surface maxima. Particle volume decreased at all depths during early June and then increased in late September, reached a maximum in early October and subsequently decreased (Fig. 4). During September and October, glass-fiber filters appeared gray after filtering seawater samples, and the darkest color was produced by water from 200 m. Particles with

123

A

M

•

o.zs"-~

J

LL-.-z.4,._L~ ."r-

"

.

J

A

S

0

~.~o~/s

D

o

20,

40'

60"

80-

e

IO0-

E I

~ t20-

140-

•

02

"

"28

"

160"-

0.28 180-

200-

./

\

Fig. 3. Temporal and spatial distributions of pheopigments (~g l -I) in Saanich Inlet during 1981.

apparent diameters greater than 32 # m dominated maximum suspensions observed during spring and fall seasons• Otherwise, distributions of particle volumes in different size ranges were quite variable• Volumes of sediment particles were dominated by those with apparent diameters between 3 and 5 /~m and those with diameters greater than 32/~m. Maximum bacterial activity occurred from late April to mid-June, and from mid-July to mid-September at depths between 0 and 25 m (Fig. 5). Activities were detectable down to 50 m during most cruises and while they were usually undetectable at depths of 100 m and greater, significant activities were occasionally measured (Fig. 5). The oxycline, bounded by 02 concentrations of 0.76 and 3.0 ml 1-l, occurred at

124 TABLE II Maximum cellular concentrations (cells 1 i × 10 3) of micro- and nanoplankton occurring at depths between 50 and 150 m Time (months) April 7 Chaetoceros Chaetoceros Chaetoceros Chaetoceros Chaetoceros

debilis Cleve didymus Ehrenberg difficilis Cleve gracilis Schut t

27

May

June

Jul',;

Aug.

Sept.

20

10

3(7

17

29

0.20 0.10

0.39

4.71

1.18 10.8

0.30

0.59

0.73 1.05 6.99 2.51

sp.

4.37

Ciliata Dinophysis sp. Leptocylindricus danicus Cleve Melosira sp.

nano-flagellates

0.30

3.26 20.1

0.52 3.67 7.36

11.6

1.64 0.18

0.30 0.39

Nitzschia closteriurn (Ehrenberg)

W. Smith Nitzschia delicatissima Cleve Oxvtoxurn sp. Skeletonema costatum (Greville) Cleve Thalassionema nitzschioides Grunow

Unidentified Centric Diatoms Unidentified Pennate Diatoms

2.26

5.77

3.28

1.76

1.09

0.30 0.49

3.67 0.35 11.5

0.59 0.2(7

0.52 0.10

0.30 0.10 0.39 0.20

depths between 80 and 130 m during early April (Fig. 6). Below the oxycline, at 150 and 200 m, 0 2 was analytically detectable and no o d o r of H2S was noticed; however, statistically, c o n c e n t r a t i o n s varied between 0 and 0.76 ml 1 ~. C o n c e n t r a tions of 0 2 were m a x i m a l between the sea surface and 10 m from late April to m i d - A u g u s t (Fig. 6). In m i d - M a y , 0 2 c o n c e n t r a t i o n s increased at 25 m. and by m i d - J u n e the oxycline had increased in d e p t h by about 20 m to between 100 and 150 m. In early July the oxy.cline was at shallower depths, between 70 and 140 m, and then in early August, increased in d e p th to b e t ween 90 an d 190 m, almost reaching the b o t t o m (Fig. 6). This was followed by an a p p a r e n t upward d i s p l a c e m e n t of the 0 - 0 . 7 6 ml 1-1 water off the b o t t o m to depths between 100 and 150 m (Fig. 6). By late N o v e m b e r the 0 - 0 . 7 6 ml 1- t water had d i s a p p e a r e d and below 90 m, concentrations of O 2 varied b e t w e e n 0.76 and 1.5 ml 1-1. DISCUSSION T h e spring increase in d i a t o m biomass began in either early April or late M a r c h and c u l m i n a t e d in c o n c e n t r a t i o n s of chlorophyll a greater than 10 ~g 1 ~ between

125 T A B L E IIl M a x i m u m concentrations (particles 1- J x 10-3) of identifiable particles occurring at depths between 50 and 150 m Time (months) April 7 Diatom frustules Bacteriastrum hyalinum Lauder Chaetoceros affinis Lauder Chaetoceros gracilis Schutt Chaetoceros sp. Melosira sp Nitzschia closterium (Ehrenberg) W. Smith Nitzschia delicatissima Cleve Rhizosolenia sp. Skeletonema costatum (Greville) Cleve Thalassionema nitzschioides Grunow Thalassiosira spp. Unidentified Centric Diatoms Unidentified Pennate Diatoms Diatom resting spores Fecal pellets Dinoflagellate theca Dinophysis sp. Protoperidinium sp.

27

May

June

July

Aug.

Sept.

20

10

30

17

29

0.20 0.29 0.18 0.88 0.55

0.59

0.30

0.55 0.73

0.49 0.59 0.10

3.50

1.09

1.57

9.45

0.73 14.9

4.31

0.10 6.67

11.2 0.20

1.26

0.73 0.18

0.88

0.20

0.88 0.52

0.20

0.20 0.10

0.10

T A B L E IV Concentrations of pigments per gram dry weight of anoxic or oxygenated sediment. Calculations of pigment masses were made with specific absorption coefficients taken from Lorenzen and Jeffrey (1980) Identity (units)

Anoxic April (n = 4)

Pheopigments(E665,

c m - 1) Pheophorbide a / C h l o r o p h y l l i d e a (/t g) * Pheophytin a (# g) Xanthophylls (E440_ 448, c m - t ) Carotenoids (E440_ 470, c m - t)

Oxygenated July-August (n ~ 2)

June-July-August (n = 3)

0.50 +0.56 1.6 -+1.3 0.080-+0.16 0.039-+0.040

0.20 +0.14 0.11 -+0.077 0.043,:1:0.012 0.008-+0.006

0.095 +0.021 **

-

0.031_+0.037

* Masses were calculated using the specific absorption coefficient for pheophorbide a. ** Data are reported as means and standard errors.

126

A

M

J

J

A

S

0

13

N

20"

40-

60-

80-

rOOE •

"

"

°

'

o-!

I a_ Ig'O-

140-

160-

180-

f Fig. 4. Temporal and spatial distributions of suspended particles (ram ~ [ i ) with sizes ~arxing between 2.0 and 40 p.m in Saanich Inlet during 1981.

late April and mid-May. This spring increase was dominated by species of the centric diatom genera, Chaetoceros and Thalassiosira. exactly as observed in 1976 (Hobson, 1981). However, during 1976, maximum chlorophyll a concentrations were about 30 >g 1 l and occurred in mid-April (Hobson, 1983). Apparently these large crops occur because zooplankton grazing only begins late in the bloom. Thus, pheopigments, probably produced by the degradation of chlorophyll a by zooplankton metabolism (Shuman and Lorenzen, 1975), accumulated in mid-May and early June, after chlorophyll a concentrations had peaked. The subsequent decrease in chlorophyll a was probably due to the effects of grazing and the stripping of most NO 3 from the euphoric zone by the phytoplankton (Huntley and Hobson, 1978),

127 A

M

d

d

A

S

0

N

D

i:i 20"

0"16

Fig. 5. Temporal and spatial distributions of bacterial metabolism (nmoles thymidine 1 I h-1 Saanich Inlet during 1981.

X

103) in

which inhibited further diatom increases. The accumulation of pheopigments that was observed in late July and early August suggests that a summer bloom occurred that was immediately grazed. The temporal variations of plant cells did not result in measurable changes of pigments found in sediments. Of these pigments, which included degradation products of chlorophyll a, xanthophylls, and carotenoids, pheophytin a was better preserved in anoxic than in oxygenated sediments. Maximum bacterial activity and accumulation of particles in the euphotic zone co-occurred with the spring diatom increase and the subsequent period of pheopigment accumulation. Also, during this period, both particle concentration and

128

A

M

d

J

A

S

0

0

N

D ~":"-6-I

20"

40"

60

,oo

i

.

.

.

.

.

.

.

.

.

•

•

•

('7.

120-

Q_

140-

~.~

160-

180-

0.76

Fig. 6. Temporal and spatial distributions of O 2 (ml 1 l) in Saanich |nlet during 1981.

bacterial activity increased in the deep water down to a depth of 150 m. Many of the particles were frustules of cells of Thalassiosira spp., which were an important component of crops in the euphotic zone. While the particles were not rich in either chlorophyll a or pheopigments, they must have included organic matter, which supported bacterial metabolism. The summer phytoplankton bloom supported a second major peak in bacterial activity that was observed from the sea surface to depths between 100 and 150 m. However, during this summer period, there were no accumulations of particles in the water column. Presumably, bacterial activity was supported by dissolved organic matter, which either had accumulated in the water column since the spring bloom or was produced by the summer bloom, or both.

129 No changes in dissolved 02 concentrations were observed in the deep water from early April to mid-May even though bacterial activities occurred in and near to the oxycline. This suggests that either the combined effects of animal respiration and bacterial metabolism on 02 concentrations were undetectable or downward diffusion of 02 balanced utilization. Instead of decreasing levels of 02 , an increase occurred in the deep water in mid-June. This increase was preceded by maximum concentrations of 02 in the euphotic zone, probably caused by maximum photosynthetic rates in the spring. It seems unlikely that the high-O 2 water in the euphotic zone was mixed downward to the bottom because no forcing mechanism is readily apparent. However, the increase in deep-water 02 could have been due to mixing with O2-rich water cascading over the sill although flushing in the Inlet has not been observed earlier than August (Anderson and Devol, 1973). Perhaps a small volume of water spilled over the sill before the main volume, which appeared in early August. That this latter event occurred is supported by the observation of an upward displacement of low-O 2 water that occurred in mid-August and persisted until mid-November. During this period, particle concentrations increased in the deep water but were not associated with either plant pigments or bacterial metabolism, indicating a sediment origin. Both the upward displacement of low 02 water and increase in particle concentration have been observed during other flushing events in fjords (e.g. Gade and Edwards, 1980). In conclusion, particles produced during the spring diatom bloom were rich in chlorophyll a and pheopigments, which disappeared as particles sank deeper in the water column to depths between 150 and 200 m. The volume of particles, with sizes ranging from 2.0 to 4 0 / t m , was dominated by those with a mean size of about 32 ~m. Qualitatively, many of these particles were frustules of the two diatom genera, Thalassiosira and Chaetoceros, which dominated phytoplankton crops in the euphotic zone. A positive correlation between particle volume and bacterial production was observed, supporting, in part, Herlinveaux's postulate. However, no correlation between bacterial production and changes in dissolved 02 was seen in the deep water. This observation was masked by flushing that occurred in August and may have begun as early as mid-June. ACKNOWLEDGEMENTS I wish to thank Capt. D. Horn and crew of the MSSV " J o h n Strickland" for their help in the field. The research was supported by an operating grant provided by the National Sciences and Engineering Research Council, Ottawa, and faculty research grants from the University of Victoria. REFERENCES Anderson, J.J. and Devol, A.H., 1973. Deep water renewal in Saanich Inlet, an intermittently anoxic basin. Estuarine Coastal Mar. Sci., l : l- 10.

130

Bary, B. McK., 1966. Back scattering at 12 k c / s in relation to biomass and numbers of zooplankton organisms in Saanich Inlet, British Columbia. Deep-Sea Res., 13: 655-666. Broenkow, W.W. and Cline, J.D., 1969. Colorimetric determination of dissolved oxygen at low concentrations. Limnol. Oceanogr., 14: 450-454. Devol, A.H., 1981. Vertical distribution of zooplankton respiration in relation to the intense oxygen minimum zones in two British Columbia fjords. J. Plankton Res., 3:593 602. Fuhrman, J.A., A m m e r m a n , J.W. and Azam, F., 1980. Bacterioplankton in the coastal euphoric zone: Distribution, activity and possible relationships with phytoplankton. Mar. Biol., 60:201 207. Gade, H.G. and Edwards, A., 1980. Deep water renewal in fjords. In: H.J. Freeland, D.M. Farmer and C.D. Levings (Editors), Fjord Oceanography. Plenum, New York, N.Y., pp. 453 489. Herlinveaux, R.H., 1962. Oceanography of Saanich Inlet in Vancouver Island, British Cglumbia. J. Fish. Res. Board Can., 19: 1-37. Hobson, L.A., 1981. Seasonal variations in maximum photosynthetic rates of phytoplankton in Saanich Inlet, Vancouver Island, British Columbia. J. Exp. Mar. Biol. Ecol., 52: 1-13. Hobson, L.A. and Hartley, F.A., 1983. Ultraviolet irradiance and primary production in a Vancouver Island fjord, British Columbia, Canada. J. Plankton Res., 5: 325- 331. Hobson, L.A., Menzel, D.W. and Barber, R.T., 1973. Primary productivity and sizes of pools of organic carbon in the mixed layer of the ocean. Mar. Biol., 19:298 306. Huntley, M.E. and Hobsom L.A., 1978. Medusa predation and plankton dynamics in a temperate fjord, British Columbia. J. Fish. Res. Board Can., 35: 257-261. Jeffrey, S.W., 1968. Quantitative thin-layer chromatography of chlorophylls and carotenoids from marine algae. Biochim. Biophys. Acta, 162: 271-285. Lorenzen, C.J., 1967. Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol. Oceanogr., 12: 343-346. Lorenzen C.J. and Jeffrey, S.W. 1980. Determination of chlorophyll in seawater. IJNESCO Tech. Pap. Mar. Sci., 35, 20 pp. Pickard, G.L., 1975. Annual and longer term variations of deepwater properties in the coastal waters of southern British Columbia. J. Fish. Res. Board Can., 32: 1561-1587. Richards, F.A., 1965. Anoxic basins and fjords. In: J.P. Riley and G. Skirrow (Editors), Chemical Oceanography, Vol. 1. Academic Press, London, pp. 611 645. Shuman, F.R. and Lorenzen, C.J., 1975. Quantitative degradation of chlorophyll b,¢ a marine herbivore. Limnol. Oceanogr., 20: 580-586. Strickland, J.D.H. and Parsons, T.R., 1968. A Practical Handbook of Seawater Analysis. Bull. Fish. Res. Board Can., No. 167, 311 pp. Taylor, L.R., 1961. Aggregation, variance and the mean. Nature, 189:732 735. Tunnicliffe. V., 1981. High species diversity and abundance of the epibenthic community in an oxygen-deficient basin. Nature, 294: 354-356.