Not to be cited without prior reference to the author

ICES 1990 PAPER C.M. 1990/L:19

CONTRIBUTION OF ZOOPLANKTON GRAZING IN THE DECOKPOSITION OF A CERATIUK BLOOK

by

Torkel Gissei Nielsen

Danish Institute for Fisheries and Marine Research Charlottenlund Castle, DK-2920 Charlottenlund, Denmark

ABSTRACT

Dinoflagellates belonging to the genus Ceratium dominate the phytoplankton in August-September in Danish coastal waters. These blooms have been associated with the occurrence of oxygen depletion in the bottom waters, but only few investigations on the pelagic grazing of Ceratium have been carried out. During the present investigation of a Ceratium bloom growth rates and vertical distribution patterns of dominating Ceratium spp. were investigated. The vertical distribution of potential predators were also investigated. The grazing pressure due to ciliates is low. Laboratory experiments show that only the largest copepod species (Centropages hamatus and Q. typicus) and cladocerans are able to graze Ceratium. Copepods biomass remained fairly constant during the investigation period, but cladoceran biomass increased and eventually totally dominated the mesozooplankton. The vertical distribution of these species correlated with that of Ceratium. The crustaceans graze from 30 to 70% of the Ceratium production per day. This investigation illustrates that a large fraction of the Ceratium cells are grazed in the water column and do not necessarily sediment.

INTRODUCTION

Spring and autumn phytoplankton blooms are two eharaeteristie

events in the annual phytoplankton eyele of temperate seas. The

spring bloom develops in response to the inereased insolation and

stabilization of the water eolumn while the autumn bloom is

assoeiated wi th the breakdown of the summer stratifieation so

that nutrient rieh bottom waters are transferred to the euphotie

zone (Cushing 1989). Between these major events subsurfaee

nanoflagellate blooms develops after the stratifieation of the

water eolumn have been establi shed in the springjearly summer

(Nielsen et ale 1990) and in the other end of the stratifieation

Ceratium spp. blooms often develop in late summer.

Due to the small overwintering population of eopepods in

eoastal waters and the low temperature the major part of the

spring bloom build up eventually sink to the bottom rather than

being grazed by eopepods (Nieolaj sen et al. 1983, Roff et al.

1988). During summer the eopepod biomass build up and normally

peak in August -September (e. g. Smetaeek 1980 Blanner 1982,

Nieolajsen .1982 ),eoineiding with blooms of large dinoflagellates

(Colebrook el at. 1978, Conover 1978, Lindahl

&

Hernroth 1983).

These are domina ted by speeies belonging to the genus Ceratium.

Sinee they eontribute substantial to the annual produetion of

eoastal waters (Edler 1986) and their deeline and deeomposition

has been assoeiated with the reeurrent oxygen depletion events in

the bottom water (e.g. Mahoney & Steim1e 1979, Fa1kowski et ale

1980), information on the deeomposition of these blooms is

important. In eontrast to the spring bloom, very few

investigations on zooplankton grazing on these Ceratium

3

population in the autumn has been associated with the development of the Ceratium population (Smetacek 1981). Ceratium is generally believed to be poor food for copepods due to their size (Graneli el at. 1989), shape (Hargrave &. Geen 1970) or low nutri tional value (ref) but very few grazing experiments have been conducted. The abundant, but frequently ignored, cladocerans normally peak in the late summer-early autumn

(Gieskes 1971, Boch &. Taylor 1973) coincident wi th blooms of dinoflagellates (e.g. Ceratium spp.) (Bainbridge 1958,

Morey-polyphemoides has revealed that they feed on Ceratium (Morey -Gaines 1979). However, grazing experiments with cladocerans on

•

•

Gaines 1979) and gut content exarninations of Podon

ceratia are still lacking.

Since Ceratium spp. dominate the phytoplankton 1- 2 months each year in Danish coastal waters, the aim of the present paper is to describe dynamics of the bloom and to determine the role grazing on Ceratium populations.

MATERIALS AND METHODS

The field data originate from a permanent station in the southern part of Kattegat (56°15.42 N 12°00.12 E, 30 m depth). The station was visited daily from 24 Aug. to 10 Sept. 1989 by RV Ophelia

(24 Aug~ - 3 Sept.) or RV Gunnar Thorson (4 - 8 Sept.).

Sampling was conducted around noon. Vertical profiles of temperature, salinity and in §itu fluorescence were recorded on all sampling occasions. Temperature and salini ty were recorded for every metre while the fluorescence measurements were continuous throughout the water column. The fluorometer was calibrated daily against spectrophotometrically determined chlorophyll content in water sampies from 4 to 5 depths. The

4

sured in size fractionated

and measured

fluorometri-relative size distribution

of the

duplicate in

as described by

Growth rates

of the phytoplankton were

samples of surface water

measured

~m nitex screen filters

extracted in 96

%

ethanol

GF/F filters, 3 ~m

nucleo-pore filters and 11 and 50

cally,

and ~ fusus) were

mea-the laboratory under in

Nielsen el at. (1990).

water sampies incubated in

situ like conditions, or

on deck during the Gunnar

dominating Ceratium spp. (

Ceratium furca, ~ tripos

(2.5 m) filtered on 25 mm

Thorson cruise. Wi thin 3

~ n ~ u ~ u ~ u ~ ~ ~ I 2 3 4 5 6 7 a . August " September 20 Depth. m 0r---r--r--~---.,...-n-,...-.,.---...-r.,...., 24

Fig. 1. Temporal variation in Al salinity, 0 / 0 0 , Bl

temperature, °c, and Cl chlorophyll~, ~g 1-1 at the permanent station in"the southern Kattegat from 21 august to 8 september 1989. Distance between iso1ines is 2 in A and 1 in Band C.

•

•

hours of collection the water was passed through a 200 ~m sieve (

by reverse filtration (to rernove larger predators).

Replicate sampies were filled into 2.4 1 polycarbonate bottles, sealed with plastic film to prevent bobble formation. The bottles

were mounted on a slowly rotating wheel (0.5 rprn) and incubated

for 24 h in a walk-in thermostated room (in situ temperature ±

that approached the light climate at 2.5 m depth at the sampling si te. Ini tially and at the end of each experiment replicate sampIes of 1 1 from each fraction were preserved in 1

%

Lugols 'solution. After 24 h the sampies were concentrated on a 11 Ilm mesh net and rinsed into 50 ml containers and counted using an inverted microscope. At least 400 cells werecounted per sampie. The growth rate (r, d-1) for'each species was calculated from the change in abundance, assuming exponential growth. r =

•

lnlN(t)jN(O)l/t. where N(t) and N(O) are the mean numbers at the

st~rt and end of the experiment. respectively. and the duration

in days.

Depth integrated zooplankton sampies were collected using a submersible pump ( 400

lowered at ca. 10 m

-1

1 min ) min- 1 The

fi tted wi th a 50 Ilm net and samples were preserved in 2 %'

buffered formalin. Zooplankters in subsampIes were later

•

identified. counted and their lengths were measured. At least 200 individuals were counted in each subsamples (1/100 to 1/200). Abundance data for copepods and cladocerans were converted into biomass (dry weight) using the length-weight regressions in Lampitt (1978), Klein Breteler (1982). Steven Hay (unpublished • Calanus finmarchius and Paracalanus parvus) and Kankaala

&

Johansson (1986), and converted to carbon assuming a conversion factor of 0.45 (Ki~rboe el at. 1985a). Due to the difficulties in separating the smaller stages of Centropages hamatus and C. typicus , the pump sampies were size fractionated (180 Ilm) and the larger stages (C4 to adult) of these two species were counted in a subsampIe (1/5 to 4/5). The ratio between the two species in these was taken as representative for the entire population and used for the calculation of the grazing pressure on the Ceratium

•

•

cells. Copepod egg production was measured according to Ki~rboe

et al. (1985b). Adult females were sampled above the pycnocline

and brought to the laboratory in a thermostated j ar (100 I).

Within 3 h of collection fertilized females were sorted out and

added to 620 ml blue cap bottles (1 - 5 individuals in· each) •

containing 250 ~m screened surface water. The bottles were

incubated for 24 hours on a rotating wheel (0.5 rpm) in the

laboratory at in situ temperature (± 1°C) or on deck during the

Gunnar Thorson cruise. At the end of the experiment the spawend

eggs were counted .

The vertical distribution of Ceratium spp. and micro-and

mesozooplankton were investigated using a 30 1 water sampler at 8

depths; sampling was most intensive around the Ceratium peak. if

present. Sample depths were chosen on the basi s of vertical

profile of salinity. temperature and fluorescence. Vertical

distribution of Ceratium and microzooplankton were conducted

every second day. On the days in between. sampies were only taken

at two depths ( surface and pycnocline) . The vertical

distribution of mesozooplankton were investigated every fourth

day. Diel vertical migration of the Ceratium spp. was

investigated from 4 to 5 September. Water samples of 1 1 were

taken at 7 - 8 depths at approximately 6 hours intervals . For

enumeration of Ceratium and microzooplankton 1 1 of the sampies

were preserved in 1

%

Lugol's . Zooplankters in the remaning 29 I

were concentrated on a 45 ~m sieve and preserved in 2

%

buffered

formaline. Depending on the cell concentration 50. 100 or 1000 ml of the Lugol's fixed sampie were examined. while mesoplankton in

the total or a subsample (1/2 1/20) of the formalin fixed

•

•

carbon biomass assuming a carbon content of 2600, 12000 and 3300

-1

pg C cell for Ceratium furca, C. tripos and ~ fusus, respectively (Edler 1977). Ciliates were identified according to Leegard (1915), Kahl (1932) and Lynn el at. (1988). The abundance data of the ciliates were converted to biomass assuming simple geometrical shape and a carbon volume ratio of 0.071 (Fenchel &

Finlay 1983). The mesoplankton biomass was calculated as above.

Grazing experiments

Ceratium spp. for the grazing experiment were collected in the surface (2.5 m) or, if present, at the depth of maximal florescence using a 30 1 water sampler. The cells were concentrated on a submerged 20 ...m sieve and washed wi th GFF filtrated water (from·the sampling depth) to remove smaller algal species. At the start of the incubation, the Ceratium spp. were diluted with GFF filtered water to a concentration of about 0.5 x 106 ...m3 ml-1. Ini tially all concentrations were adjusted by a particle counter ( Coulter Multisizer). Copepods and cladocerans for the grazing experiments were collected at the permanent station above the pycnocline with a 200 ...m opening-closing net . Within 3 h after collection adult females were transferred to GFF filtered surface water and starved for 24 h prior to the grazing experiment. From 7 to 20 copepods or 30 to 50 cladocerans were transferred to each of four 620 ml blue cap bottles; two bottles without animals served as controls. The initial Ceratium concentration was measured in 500 rol of the incubation medium fixed in 1% lugols. The bottles were incubated at in situ conditions for 24 hours. At the termination of the experiment the entire content of the incubation bottles was fixed in 1% Lugol's

solution. Sampies were concentrated on a 11 ~m sieve and washed into a settling chamber and counted with an inverted microscope. At the end of the experiment cepha1othorax length and total

length were measured on the copepods and cladocerans, respectively. elearance and ingestion were calculated according to Frost (1972).

RESULTS

Profiles of salinity, temperature and chlorophyll a from August

•

21 to September 8 ,1989 are shown on Fig. 1. During the first week a steep pycnocline was present at 16 - 20 m depth gene ra ted by both salinity and temperature. The salinity and temperature of

water varied between 16

-was less steep (a pycno-creased to > 32 0 / 0 0 .

J,lM

0 0.2 0.4 0.6 0.8 1 0 N0 3 5 P04 Temperature

e

10 Sal1nity

..

.c:

-

15 0-G) Q ₂₀ 25 10 15 20 25 30 35

Temperature. Sal1nity

30 the 2 surface - 19 0 / 0 0 , stratification September brackish salinity From 17 oe and 13

respectively. Below the

ture dropped to 8 to 10 oe and the salini ty in-the

pycnocline the

tempera-•

cline between 12 and 22 Fig 2. A typical profile of nutrients at the

salinity dropped to 13 to

m) and the surface

permanent station in the southern Kattegat on 6 september 1989. NOJ and P04 relate to the upper axis while temperature.DC. and salinity. DjDD, relate to the Iower axis.

15 0 / 0 0 due to horizontal

advection of surface water from the BaI tic

current. During the first ten days the surface concentration of chlorophyll ~ was low: < 1 IJ.g chI ~ I -1, although patches of

higher concentrations occurred below and within the pycnocline. Coinciding with the inflow of the Baltic water ( September 2 to 7) the surface chI ~ concentration increased to abut 6 IJ.g chI a

-1

1 . Typical profiles of nitrate and phosphorous are shown in Fig. 2. Above the pycnocline the nitrate and phosphorous were close to the detection level, in the bottom water the

•

concentration increased to about 0.4 and 0.8 IJ.M for P04 and N03 respectively. The chlorophyll a concentration in the surface

U

.----=g~C_h_l_a_l_-_l

--,

10 r

-•

8 ~ ) 50 J.lm

fffm

11 - 50 IJm

lill1

3-11lJm

-

0-31Jm 21 22 23 24 25 26 27 28 29 30 31

August

1 2 3 4 5 6

September

7 8

Fig. 3 Size distribution of phytoplankton (~g chl ~ 1-1) in the surface sampies at the permanent station between 21 August and 8 september 1989.

water (2.5

m)

varied between

1.16

and 5.8

~g

chI

~

1-1 (Fig.3 ). During the first part of the period (unti 1 September 1) the

eoneentration inereased to inflow of Baltie water the

There was an inerease in

assoeiated

distribution size

fraetions

~m

In the first ( August 21.

~m or > 50 ~m fraetions. with the major part of the biomass in either the < 3 modal

algal biomass had a bi-with the Baltie water .. The 2 . 5 ± 1. 4

~g

chI a 1-1 stant 1.54 ± 0.35 ~g chI a 1-1. Assoeiated wi th the biomass was low and

eon-both the < 11 ~m and > 11

c

24 12 Deplh. m

0r--r---;r---r-"...".T7"~----.--,

made was responsible for

the biomass, respeetively. period the < 3 ~m fraetion

and seeond part ( to 31) September 1 to 8) of the 22 ± 8

%

and 28 ± 16

%

of ~ n ~ ~ ~ U D ~ ~ ~ ~ 1 2 3 4 5 6 7 a August SeotembP.r

•

The > 50 ~m (dominated by

sponsible for 57 ± 9% and 62 ± 17

%

respeetively

Fiq. 4. A-C: temporal and vertieal distribution of the dominatinq dinoflagellates belonqing to the genus Ceratium, expressed as eells ml -1. A) 9.

furea B) 9. fusu~ C) 9. tri~. D: total biomass of the Ceratiu~ Bpp. expressed as ~g C l -i . Distanee

Ceratium spp. ) was

re-between isolines are 5, 2, 2 and 25 on A. B, C and D

respeetively. during the two periods.

I identified seven speeies belonging to the genus Ceratium: C. fure<!, C. fusus, C. tripos, ~ lonSl:i,.pes, C. mC!.c;:roeeros, ~

lineatum and ~ horridum. The three first mentioned ones constituted the major part of the biomass ( 82 to 100

% .

mean 97

±

3

%).

The temporal and vertical distributions (cells numbers and biomass) of the three dominating species are shown in Fig. 4. It is important to keep in mind that the development outlined does not necessarily reflect cell multiplication and mortality.

since the numerical changes may be due also to horizontal advection. but Ceratium spp. totally domina ted the plankton

TIme: 19 Time: 24 TIme: 08 Time: 12 Time: 17

A 0 5 10 15 0 5 10 15 0 10 20 0 5 10 15 0 5 10 H 0.5 0.5 0.5 0.5 0.5

-

5 5 5 5 10 10 10 10 10 15 15 15 15 15 20 20 20 20 20 25 25 25 25 25 10 20 30 10 20 30 10 20 30 10 20 30 10 20 30 B 0 2 3 4 5 0 4 5 0 2 3 4 5 0 1 2 3 4 5 6 0 1 2 3 4 5 6 0.5 0.5 0.5 0.5 5 5 5 10 10 10 / 10 15 15 15 15 20 20 20 20 25 25 25 25 10 20 30 20 30 10 20 30 10 20 30 10 20 30 C 2 0 2 0 1 2 3 4 5 6 0 2 0 2 0.5 0.5 0.5 0.5

•

5 5 5 5 5 10 10 10 10 10 15 15 15 15 15 20 20 20 20 20 25 25 25 25 20 30 10 20 30 10 20 30 10 20 30 10 20 ·30

Fiq. 5. Time ~eries of the vertical distribution of the dominatinq Ceratium spp. (cells mi-I, hatched area upper aXis) A) g. Lurca, B) f. ~sus and C) f. tripos and profiles of temperature,OC, and salinity, 0 / 0 0 ,(-*- and -"-, re~pectively, lower axis) at the permanent station from 4 to 5 September 1989

community on all sampling occasions. The existence of two separate populations is evident; one is restricted to the brackish surface water and the other is found below the pycnocline. The bloom was numerically dominated by C. furca (maximum abundance 30 cells ml-1) except during the period of advection of tbe brackish surface water wbere C. fusus reached a density of 23 cells ml-1. The biomass peaked within and below the pycnocline between August 21 and 30, and in the surface water during the last part of the peroid. Between August 27 and 31 high biomasses occurred at the same time on both sides of the pycnocline. Diel vertical migration was only observed in the case Ceratium fusus. (Fig. 5). The profiles show that the cells concentrated at specific depths: the peak concentration of Ceratium furca and C. tripos (Fig. 5a and c) was observed within the upper 5 m at all sampling occasions, although C. tripos bad an additional peak in the pycnocline. In C. fusus (Fig. 5 b) the peak concentratiön was a 7.5 and 15 m at none and midnight, respectively.

lable 1. Growth rate (r, d-1) of the-dominating- Ceratium species, measured in size fractionated surface (2.5 m) salllpies. - no of measurements. August September Date 21 22 23 25 26 27 29 30 31 3 4 5 6 7 Mean ± SD Ceratium furca 0.23 0.16 0.12 0.14 0.24 0.12 0.16 0.09 0.24 0.14 0.06 0.15 0.17 0.05 0.15 0.15 ±0.06 ~. fusus 0.10 0.27 0.12 0.04 0.17 0.25 0.26 0.15 0.16 0.25 0.19 0.21 0.20 0.18 ±0.07 ~. tripos _{0.29 0.18 0.11 0.16 0.27 0.33 0.11 0.18 0.24 0.03 0.05 0.26 0.11 0.11 0.17 ±0.09}

The speeifie growth rates (r, d-1) of the three dominating Ceratium speeies measured in the size fraetionated surfaee sampies from August 21 to September 7 are shown in Table 1. The average growth rate for the three speeies were nearly equal;

0.15, 0.18 and 0.17 d-1 for C. furea, C.fusus and .Q. tripos,

respeetively.

Vertieal distribution of eiliates

trieh eiliates dominated

o

Depth. m o...----.,...,--r--r--..,....---,....-...,.-...,...,---,,.-,

o

A

~

'\@09!!!J

o

Ls)r

~~tV

20 12 24 or the Oligo-to speeies restrieted Eighteen

ling occasions. The bulk

layers above the pycno-eline and the autotrophie was

of the eiliate biomass morphotypes of eiliates

the biomass at most samp-were identified.

Mesodinium rubrum peaked 20

•

inthe thewateruppereolumnquarter(Fig.of 6). The oligotriehs were dominated by Lohmaniella 24 '8 oviformi~. ~. ~piral~s, ₂₀ Strombidium spp., S. 24 vesieulusus, Laboea 28L-l.-.,;l.-..J---l---l.-...l.-...l.--L--.l..'--.l..'----L'----L'~ n ~ ~ ~ u v ~ n ~ ~ 1 - L - L - L - L . - l - - l - - - !2 3 4 5 6 7 a August September

strobila and Tontonia spp. and the tintinnids

by

Helicostomella

Fig. 6. Temporal variation in the vertical distribution of the biomass (~g C l - I ) of the

domination ciliates Al oliqotrichs Bl Tintinnlds end

subulata. The peak abundances of Mesodinium _{- - -}rubrum naked oligotrichs and tintinnids were 3.4. 2.4 and 2 individuals 103

l-I -1

or 6.3. 5.4 and 3.8 f..l.g C l , respecti vely. The raptorial prostomatide ciliate Tiarina fusus (not included in Fii. 6) was present at all samp1ing occasions and their vertical abundance peaked within the ceratium biomass peak. The highest abundance recorded during

corresponding to

the investigation period a biomass of 0.2 f..l.g C

-1

was 80 ce11s 1 1-1. Even higher concentrations were observed on September 28 (biomasses of 1.26 and 0.89 f..l.g C 1-1 according to 540 and 380 ipd 1-1 in the surface and pycnocline. respectively)

Composition, biomass and vertical distribution of mesoplankton. Copepods and cladocerans dominated the mesoplankton. the only other organisms which were present in significant numbers were

Table 2. Biomass (mg dw .2) of the dominating Copepods and cladocerans at the permanent station from 21 Aug. to 9 Sept. 1989. Data obtained fom the depth integrated pump samp1es. - indicate that the species was not present in the sampie.

Oithona Paracalanus Pseudocalanus Acartia Centropages Temora Calanus Evadne Porlon Total

spp. parvus spp. spp. spp. longicornis spp. nordlllanni spp. biollass

21 Aug. 586 500 13 93 100 206 1498 25 auge 291 376 116 21 12 43 25 30 133 1047 27 Aug. 274 679 152 2 10 2 57 164 225 1565 29 Aug. 602 534 254 68 112 112 139 1821 31 Aug. 360 379 176 92 5 465 152 1629 2 Sept. 547 860 311 61 12 6 3 767 124 2693 4 Sept. 482 412 202 12 4 2 530 78 1722 6 Sept. 339 416 160 88 12 12 1523 23 2573

Table 3. Cladoceran biomass as percentage of the total mesoplankton biomass in the depth integrated pump sampies.

Date 21 Aug. 25 Aug. 27 Aug. 29 Aug. 31 HUg. 2 Sept. 4 Sept. bSept.

20 16 25 14 20 33 35 60

appendicu1aria (Oikop1eura dioica) and po1ychaete, bivalve, gastropod and echinoderm larvae. Seven taxa of copepods were present in the pump sarnples and three of these, Oi thona spp., Paracalanus p-arvus and Pseudocalanus spp., made up the major part

( 89 - 98

%,

mean 92) of the biomass at all sampling occasions (Table 2) . The cladocerans were dominated by Evadne nordrnanni and Podon sp. Ini tially the copepods dominated the crustacean

cladoceran biomass

in-cladoceran biomass until

Depth. m or----::,.---...-...--r--r~---r-r-r--~A., the their (Tab1e relatively and drastica1ly during was biomass biomass

made up 60% of the cru-zooplankton

constant

creased

stacean

3). Podon dominated the entire period (1223 ± 311

2

rng dw m ). In contrast

(Tab1e 2) and eventua11y

•

August 30, whereafter Evadne nordrnanni took

Fig. 7. Temporal variatio~ in the biomass (pg C 1 1) of the dominating cladocerans A) Fodon ap. and B)

over (Fig. 7) .. The verti- ~vadB.~ nOLdma!l}ll . Isolines distance is 2.

Deplh. m Depth. m 0 0 A E:

I

0

12 12 16 16 20 20 24

0

24 28 8 0

F

C~

_1."

•

12 /"'O~ 12 10 16 10 ₁₆

~'~

20 20 24 24

"

r-

~

\

--.

-28 28 0 C G 4 12 12 16 16 20

o

24 21 22 23 24 25 26 27 28 29 30 31 August 2 3 4 5 6 7 8 September

Fiq. 8. Temporal variation in the vertica1

12 distribution of the copepod biomass (~q C

1-1_{) A)}

spp., F) Temora 1ongiremis, and G) Ca1anus spp. Note Pseu_<:l0ca1anus spp., D) Centrop~~spp.. E) Acartia that the iso1ines are seperated by 5 in A to C and 1

in Dto G. C) spp .• Oithona B) parvus. Paracalanus 16 20 24 21 22 23 24 25 26 27 28 29 30 31 1 August 8

show that the major part of the cladocerans were located above and wi thin the pycnocline (Fig. 7). I soplets of the vertical distribution of copepods are shown in Fig. B There were conciderable differences in the vertical distribution among species. The major part of the biomass of Paracalanus parvus and .Oithona spp. (Fig. B A and B) was located above the pycnocline,

while the third dominating species Pseudocalanus spp. (Fig. BC) was concentrated below the pycnocline. Among the less abundant species, Acartia spp. (Fig. 8E) were most abundant in the surface water while Temora longiremis and Calanus spp. (Fig. BF and BG) occurred just above the bottom and Centropages spp. (Fig. 8D) in the bottom of the pycnocline where the Ceratium

located.

Copepod egg production

cells were

The most fecund copepod species were the larger forms; Centropages hamatus, C. typicus and Calanus spp produced on

-1

average 16, 52 and 15 eggs d respectively. The egg production of the smaller forms (Acartia spp., Paracala~~s parvus and Temora

respectively (Table 4). The egg production rate for Centropages

•

longiremis) was generally lower, 10, 10 and 8 eggs d-1

Table 4. Egg production (egg female- 1 d- l) of the domination copepod species at the permanent station frol 21 august to 7 september 1989 Ino. of measurements in parenthesisl. - no measuremnets

August September Date 21 22 23 25 26 27 29 30 31 2 3 4 5 6 7 Centrophages typicus 31.2 36.5 39.2 39.3 37.3 86.8 62.0 61.5 59.4 49 76 31. 8 56 . 75.2 30.8

h

halllatus 13.7 13.8 13.3 13.Q 15.6 11.6 14.4 15.1 25.9 18.8 25.6 15.0 18.0 21 11.3 13.8 Acartia spp. 5.3 5.2 3.2 10.6 7.9 10.0 10.0 8.6 15.5 9.1 9.7 10.6 17.7 Paracalanus parvus 10.6 9.5 11.0 11.4 6.b 5.5 7.1 7.8 7.4 10.7 18.3 14.3 12.3 7.7 11.3 10.9 Telara longicornis 13.6 13.5 2.0 4.0 5.3 Calanus sp. 15.0 19.0 13.0 13.0

typicus, C. hamatus and Paracalanus parvus correlated with the total phytoplankton biomass

(~g

chI a l - I ) (r = 0.52, 0.44 and

•

0.71, respectively). If the correlation to the different size fractions are considered C. typicus and C. hamatus were most elose eorrelated to the larger size fraetion (> 11 ~m) (r = 0.57 and 0.56), Acartia spp. to the smaller (< 11~m) (r = 0.33), while Paracalanus parvus were equally correlated to both fractions {r

=

0.58).

Grazing experiments

The results from the grazing experiments are shown in Table 6 .

Table 5. Ratio between the larger stages (C4 to adultl of Centropages typicus and ~. hamatus in the pumpsampies.

Date 21 Aug. 25 Aug. 27 Aug. 29 Aug. 31 Aug. 2 Sept. 4 Sept. 6 Sept.

Ratio 0.1 0.23 0.2 0.15 . 1.05 0.25 0.7B

Table 6 Clearance rates of the dominating copepods and cladocerans for the three dominating species of Ceratium. (no. of measurenents or experiments in

parenthesisl.

Species Length Body weight Clearance

hml (/lg CI (mI ind-1 d- 11

Ceratium furca

h

tripos C.fucus Centropages typicus 930±151 7.43 27 ± 5 42 ± 20 32 ± 11 (43) (101 001 1151 Centropages hamatus B75 ±30 6.40 10 ± 4 H± 5 19 ± 5 (221 191 191 191 Acartia spp. B20±25 3.58 0 0 0 (201 (41 141 141 Paracalanus parvus 709±71 3.99 0 0 0 1101 (41 (41 141 Oitona spp 408±16 0.47 0 0 0 1121 (41 (41 141 Evadne nordmanni 63B±B8 2.26 3.2 ± 0.3 8.3 ± 3.8 2.5 ± 0.4 1371 (BI (BI (41 Podon spp. 715±74 2.67 3.1 ± 1 7.9 ± 3.B 10 ± 7 (341 181 (BI (41

Both cladocerans species but only two of the four species of copepods tested were able to clear the three offered Ceratium species. From the clearance values in Table 6, the ratio between the two Centropages species (Table 5) and the vertical distribution of the

rele-on the three dominating 24

Because the cladocerans dominated the biomass of

o

Depth. m 0,---..,...---..,...,.---.--, A '8 20 '8 28I..l.-l--L-JI..-J--l~~--l..--I..-..l..-L-Ll-ll..-.:LI....J..-'>....Ll....u...~ ~ ~ ~ ~ ~ ~ ~ U ~ ~ U 1 2 3 4 5 6 7 8 August September 12 20 24 9). this were located roughly grazers, vertical of pycnocline was the the pressure potential

ly, the highest grazing

around

and Fig. 8D and G ) the

the pattern in the

gra-group (Fig. 7 ). General-the

pressure

vant zooplankters (Fig. 7

the grazing pressure (% water volume cleared d-I)

Ceratium species calculated (Fig. vertical di stribution of followed distribution zing

•

where 2-4, 2-6 and 4 - 14

%

of the water column was cleared per day for

Cera-tium f~_~~, C. fusus and

Fiq. 9. Temporal variation in the vertieal grazinq pressure on the three dorninatinq eeratia (% of the water eleared d-I). A) Ceratiu~ furea, B) ~ fucus and C) ~ !tiPos . The qrazinq pressure is ealeulated from the results in Table 4 and 6 and the vertieal distribution in Fig. 7 and 8.

In the Kattegat area

DISCUSSION

Ceratium is present in the plankton

•

•

year-round, but in the late summer they increase in abundance and normally totally dominate the phytoplankton in August-September.

The autumn bloom typically develops in abimodal pattern; a

Ceratium dominated bloom in August-September during the late

summer stratification, succeeded by a mixed bloom of diatoms and

dinoflagellates in September- October during the destratification

(Smetacek 1984, Torkel Gissei Nielsen, unpublished data). This

investigation focuses on the dinoflagfellatejCeratium bloom. The

highest density recorded during the present investigation was 54

-1 -1

cells ml (corresponding to 185 ~g C l ) , compared to other

investigations in the area this represents a "normal" year, 10

-20 (Edler 1984) to 570 Ceratium ml-1 (Lindahl

&

Hernroth 1983).

During the last decade these Ceratium dominated blooms have drawn

attention, since i t is often assumed that a large part of the

bloom sediments, and i ts menerlisation is associated wi th the

oxygen depletion of the bottom waters which occur in many areas

(Mahoney

&

Steimle 1979, Lindahl

&

Hernroth 1983, Smetacek 1984).

The vertical distribution of the ceratia during the present bloom deviates from the textbook description of the behavior of

large dinoflagellates; upward. swimming during the morning,

accumulation in the surface around none and downward in the

evenings (Levandowsky & kaneta 1987). During the first 12 days

the highest biomass was located below the pycnocline. From 27 to

31 August a biomass peak appeared both above and below the

pycnocline, whereafter the bottom population disappeared and the bloom was dominated by the ceratia in the brackish surface water.

speeies eonsidered here are able to swim 0.5 1 m

•

•

(Levandowski

&

Kaneta 1987)' as calculated from mieroseopie

observations. Studies on the vertieal migration of Ceratium furea

and Prorocentrum micans in Laholm Bay in the southeastern

Kattegat confirmed the laboratory measured migration speeds in

the field (Edler

&

Olsson 1985). However, I found no evidence of

such strong diel migration during this investigation, so

apparently two separate populations oeeurred; one in the bottom

waters and one restricted to the advected baltic surface water. One reason for the distinet.subsurfaee aeeumulation of Ceratium eould be absence of eri tical nutrients in the owerlaying water

(Haney

&

Eppeley 1981, Cullen

&

Eppeley 1981); in this case the

ni trate and phosphorus eoneentration in the surface water was

very low.

Rather few papers on growth rates of marine Ceratium are

aviable due to diffieulties in eulturing this genus. The three

species whieh dominated the present bloom are ab1e to grow at a wide temperature and salinity range -1 to 29.5 °c and 10 to 35

% 0 , respeetively (Nordli 1957). Culture studies· on growth of

the Ceratium speeies eonsidered. here have revealed that maximal

growth occurrs at 20 % 0 salinity and 15°C. The growth rate was

stronger correlated to temperature than salinity so Nordli

(1957) eoneluded that high temperature was a key faetor for the

development of Ceratium blooms in scandinavian waters. In

addi tion the Ceratium spp. are adapted to growth at low light

intensities; e.g., Malone (1977) reported growth to oeeur at the

1

%

light depth. The average growth rates obtained during this

investigation, 0.15, 0.18 and 0.17 d-1 for Ceratium furea, C.

•

•

maximum growth rate reported in the literature 0.23 to 0.35 d- 1

(Nordli ( 1957) , Elbräehter ( 1973 ) and Wei ler &. Eppeley 1979).

But i t is importent to keep in mind that the size fraetionation

approach assumes that all the predators are removed by

filtration. In this ease one of the important predators, the

heterotrophie dinoflagellates, are of the same size as the

Ceratium and thus. ineluded in the ineubations, resulting in an

underestimation of the Ceratium spp. growth rates.

Dinoflagellates as a group have substantial lower growth rate

than other algaes of the same mass (Banse 1982). but any way

they are able to build up dense population in periods where the zooplankton biomass normally peaks. the following diseussion will

foeus on the potential grazing pressure performed by the

different groups of zooplankton.

Grazing on Ceratium

Among the eiliates (mainly the autotrophie Mesodinium rubrum,

naked oligotriehs and tintinnids) few potential Ceratium grazers

were present. The maximal size of tintinnid prey is determined by

the diameter of the loriea opening and the optimal size is 40

%

of the loriea opening (Heinbokel 1978). During the present study the long slender Helieostomella subulata with a loriea opening of

20-30 ~m totally dominated the tintinnids. The dominating

oligotriehs were all ~ 50 ~m ( Lohmaniella oviformis, L.

spiralis and strombidium spp). Experiments with Lohmaniella

spiralis and two strombidium speeies (Jonsson 1986) revealed

that their optimal prey size was 40% of the peristome as for

tintinnids. So, the only potential eeratia predator among the

•

•

was not very abundant and the annual peak oeeurred one month

after this Ceratium bloom (Nielsen unpublished), although i ts

oeeurrenee is normally restrieted to periods when ~eratium spp.

are eommon (Elbräehter 1973, Smetaeek 1981 and Nielsen & Ki~rboe

submitted). During this study Tiarina fusus was observed to

ingest Ceratium furea and Elbräeher (1973) observed Tiarina

sueking out dividing Ceratium eells before the eells were ful1y

regenerated. The highest abundanee of Tiarina fusus reached

during this investigation was 80 1-1 equivalent to 0.2

~g

Cl-I.

Assuming a growth rate of 0.7 d- l (Nielsen & Ki~rboe, submitted)

and a earbon growth yield of 40

% (

Fenchel 1987) this peak

population would ingest 0.5

~g

C 1-1 d-1. Assuming a maximal

biomass of the bottom and surfaee ceratia bloom of 100 and 150 ~g

C 1-1 respeetively (Fig. 4) and an average growth rate of 0.167

d-l (Table 1), the Tiarina fusus population would be able to

graze at most 0.3 - 0.5

%

and 1.8 - 3

%

of the biomass and

produetion per day, respeetively. Thus the eiliate grazing had

only little effeet on the dynamies of the eeratium bloom.

The most important Ceratium predator among the protozoans is

probably the thecate heterotrophie dinoflagellates whieh are

known to feed on large algaes (Jaeobson

&

Anderson 1986). During

the egg produetion experiments large (80 ~m) Protoperidinium

species were observed wi th Ceratium in their feeding weil. The

annual peak of these large heterotrophie theeate dinoflagellates often oeeurs at periods when Ceratium dominates the phytoplankton

(Smetacek 1981, Hansen in prep). During this Ceratium bloom

Protoperidinium divergens, P. pel1ueidum and members of the

Diplopsalis group dominated the protozoan biomass (Hansen in

during this period. Assuming a growth rate of 0.167 d- 1 (as the ceratia. Table 1) and a yield of 40% the maximal ingestion of

-1 -1

this group is about 9.1 ~g C I d equivalent of 9 and 6

%

of the biomass and 50 and 33

%

of the production per day of the of the surface and bottom ceratium bloom respectively.

Traditionally copepods are considered the most important grazers on the larger phytoplankton species. Despite this and the obvious ecological importance of Ceratium in coastal waters.

•

•

very few papers dealing wi th copepod grazing on Ceratium are available. al though ceratia is believed to be poor food for copepods (Marshai

&

Orr 1955. Conover 1978). Much of the present knowledge is based on data obtained by suboptimal methodology; the copepods have to ingest the theca of the ceratia if gut content or fecal pellet analyses could be used as conclusi ve evidence. A related problem arises when coulter counter is used in enumeration of cells in clearance experiments (e.g. Falkowski el at. 1980). because several papers have documented that copepods can ingest the cytoplasma of larger algaes after they have broken the cells (Beklemishev 1954. Cushings 1955. Marshall

&

Orr 1962. Elbrächter 1973. Schnack 1976 and the present investigation). During the present study the empty cells were treated as ingested by the copepods. The results from the grazing experiments showed that only the largest copepod species (centropages hamatus and C. hamatus ) were able to ingest the ceratia. whereas the smaller neri tic species were unable to ingest Ceratium. The sporadic results from the literature confirms this. Laboratory experiments conducted wi th Acartia. Centropages and Paracalanus in petri dished did not result in any grazing on the Ceratia present (Elbrächter 1973). Mesocoms

experiments eondueted during a dinoflagellate bloom in August 1988 using 10 times natural zooplankton eoneentration (dominated by Oithona sp.), did not reduee the biomass of Ceratium furea. On

the eontrary. presenee of high zooplankton eoneentration

stimulated the growth rate of the dinoflagellate (Graneli el at.

1989). Grazing by Pseudoealanus rninutus, Ternora longirernis,

Oithona similis and Aeartia tonsa on natural phytoplankton

•

•

showed that Ceratium was not utilized (Hargrave 0< Geen 1970).

From fecal pellet and gut eontent analysis Conover (1978)

concluded that even the smallest species of Ceratia were not

ingested by the dominating eopepods (mainly Temora longiremis) in

the Bedford Basin, Canada. In eontrast to this, laboratory

experiments conducted by Schnack (1976) showed that Temora

longicornis had a rather high filtration rate on Ceratiurn

horridurn (about the

sa~e

size as C. tripos ), 17 to 23 ml d-1

ind-1. These filtration rate are of the same order of magnitude

as the clearance rates obtained for Centropages hamatus (10 to 19

rnl d-1) during the present investigation and about half of the

values obtained for the larger C. typieus (27 to 42 ml d-1)

According to Marehall 0< Orr (1955) ceratia are rarely found in

the gut of Calanus. al though they often occur together in the

plankton, and they concluded that Calanus avoid feeding on

Ceratia. Indirect evidenee for Calanus ingestion of Ceratium was

reported by Peterson el at. (in press) during a study of the

copepod production along a transaet across the Skagerrak in

August 1988. They observed a difference in the maximal egg

production of the srnaller copepod species (Paracalanus parvus,

Temora longicorni~ and Acartia longiremis) and the larger species

difference to the ability of the large species to exploit a bloom of Ceratium.

The ratio of observed to maximal egg production (fed ad libitum) of the copepods involved in this study showed that the food conditions was most favorable for the larger species (Centropages typicus. C. hamatus and Calanus ) which produced 52%. 34% and 25% of their maximal egg production respectively. compared wi th the smaller species (Acartia. Paracalanus parvus and Temora longicornis ) which produced 15%. 18% and 20% of their maximal production. This difference may be explained by the ability of the first group to exploit ceratium. The correlation

•

between egg production and the different chlorophyll a fractions somehow supports this. Cf the three species incubated on all sampling occasions Paracalanus parvus showed the best correlation to the total chlorophyll indicated that this species was more food limited than the larger Centropages species. Paracalanus was

•

equally correlated to chlorophyll > < 11 ~m. while Centropages was best correlated to the fraction > 11 ~m. Despite the ability of Centropages hamatus and C. typicus to exp10it the Ceratium bloom they only made up a small fraction of the total copepod biomass . This may be due to the very low production of these species during the previous summer months < 5 eggs d-1

(Ki~rboe

&

Nielsen unpublished).

The other group that characterized the mesozooplankton during this investigation. the cladocerans. made up 14 to 60

%

of the crustacean zooplankton biomass. Distinct peaks of cladocerans in late summer is common in rnany marine environments; e.g .• Kiel bay ( Poggensee &. Lenz 1981). Bothnian Sea (Erikson el at. 1977). Kattegat (Eriksson 1974). North atlantic and North sea (Gieskes

•

•

1971a), Chesapeake Bay (Boseh

&

Taylor 1973), Los Angeles Beaeh

harbor (Morey-Gaines 1979) and the whi te Sea (Makrushin 1981).

The eeologieal importanee of eladoeerans is often ignored or

strongly underestimated during routine" plankton studies, where

sampling intensi ty normally is too low to deteet and deseribe

eladoeeran population dynamies. Their reproduetion is prineipally

parthenogenetie, whieh means that populations ean build up very

rapidly. The duration of these peaks is very short whieh render

very frequent sampling if population dynamies has to be

investigated. The physieal and ehemieal parameters that limits

the development and distribution of marine eladoeerans is fairly

weIl understood (Aekerfors 1971, Gieskes 1971 a, b, Eriksson

1977, Poggensee & lenz 1981). But despite their wide

distribution, the knowledge of the feeding biology of the

podonidae is very limited. Possible major reasons for the laek of

informations on this group is tradition and the problems in

eulturing eladoeerans, due to the hydrophobie earapaee of the

animals whieh easily is eaptured in the surfaee tension. From the

large eyes and the raptorial legs and mouthparts most authors

presume that the podnidae feed on large prey. The only exeeption

to this is Penilia avirostris, that exelusively feed on small

partieles (Paffenhöfer & Oreutt 1986, Turner el at. 1988).

Seanning eleetron mieroseope (SEM) studies on the morphology of

the mouth parts of podonida (Nival & Ravera 1979,1981) revealed

that they probably eonsume partieles from 20 to 170 ~m in

diameter. Examinations of what preserved Evadne nordmanni were

gasping between the endite of second and third leg or the mouth

parts indieated that the preferred prey were tintinnids and

•

(Bainbridge 1958). Studies of gut content of Podon leukarti and

Evadne nordmanni showed that they probably were feeding on

phytoplankton (Skeletonema costatum and porocentrum balticum

dominated the phytoplankton during the sampling) (Poggensee &.

Lenz 1981). A striking feature is that the cladocerans peaks very

often is contemporary wi th dinoflagellate blooms. Thus,

Morey-Gaines (1979) found a significant corelation of a Podon (Pleopis

polyphemoides) and a Ceratium spp. bloom in the Los Angelse Beach

harbor. Inspection of gut content revealed that 30% of the

examinde individuals contained Ceratium thecal plates. To my

knowledge the only feeding experiments conducted with raptorial

marine cladocerans is Jagger·el at:'s (1988) work with Podon

intermedius. From SEM inspection of faecal pellets they concluded

that they preferred large diatoms (Rhizosole~ia). Although

Ceratium was abundant on the sampling locality no remains were

found in the fecal pellets. Feeding experiments showed no

clearance on Tetraselmis chui (8 ~m). Procentrum gracilis (40

*

15

~m)

and Hemiaulus sp. (60

~m)

but 2 12 ml d-1 in the

experiment using Rhizosolenia (150

*

20 ~m).

The vertical distribution of the cladocerans during this

•

investigation showed that they peaked wi thin the layers

containing the highest Ceratium concentration and wi thin these

depths Ceratium spp totally dominated the potential food within

the range proposed by Nival &. Ravera (1981). The clearance

experiments showed that Evadne nordmanni and Podon were able to

clear 3 - 8 and 3 -10 ml d-1, respectively in experiments using

the dominating Ceratium , whic}l is of the same order of magnitude as the resu1ts of Jagger el at.(1988).

•

were cleared for Ceratiurn furca, C. fusus and C. tripos by crustaceans. If the growth rate rneasured in the surface (Table 1) is taken as representative for the entire water column, the crustacean zooplankton (totally dominated by cladocerans) 33, 27 and 70

%

of the daily Ceratium production. The high Evadne nordrnanni population in and around the pycnocline during the last part of the investigation, may weIl be responsible for the disappearance of the bloom in the bottom waters; at this time the bloom persisted in the surface where the cladocera was only one quarter on the pycnocline biomass.

In conclusion i t can be summarized that, contrary to the general view, a substantial part of the production of a "normal" Ceratium bloom can be decomposed in the pelagic zone. The most important grazers the heterotrophie dinoflagellates and the cladocerans have not received much attention so far, but these groups alone possesses the potential of controlling the developrnent of Ceratiurn bloorns, so future investigations have to include them if the dynamics of the Ceratium blooms have to be fully understood .

•

•

ACKNOWLEDGEMENTS

I want to thank Thomas Ki~rboe for inspiring coporation, Tom Fenchel, Per Juel Hansen and Thomas Ki~rboe for critically reading the manucript and Alice Christoffersen, Jack Melby and Lisbeth Olsen for technical assistance. And the crew on ~ ~ Ophelia Bendt J~rgensen and Benly Thrue for the help with sampling. This investigation was supported by grants from the Danish environmental protection agency (HF-gO, 2-03b) .

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