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Marine Bio logy 67, 283-288 (1982) MARINE BIOLOGY9 Springer-Verlag 1982

Estimating the Grazing Impact of Marine M icro-zoop lankton *M. R. Landry and R. P . HassettScho ol o f Oceanography, WB-10, University of Washington; Seattle, Wa shington 98195, U SA

AbstractThis paper describes a dilution technique for estimatingthe micro-zooplankton grazing impact on natural com-munities of marine phytoplankton. Experiments performedin coastal waters off Washin gton, US A (October, 1980),yield estimates of micro-zooplankton impact equivalent to6 to 24% ofph ytop lank ton standing biomass and 17 to 52%of production per day. Indirect evidence suggests that mostof this impact is due to the feeding of copepod nauplii andtintinnids; in contrast, non-loricate ciliates, com-prising 80 to 90% of numeri cal a bund ance, app eared tocontribute little to phytoplankton mortality.

IntroductionThe micro-zooplankton is the componen t o f the marineplankton consisting o f Protozoa and Metazoa w hich pass a200/~m mesh screen (Dussart, 1965). These organisms areindividually inconspicuous, rarely dominate zooplanktonbiomass, and, consequently, receive less attention than lar-ger zooplankton; even so, their role in marine food websma y be significant since, by virtue o f small size, they havedispro portio nately high specific rates of growth, metab -olism, and feeding (Zeuthen, 1947; Johannes, 1964; Fen-chel, 1974; Hein bokel , 1978 a). Moreo ver, micro-z ooplan k-ton generally feed on the smaller sizes of particulates,which are not utilized efficiently by large consumers; thus,the micro-zooplankton, as trophic intermediates, make theconsiderable production o f nanno- and ultraplankton ac-cessible to higher order consumers (Beers and Stewart,1967; Parsons and LeBrasseur, 1970; Berk et al., 1977).The magnitude of the micro-zooplankton grazing onmarine phytoplankton has usually been estimated indi-rectly from production budgets o f phytopla nkton (e.g. Ri-* C ontribution No. 1237 from the School of Oceanography, Uni-

versity of Washington, Seattle, Washington 98195, USA

ley, 1956) and energetic requiremen ts of organismsbased on size (e.g. Beers and Stewart, 1971). Only recentlyhave efforts been made to measure grazing impact moredirectly. One approach is to extrapolate from laboratory-determined feeding relationships to field situations ofknown species abundances of micro-zooplankton and sizecomposition of potential prey (e.g. H einbok el an d Beers,1979). Give n the difficulty of individu ally manip ulatingtiny organisms in diverse, natural assemblag es of plankton,this approach is frequently the only viable alternative forestimating th e grazing impact o f particular species orgroups (e.g. tintinnids) o f micro- zoopl ankton whose feed-ing rates, behavior, and prey preferences are adequatelyknown from laboratory studies. H owever, few such experi-mental data exist for most groups of micro-zooplankton,including the abundant oligotrichs; therefore, the ap-proach, in addition to being laborious, is generally unsuit-ed for the estimation of total micro-zooplankton impact onphytoplankton.

A more direct technique for estimating micro-zoo-plankton feeding rates in nature was presented b y Capriuloand Carp enter (1980). The natural a ssembla ge of plankt onis divided into two size components: one fraction, whichpasses a 35 ktm screen, contains few micro-z oopl ankto n butthe majo rity of their preferred fo od and serves as a control;the other fraction (prescreened through 202/~m netting toremove macro-zooplankton) is concentrated behind a35/zm screen to 5-10 times the natural density. Grazingrates are measured, relative to the control, in a mixture ofthe smaller an d larger size fractions. On e dr awb ack of thistechnique is that phytoplankton abundance and size com-position differ between experimental and control contain-ers; therefore, interpretation of grazing impact from gen-eral measures o f phytoplan kton biomass (e .g. chlorophyllconcentrations) is ambiguous; i.e. , one presumes that themeasured disappearance of chlorophyll was from the smal-ler size fraction. An even more important limitation is thatthe technique measures grazing impact not for the entiremicro-zooplankton community but only for the size frac-

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284 M.R. Land ry and R. P. Hassett: Grazing by Micro-zooplanktont i o n r e t a i n e d b y a 3 5 ~ m s c re e n . F o r e x a m p l e , n o n - l o r i c a t ec i l i a t e s , w h i c h g e n e r a l l y d o m i n a t e t h e m i c r o - z o o p l a n k t o n(Bee rs and S tew ar t , 1970; Bee r etal . , 1975), a re not re-t a ined , ev en by m es h a s s ma l l a s 20 k tm (S me tac ek , 1981) .T h e a p p a r e n t d o m i n a n c e o f t i n t in n i d s in s a m p l e s c o n c e n -t r a t e d b y C a p r i u l o a n d C a r p e n t e r ( 1 9 8 0 ) m a y b e t h e r e s u l to f t h is r e t e n t i o n p r o b l e m .

I n t h e p r e s e n t p a p e r , w e r e p o r t o n a n e x p e r i m e n t a lt e c h n i q u e f o r m e a s u r i n g t h e n a t u r a l g r a z i n g i m p a c t o f m i -c r o - z o o p l a n k t o n c o m m u n i t i e s , a n d g i v e t h e r e su l t s o fi n i t i a l e x p e r i m e n t s p e r f o r m e d i n t h e c o a s t a l w a t e r s o fW a s h i n g t o n s ta t e, U S A . T h e r e l a t i v e ly s im p l e t e c h n i q u e i sb a s e d o n d i l u t i o n o f n a t u r a l s e a w a t e r r a t h e r t h a n c o n c e n -t r a t i o n o r f r a c t i o n a t i o n a n d i n v o l v e s m i n i m a l h a n d l i n g o ft h e l i v e p l a n k t o n s a m p l e .

M a t e r i a l s a n d M e t h o d s

T h e o r e t i c a l C o n s i d e r a t i o n sW e m a d e t h r e e a s s u m p t i o n s r e g a r d i n g t h e i n t e r a c t i o n sa m o n g n u t r i e n t s , p h y t o p l a n k t o n , a n d m i c r o - z o o p l a n k t o ni n t h e s e a. F i r st , w e a s s u m e d t h a t g r o w t h o f i n d i v i d u a l p h y -t o p l a n k t o n i s n o t d i r e c t l y a f f e c t e d b y t h e p r e s e n c e o r a b -s e n ce o f o t h e r p h y t o p l a n k t o n per se . T h e i m p l i c a t i o n o f t h isa s s u m p t i o n i s t h a t a r e d u c t i o n i n t h e d e n s i t y o f ce l ls i nna tu ra l s eaw a te r w i l l no t , i n an d o f it s e lf , d i rec t ly caus e achang e in the g row th ra t e o f r em a in ing cel ls . Second , wea s s u m e d t h a t t h e p r o b a b i l i t y o f a p h y t o p l a n k t o n c e l l b e i n gc o n s u m e d i s a d i r e c t f u n c t i o n o f t h e r a t e o f e n c o u n t e r o fcons umers w i th p rey ce l l s . T h i s imp l i e s tha t cons umers a ren o t f o o d - s a t i a t e d a t n a t u r a l p r e y d e n s i t i e s a n d t h a t t h en u m b e r o f p r e y in g e s t e d b y a g i v e n c o n s u m e r i s l i n e a r l y r e -l a t e d t o p r e y d e n s i ty . T h i r d , w e a s s u m e d t h a t c h a n g e i n t h ed e n s i t y o f p h y t o p l a n k t o n , P , o v e r s o m e t i m e , t, c a n b e r e p -r e s e n t e d a p p r o p r i a t e l y b y t h e e x p o n e n t i a l e q u a t i o n .

Pt = Po e(k-g)t, (1 )w h e r e k a n d g a r e i n s t a n t a n e o u s c o e f f ic i e n ts o f p o p u l a t i o ngrowth and g raz ing mor ta l i ty , r e s pec t ive ly . T h i s i s a com-m o n a s s u m p t i o n i n m o s t f e e d i n g s t u d i e s i n v o l v i n g p l a n k -ton . A con s tan t g row th coe f f i c i en t , k , fo l lows f rom our f i r s ta s s u m p t i o n i f c o n c e n t r a t i o n s o f n u t r i e n t s a n d o t h e r g r o w t hf a c t o r s r e m a i n a p p r o x i m a t e l y c o n s t a n t ( a n d / o r n o n l i m i t -i n g ) . A c c o r d i n g t o o u r s e c o n d a s s u m p t i o n , t h e m o r t a l i t yc o e f f i c ie n t g v a r i e s d i r e c t l y w i t h t h e d e n s i t y o f c o n s u m e r sb u t i s n o t a f f e c t e d b y c h a n g e s i n p h y t o p l a n k t o n c o n c e n t r a -t i o ns . T h e c o e f f ic i e n ts k a n d g m a y v a r y w i t h t i m e o f d a yw i t h o u t a f f e ct i n g o u r c o m p a r i s o n s o f g r o w t h r a t e s o fn a t u r a l p h y t o p l a n k t o n i n d i f f e r e n t d i l u t i o n s o v e r a f i x e dp e r i o d o f in c u b a t i o n .

G i v e n o u r t h r e e a s s u m p t i o n s , w e n o w c o n s i d e r t h e i m -p l i c a ti o n s o f d i lu t i n g n a t u r a l s e a w a t e r c o n t a i n i n g b o t hp h y t o p l a n k t o n a n d s m a l l c o n s u m e r s w i t h f i l t e r e d s e a w a t e rf r o m t h e s a m e s o u r c e . T h e i n s t a n t a n e o u s g r o w t h r a t e o f in -d i v i d u a l p h y t o p l a n k t o n c e l l s s h o u l d n o t c h a n g e a c c o r d i n gt o o u r f i r s t a s s u m p t i o n , p r o v i d e d t h a t n u t r i e n t l e v e l s d o n o t

c h a n g e a p p r e c i a b l y d u r i n g t h e i n c u b a t i o n . H o w e v e r , t h ei n s t a n t a n e o u s r a t e o f p h y t o p l a n k t o n m o r t a l i t y s h o u l d d e -c l in e i n d i r e c t p r o p o r t i o n t o t h e d i l u t i o n e f f e c t o n c o n s u m -e r d e n s i ty . T h a t i s, a l t h o u g h i n d i v i d u a l c o n s u m e r s c o n t i n u et o h a v e a c o n s t a n t i m p a c t o n t h e p h y t o p l a n k t o n p o p u -l a t i o n ( m e a s u r e d , f o r e x a m p l e , a s c l e a r a n c e r a t e p e r c o n -s u m e r) , t h e c o m b i n e d i m p a c t o f t h e c o n s u m e r p o p u l a t i o ni s l es s becaus e the r e a re few er cons umers .R a t e s o f p h y t o p l a n k t o n g r o w t h a n d g r a zi n g m o r t a l i tyc a n b e i n f e r r e d f r o m o b s e r v e d c h a n g e s i n p o p u l a t i o n d e n -s it y f o l l o w i n g i n c u b a t i o n s o f d i f f e r e n t d i lu t i o n s o f n a t u r a ls eawa te r . Fo r example , g iven a d i lu t ion s e r i e s cons i s t ing o fun f i l t e red to f i l t e red s eawa te r in the ra t io s 1 :0 (100% un-f i l te red seaw ater) ; 3 :1 (75%); 1 :1 (50%); and 1:3 (25%), thea p p r o p r i a t e e q u a t i o n s d e s c r i b i n g t h e c h a n g e s i n p h y t o -p lank ton ove r t ime , t , a re : Pt = Poe (k-g)t (i.e., 1/t in(P t /Po) = k - l . 0 g ) , P t = Poe (k-~ (i.e., 1/t In(P t /Po) = k - 0 . 7 5 g ) , P t = Po e(k-~ (i .e. , 1/t In( P J P o ) = k - 0 . 5 g ) , P t = Poe(k-o.25g)t (i.e., 1/t in( P J P o ) = k -0 . 25 g) . In th i s s e r ie s o f equa t ions , t he ob -s e r v e d r a t e o f c h a n g e o f p h y t o p l a n k t o n d e n s i t y a t t h e d i f-fe ren t d i lu t ions i s l i nea r ly re l a t ed to the d i lu t ion fac to r( d e c i m a l f r a c t i o n o f u n f i l t e r e d s e a w a t e r) . T h e n e g a t i v es lope o f th i s r e l a t ions h ip i s t he g raz ing co e f f i c i en t g ; t heY-ax i s in t e rcep t i s t he phy top lank ton g rowth ra t e k . I t i sn o t n e c e s s a r y to p e r f o r m e x p e r i m e n t s a t m a n y d i f f e r e n t d i -l u t i o n l e v e ls i n o r d e r t o e s t im a t e g r o w t h a n d g r a z i n g c o ef -f i ci e n ts ; t h e o b s e r v e d r a t e s o f c h a n g e o f p h y t o p l a n k t o ndens i ty a t any two d i lu t ion l eve l s w i l l y i e ld two equa t ionsw i t h t w o u n k n o w n s w h i c h c a n b e s o l v e d e x p l i c it l y f o r gand k . L ine a r reg re s s ion ana lys is , how eve r , w i l l p rov ide e s -t ima te s o f con f iden ce l imi t s fo r the coe f f i c i en t s .

E x p e r i m e n t a l D e s i g n a n d A n a l y s i sT h e p r e c e d i n g e x p e r i m e n t a l d e s i g n f o r e s t i m a t i n g m i c r o -zoop lank ton g raz ing was t e s ted on a c ru i se aboa rd the R . V ." W e c o m a " i n c o a s ta l w a t er s o f f W a s h i n g t o n d u r i n g O c t o -b e r , 1 9 8 0 . E x p e r i m e n t s w e r e p e r f o r m e d a t 3 s t a t io n s o v e r -l y i n g w a t e r c o l u m n d e p t h s o f 2 0, 5 0, a n d 2 0 0 m a n d r a n g -i n g f r o m 7 t o 5 0 k m f r o m s h o r e .

A P h o e b e b o t t l e w a s u s e d t o c o ll e c t a p p r o x i m a t e l y 8 0t o 9 0 l i te r s o f s ea w a t e r f r o m 3 m d e p t h f o r e a c h e x p e r i -m e n t . H a l f o f th e w a t e r w a s f i l t e r e d th r o u g h a 0 . 4 5 / z m M i l-l ipo re f i l t e r he ld in a l a rge vo lume f i l t r a t ion appa ra tus .T h i s f i lt e r e d w a t e r w a s t h e n c o m b i n e d w i t h t h e r e m a i n i n g ,un f i l t e r ed s eaw a te r in ra t io s o f 1 :0 , 3 :1 , 1 :1 , and 1 :3 un f i l -t e red to f i l t e red wa te r . F ive 2 - l i t e r g la ss re agen t bo t t l e sw e r e f i l l e d w i t h e a c h d i l u t i o n m i x t u r e . T o i n s u r e t h a t n u -t r i e n t s w o u l d b e e q u a l l y a v a i l a b l e t o p h y t o p l a n k t o n a t a l ld i lu t ion l eve l s, exces s n i t r a t e (10 r 1 -1) and phos ph a te( 1 / z g - a t 1- 1) w e r e a d d e d t o e a c h b o t t l e . I n e a c h e x p e r i m e n t ,s eve ra l add i t ion a l bo t t l e s o f the d i f fe ren t d i lu t ion l eve l sw e r e p r e p a r e d w i t h o u t t h e a d d i t i o n o f n u t r i e n ts . A l l r e -a g e n t b o t t l e s w e r e s e a l e d w i t h o u t a i r b u b b l e s a n d a t t a c h e dto a ro ta t ing whee l con ta ined w i th in a l a rge , c l ea r p l a s t i c ,w a t e r - c o o l e d i n c u b a t o r a b o a r d t h e r e s e a r c h v e s s e l . T h e

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M. R. Lan dry and R. P. Hassett: Grazing by Micro-zooplankton 285b o t t l es w e r e t h e n a l l o w e d t o i n c u b a t e a t a m b i e n t l i g h t .9l e v e ls a n d s u b s u r f a c e w a t e r t e m p e r a t u r e s f o r 2 4 h . .8

In a va r i a t ion on the ba s i c exp e r im en ta l de s ign , the 4 .7d i l u t i o n m i x t u r e s i n o n e e x p e r i m e n t w e r e a l so d i s p e n s e d i n .6t r ip l i c a t e in to l - l i t e r vo lume d ia lys i s s ac s (Spec t rapor 2 ,

.564 m m d iame te r , 12 000 M W cu to f f ) . T h e s ac s we re in - " ~ .4d i v i d u a l l y p l a c e d i n t o n y l o n m e s h b a g s , t i e d t o a l i n e s ot h a t t h e y w o u l d b e s u s p e n d e d 3 m b e l o w a s u r f ac e b u o y , - g.3a n d i n c u b a t e d in situ fo r 24 h. _'2- 2

A t t h e s t a r t o f a l l e x p e r i m e n t s , d i l u t i o n m i x t u r e s w e r e ~ . ,s am pled fo r nu t r i en t s - (n i t r a t e , n i t r i t e , am m on im n , phos - ~< opha te , and s il i c a te ) , ch lo r ophy l l a , and abu nda nce s o f = .9m i c r o - z o o p l a n k t o n ( p r e s e r v e d i n L u g o l ' s i o d i n e f i x a t i v e ) . O ,8I n d i v i d u a l b o t t l es w e r e s a m p l e d f o r c h l o r o p h y l l c o n t e n t a t .7t h e e n d o f e x p e r i m e n t s ; g e n e r a l ly , o n l y e x p e r i m e n t a l c o n - ~-t a i n e rs t h a t i n i t ia l l y c o n t a i n e d 1 0 0 % u n f i l t e r e d s e a w a t e r z .6were s amp led fo r f ina l nu t r i en t s and mic ro -zo op la nk to n , o_~ .5N u t r i e n t s a n d c h l o r o p h y l l w e r e a n a l y z e d a c c o r d i n g t o < .4m e t h o d s i n S t r i c k l a n d a n d P a r s o n s ( 1 9 7 2 ) a n d L o r e n z e n .3( 19 66 ), r e s p e c ti v e l y . M i c r o - z o o p l a n k t o n a b u n d a n c e f r o m

,2s e t t le d v o l u m e s o f 1 0 0 m l p e r s a m p l e w a s m e a s u r e d w i t ha n i n v e r t e d m i c r o s c o p e . ~

T h e a p p a r e n t g r o w t h r a te s o f p h y t o p l a n k t o n i n i n d iv i d - ou a l r e a g e n t b o t t l e s w e r e c a l c u l a t e d f r o m E q . ( 1 ) u si n g c h l o -r o p h y l l a s th e m e a s u r e o f p h y t o p l a n k t o n s t a n d i n g s t o c k.I n s t a n t a n e o u s c o e f f ic i e n ts o f p h y t o p l a n k t o n g r o w t h ( k )a n d m i c r o - z o o p l a n k t o n g r a z in g ( g) w e r e d e t e r m i n e d f r o mleas t - s qua re s an d l ine a r reg re s s ion ana lys i s o f the re l a t ion -s h i p b e t w e e n t h e r a t e o f c h a n g e o f c h l o r o p h y l l a n d t h ef r a c t io n o f u n f i l t e r e d s e a w a t e r i n t h e v a r i o u s b o t t l e s. C l e a r -ance ra t e e s t ima te s , exp re s s ed a s m l an im a l -~ d -~ , we re ca l -c u l a t e d b y d i v i d i n g t h e e s ti m a t e o f t h e m i c r o - z o o p l a n k t o ng r a z i n g i m p a c t b y t h e d e n s i t y o f m i c r o - z o o p l a n k t o n , d e -t e r m i n e d f r o m m i c r o s c o p i c a l c o u n t s .

Re su l t s

T h e r e s u lt s o f t h r e e e x p e r i m e n t s t e s t in g t h e d i l u t i o n a p -p r o a c h t o e s t i m a t i n g t h e g r a z in g i m p a c t o f m i c r o - z o o -p l a n k t o n c o m m u n i t i e s a r e p r e s e n t e d i n F i g . 1 . I n E x p e r -im en t 1 A , a g raz ing coe f f i c i en t o f 0 . 278 d -1 was de te r -m i n e d f r o m t h e r e g r e s s io n e q u a t i o n ( 95 % c o n f i d e n c e in -t e rva l fo r g = 0 . 189 to 0 .367) . T h i s l eve l o f g raz ing ac t iv i tyc o r r e s p o n d s t o a l o ss o f a p p r o x i m a t e l y 2 4% o f p h y -t o p l a n k t o n s t a n d i n g c r o p p e r d a y ( 1 7 t o 3 1 % ) . T h e g r o w t hcoe f f i c i en t fo r phy top lan k to n was 0 .628 d -1 , s om ewh a t l e sst h a n o n e d o u b l i n g p e r d a y . G e n e r a l l y , b e c a u s e n u t r i e n t sw e r e a d d e d t o t h e e x p e r i m e n t a l c o n t a i n e r s , w e w o u l d n o te x p e c t t h e c a l c u l a t e d g r o w t h c o e f f i c i en t f r o m t h e d i l u t i o ne x p e r i m e n t t o r e f l e c t a c c u r a t e l y t h e g r o w t h r a t e o f p h y -top lank ton in the f i e ld . In t e re s t ing ly , howeve r , t he d ia lys i ss ac va r i a t ion o f E xp e r im en t 1 ( i .e . , 1 B ) gave a s im i la r e s t i -m a t e o f p h y t o p l a n k t o n g r o w t h r a t e w h i c h w o u l d s u g g es tt h a t , a t t h e t i m e o f th i s e x p e r i m e n t , t h e f i e l d p o p u l a t i o nw a s n o t n u t r i e n t - li m i t e d . T h e r e f o r e , i f w e a s s u m e a n in situp h y t o p l a n k t o n g r o w t h r a t e o f 0 .6 28 d -~ a n d s t e a d y s t a t e,t h e m i c r o - z o o p l a n k t o n g r a z i n g e f f e c t m e a s u r e d i n E x p e r -

E X P 1 Ay = 0 . 6 2 8 - 0 . 2 7 8 Xr 2 =0 . , 0 ,

n;2o

l l l l l l lo

I I .J

E X P 1 By = O . 6 2 0 - O A 7 4 Xr 2 = 0 . 4 8 2

r l=8

i F i l l l l l l lE X P 2y = 0 .4 5 5 - 0 . 0 6 5 xr 2 = o . 0 8 zi3=20

o

E X P 3y = 0 . 5 8 5 - 0 . 1 2 5 r 2 = 0 . 564n = 2 08

I I' ' , ' ; 1 6 ' 9 , '.2 i ' 9 , ! o o ; ' . 4 .F R A C T I O N U N F I L T E R E D S E A W A T E R

Fig. 1. Results of 3 dilution experiments performed off the o utercoast of Washington in October, 1980 to estimate m icro-zooplank-ton grazing impact on m arine phytoplankton. Exp eriments 1 A, 2,and 3 were conducted usin g on-deck incubation techniques; Ex-periment 1B was conducted in situ using dialysis sacs. Filled cir-cles: bottles with added nutrients (excep t dialys is experim ent);ope n circles; bottles without add ed nutrients. Lines are fit by least-squares to the points. P0, initial phytoplankon density; Pt, densityat time t

i m e n t 1 A a c c o u n t s f o r a d a i l y l o ss o f a b o u t 5 2 % o f p r o -d u c t i o n .

E igh t o f 12 d ia lysi s s ac s u s ed in E xp e r im en t 1 B werer e c o v e r e d u n d a m a g e d a n d , o f th e se , 7 y i e ld e d a p p a r e n tg r o w t h r a t e s w h i c h w e r e i n t h e r a n g e o b s e r v e d f o r s im i l a rd i l u ti o n s i n E x p e r i m e n t 1 A ( F i g. 1 ). H o w e v e r , t h e o n ed i v e r g e n t d a t a p o i n t , t h e o n l y s a c r e c o v e r e d w i t h u n d i l u t e ds eawa te r , con t r ibu ted s ubs tan t i a l va r i ab i l i t y to the reg re s -s i o n a n a l ys is . T h e r e s u l t in g a v e r a g e o f t h e g r a z i n g c o -e f f i c ien t , 0 .174, ha s b roa d co nf ide nce limi t s and , w h i l e no ts t at is t ic a l ly d i f f e r e n t f r o m t h e e s t i m a t e o f g i n E x p e r i m e n t1 A , w a s o n l y m a r g i n a l l y d i f f e r e n t f r o m z e r o(0.05

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286 M.R. Land ry and R. P. Hassett: Grazing by Micro-zooplanktonT a b l e 1. Value s of variables measured for dilution experimentsMeasured parameter Experiment No.

1 2 3

Initial nutrients (~ g-at 1-1)Nitrate a 1.20 0.41 0.88Nitrite 0.19 0.15 0.20Am mon ium 0.47 0.56 0.25Phosphate ~ 0.97 0.50 0.52Sili cate 15.0 11.2 14.8

Initial chlorophyll-a ~ g 1 1) 3.54 2.03 6.77Micro-zo oplankton den sity (No. 1-1)

Copep od naupfii 160 20 80Tintinnids 2 000 760 360Non -loficate ciliates 20 000 27 000 2 700" Excessadded to each bottle

A m b i e n t c o n c e n t r a t i o n s o f n u t r i e n t s a t t h e t im e s t h e e x -p e r i m e n t s w e r e r u n a r e g i v e n i n T a b l e 1 . G e n e r a l l y , t h e s ec o n c e n t r a t i o n s a p p e a r e d s u f fi c ie n t t o s u p p o r t t h e s a m el e v e l o f p h y t o p l a n k t o n g r o w t h o b s e r v e d i n th e p r e s e n c e o fexces s nu t r i en t s (F ig . 1 ) , bu t on ly a t t he mos t d i lu t e con -c e n t r a t i o n s o f p h y t o p l a n k t o n u s e d i n t h e e x p e r i m e n t s ( i .e .,1 :3 ra t io o f un f i l t e r ed to f i l t e red s eawa te r ) . Se ve re ly de -p r e s s e d g r o w t h r a t e s w e r e o b s e r v e d w h e n e v e r u n d i l u t e dc o n c e n t r a t i o n s o f p h y t o p l a n k t o n w e r e i n c u b a t e d i n b o t tl e sw i t h o u t t h e a d d i t i o n o f e xc e ss n u tr i e n ts . T h i s w a s p r o b a b l yd u e t o n i t r a t e l i m i t a t i o n s in c e , o f t h e 5 n u t r i e n t s m e a s u r e d ,n i t ra t e w as the on ly on e dec rea s ing to low l eve l s (0 .1 ~g -a t 1 -1 o r l es s ) wh en g row th was dep re s s ed . N i t ra t e andphos pha te concen t ra t ions neve r fe ll be low 7 and 1 ~g -a t 1 1 ,re s pec t ive ly , i n con ta ine rs whe re they we re in i t i a l ly addedin exces s ; o the r nu t r i en t s changed l i t t l e du r ing the incu -ba t ions .

D i s c u s s i o n

O u r d i l u t i o n m e t h o d f o r e s t i m a t i n g m i c r o - z o o p l a n k t o ng r a z i n g i m p a c t o n p h y t o p l a n k t o n g i v e s r e g r e s s i o n e q u a -t ions w i th nega t ive s lopes , and the re s u l t ing e s t ima te s o fp h y t o p l a n k t o n g r o w t h a n d m o r t a l i t y s e e m r e a s o n a b l e .H o w e v e r , b e f o r e c o m p a r i n g t h e r e s u l ts a n d i m p l i c a t io n s o ft h e s e e x p e r i m e n t s w i t h p r e v i o u s e s t i m a t es o f m i c r o - z o o -p l a n k t o n g r a z in g , w e p o i n t o u t t h e s o u r c e s o f p o t e n t i a l b i a si n t h e a p p r o a c h .

T h e c r i ti c a l a s s u m p t i o n i n t h e d i l u t i o n a p p r o a c h i s t h a tm i c r o o r g a n is m s c o n s u m e p r e y i n d i r e c t p r o p o r t i o n t o p r e ydens i ty , mor e s pec i f i c a l ly , t ha t t h e n a tu ra l l eve l o f ava il -ab le fo od i s s uch tha t i nge s t ion ra t e s o f the s e o rgan i s m s a ren o t s a t u r a t e d . A t v e r y h i g h f o o d l e v e l s t h is w o u l d n o t b et r u e f o r a l l o r p a r t o f t h e g r a z i n g p o p u l a t i o n . I n t h e e x -t r e m e c a s e, e a c h c o n s u m e r w o u l d e a t a c o n s t a n t n u m b e r o fp r e y r e g a r d le s s o f t h e d i l u t i o n e f f e c t o n p r e y d e n s i t y . T h i sw o u l d r e s u l t i n c o n s t a n t , p e r c a p i t a m o r t a l i t y o n p h y t o -p l a n k t o n a t a ll d i lu t i o n s, a n d g r a z i n g r a te w o u l d a p p e a r to

be neg l ig ib le s ince i t s e f fec t wo u ld b e ind i s t ingu i s hab lef r o m c o n s t a n t p h y t o p l a n k t o n g r o w t h . I n t h e l e s s e x t r e m ec a s e o f s a t u r a t e d f e e d i n g b y o n l y a f r a c t i o n o f t h e c o n -s umers o r on ly a t t he h ighes t p rey dens i t i e s u s ed in expe r i -m e n t s , p h y t o p l a n k t o n g r o w t h a n d g r a z i n g m o r t a l i t y w o u l db e u n d e r e s t i m a t e d . I n l a b o r a t o r y s t ud i e s w i th t h r e e c o a s t a ls p e ci e s o f t i n ti n n i d s, H e i n b o k e l ( 1 9 7 8 a ) f o u n d i n g e s t io nr a t e s t o b e a p p r o x i m a t e l y l i n e a r l y r e l a t e d t o f o o d c o n c e n -t r a t i o n u p t o a b o u t 1 00 ~ g c a r b o n 1 - 1. A l t h o u g h c o n c e n t r a -t i o n s o f p a r t i c u l a t e c a r b o n a r e f r e q u e n t l y h i g h e r t h a n t h isl e v e l in n a t u r e , t h e f e e d i n g o f i n d i v i d u a l s p e c ie s o f m i c r o -z o o p l a n k t o n i s l i m i t e d g e n e r a l l y , b e c a u s e o f p r e f e r e n c e(e . g . S toecke r et a l . , 1981) , behav io r (e . g . Ras s ou lzadeganand E t i enn e , 1981) , o r foo d hand l ing e f f i c i enc ie s (e. g. ,H e i n b o k e l , 1 9 7 8 b ), t o o n l y a f r a c t i o n o f t h e s i ze r a n g e o fto ta l pa r t i cu la t e s .

An oppo s i t e b i a s (i .e ., ove r -e s t im a t ion o f g raz ing im-p a c t ) , w o u l d o c c u r i f a m b i e n t f o o d l e v e ls w e r e s o l o w t h a tm i c r o - z o o p l a n k t o n r e s p o n d e d t o d e c r e a s e d f o o d l e v e l s( i .e . , d i lu t ions o f p rey ) by redu c ing the i r f e ed ing e f fo r t .T h i s b e h a v i o r , t e r m e d t h r e s h o l d f e e d i n g r e s p o n s e , h a sb e e n d e m o n s t r a t e d f o r p la n k t o n i c , f i lt e r - f e e d in g c o p e p o d sw h e r e i t a p p a r e n t l y s e r v e s a n e n e r g y o p t i m i z i n g f u n c t i o n(e . g . F ros t , 1975 ; L am and Fros t , 1976) . T hre s ho ld feed ingi s no t l i ke ly to be a s s ign i f i c an t a p rob lem in the d i lu t ionexpe r imen t s a s o the r pos s ib le e f fec t s , s uch a s s a tu ra t edfeed ing . He inb oke l (1978 a ) , fo r in s t ance , d id n o t ob s e rvet h r e s h o l d b e h a v i o r i n h i s f e e d i n g e x p e r i m e n t s w i t h t i n -t inn ids . M oreove r , i t i s no t c l ea r tha t o rgan i s ms wh ich de -p e n d o n r a n d o m c o n t a c t w i t h f o o d p a r t i c l e s a n d a r ec h a r a c t e r i z e d b y h i g h s p e ci f ic r a te s o f b a s a l m e t a b o l i s mw i l l g a i n a l o n g - t e r m e n e r g e t i c a d v a n t a g e b y r e d u c e dfo rag ing ac t iv i ty a t l ow dens i t i e s o f food .T h e r e s u lt s o f th e d i l u t i o n e x p e r i m e n t s w i t h a n d w i t h -o u t a d d e d n u t r i e n t s d e m o n s t r a t e t h e i m p o r t a n c e o f th e n u -t r i e n t t r e a t m e n t i n t h e e x p e r i m e n t a l d e s i g n a n d e m p h a s i z et h e w e a k n e s s o f p h y t o p l a n k t o n e x p e r i m e n t s i n v o l v in g a p -p r e c i a b l e p e r i o d s o f i n c u b a t i o n i n c l o s ed c o n t a i n e r s . I t isc l e a r f r o m t h e r e s u l ts o f E x p e r i m e n t 3 , f o r i n s ta n c e , t h a tm a r k e d l y d i f f e r e n t c o n c l u s i o n s a b o u t p h y t o p l a n k t o ng r o w t h r a t e s c a n b e r e a c h e d d e p e n d i n g o l l t h e c o m p o s i t i o no f t h e i n c u b a t i o n m e d i u m . A g r o w t h r a t e o f o n l y 0 .1 5 d - 1 i so b t a i n e d w h e n t h e n a t u r a l p h y t o p l a n k t o n a s s e m b l a g e i si n c u b a t e d w i t h o u t a d d e d n u t r i e n t s . I n c o n t r a s t , i n c u -b a t i o n s o f t h e u n d i l u t e d p h y t o p l a n k t o n w i t h e x c es s n u t r i -en t s y i e ld a me an e s t ima te o f 0 .45 d -1 . Ho we ve r , t he ac tua lg r o w t h r a t e o f a b o u t 0 . 62 8 d - 1 i s a p p r o a c h e d o n l y w h e n i n -c r e a s in g l y m o r e d i l u t e s a m p l e s o f t h e a s s e m b l a g e a r e i n -c u b a t e d ( w i t h o r w i t h o u t e x c es s n u t r i en t s ) . W i t h o u t a d d e dn u t r i e n ts , t h e r e l a t io n s h i p b e t w e e n a p p a r e n t g r o w t h r a t e o fp h y t o p l a n k t o n a n d d i l u t i o n le v e l h a s a n e x a g g e r a t e d n e g a -t i v e s lo p e a n d l e a d s t o a n e r r o n e o u s c a l c u l a t i o n o f t h em a g n i t u d e o f m i c r o - z o o p l a n k t o n g r a z in g . In E x p e r i m e n t 3 ,a n a l y si s o f t h e r e s u lt s o f i n c u b a t io n s w i t h o u t a d d e d n u t r i -en t s y i e lds a n e s t ima te o f 0 .585 d -1 fo r the g raz ing coe f -f i ci e n t, a d a i l y l o s s o f 4 4% o f p h y t o p l a n k t o n b i o m a s s o r8 4% o f n e w p r o d u c t i o n . S i m i l a rl y , t h e 4 d a t a p o i n t s f r o mE x p e r i m e n t 2 t h a t i n v o l v e d i n c u b a t i o n s w i t h o u t a d d i t i o n a l

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M. R. Land ry and R. P. Hassett: Grazing by Micro-zooplankton 287n u t r i e n t s g i v e a m i c r o - z o o p l a n k t o n g r a z i n g i m p a c t( 0 .5 7 9 d - 1) e q u i v a l e n t t o 4 4% o f p h y t o p l a n k t o n s t a n d i n gb i o m a s s o r a b o u t 1 00 % o f p r o d u c t i o n .

In s eawa te r , any d i s s o lved cons t i tuen t e s s en t i a l fo r phy-t o p l a n k t o n g r o w t h ( i . e . , m a c r o n u t r i e n t , m i c r o n u t r i e n t , o rv i t a m i n ) m a y b e c o m e l im i t i n g d u r i n g t h e c o u r s e o f a d i -lu t ion expe r imen t and b ia s the re s u l t . S ince the e s s en t i a lc o m p o n e n t w i l l b e d e p l e t e d m o r e r a p i d l y i n t h e p r e s e n c eo f h i g h e r d e n s i ti e s o f p h y t o p l a n k t o n , t h e n e g a t i v e s l o p e o ft h e r e g r e s s i o n e q u a t i o n ( i n o t h e r w o r d s , t h e e s t i m a t e d c o -e f f i c i en t o f g raz ing ) w i l l be exag ge ra ted . N i t ra t e ap pea rs tob e t h e p r i m a r y l i m i ti n g f a c t o r i n t h e e x p e r i m e n t s r e p o r t e dh e r e , a l th o u g h i n a n o t h e r l o c a t io n , p e r h a p s t h i s w o u l d n o tn e c e s s a r il y b e t h e c a s e ; m o r e i m p o r f a n t l y , a s e c o n d f a c t o rm a y b e c o m e l i m i t i n g a f t e r n i t r a t e i s a d d e d i n e x c e s s . I nr e t r o s p e c t , t h e n u t r i e n t a d d i t i o n s h o u l d i n c l u d e a l l c o m -p o n e n t s n e c e s s a r y f o r u n l i m i t e d p h y t o p l a n k t o n g r o w t h ,e .g . t h e i n g r e d i e n t s o f a c o n v e n t i o n a l g r o w t h m e d i a . A l -t e r n a t i v e l y , t h e e x p e r i m e n t s m a y b e p e r f o r m e d i n d i a l y s i sc o n t a i n e r s f o r a b e t t e r i n d i c a t i o n o f g r o w t h r a t e s o f p h y -t o p l a n k t o n a t a m b i e n t n u t i r e n t l e v el s . T h i s w o u l d p r o b a b l yb e t h e b e s t a p p r o a c h w h e n d e a l i n g w i t h t h e d e l i c a te o r g a n -i s ms f rom o l igo t roph ic oceans , a s the s e o rgan i s ms s eem tob e p o i s o n e d b y n u t r i e n t a d d i t i o n s , e i t h e r f r o m t h e n u t r i -e n t s th e m s e l v e s o r f r o m t r a c e c o n t a m i n a n t s i n t h e n u t r i e n ts tocks (own unp ub l i s h ed re s u l t s) . Whe n e s t im a te s o f theg r o w t h r a t e o f p h y t o p l a n k t o n a r e n o t d e s i r e d , t h e i n c u -b a t i o n s m a y b e p e r f o r m e d i n d ar k n e s s.

T h e r e s u l t s p r e s e n t e d h e r e i n d i c a t e a m i c r o - z o o p l a n k -t o n g r a z i n g i m p a c t i n t h e r a n g e o f 6 t o 2 4% o f p h y -t o p l a n k t o n s t a n d i n g b i o m a s s a n d 1 7 t o 52 % o f p r o d u c t i o np e r d a y i n c o a s t al w a t e r s o f f W a s h i n g t o n . T h e s e e s t i m a t e sa r e s i m i l a r t o t h o s e r e p o r t e d i n o t h e r c o a s t a l a r e a s . F o re x a m p l e , B e e r s a n d S t e w a r t ( 19 7 1 ) w h o m a d e a s s u m p t i o n sa b o u t s i z e - d e p e n d e n t e n e r g e t i c r e q u i r e m e n t s , s u g g e s t e d am i c r o - z o o p l a n k t o n i m p a c t o f 7 to 5 2 % ( a v e r a g e 2 3% ) o fp r i m a r y p r o d u c t i o n i n t h e S o u t h e r n C a l i f o r n i a B i g h t .H e i n b o k e l a n d B e e r s ( 1 9 7 9 ) h a v e s u b s e q u e n t l y i n d i c a t e dt h a t t i n t i n n id s f r o m t h e s a m e a r e a o c c a s i o n a l l y c o n s u m eu p t o 2 0% o f d a i l y p r o d u c t i o n , b u t m o r e t y p i c a l l y a c c o u n tf o r a b o u t 4 % o f p r o d u c t i o n l os s. R i l e y ( 1 9 56 ) s u g g e s te dt h a t m i c r o - z o o p l a n k t o n g r az i ng i n L o n g I s la n d S o u n d m a ya c c o u n t f o r a l o ss o f as m u c h a s 43 % o f a n n u a l p r o d u c t i o nb a s e d o n t h e d i f fe r e n ce b e tw e e n m e a s u r e d p r o d u c t i o n a n do t h e r m e a s u r e d l o s s t e r m s i n t h e p r o d u c t i o n b u d g e t .C a p r i u l o a n d C a r p e n t e r ( 19 8 0) m e a s u r e d m i c r o - z o o p la n k -t o n f e e d i n g e x p e r i m e n t a l l y i n L o n g I s l a n d S o u n d a n df o u n d t h a t m i c r o - z o o p l a n k to n c o n s u m e d u p t o 41 % o f p h y -t o p l a n k t o n s t a n d i n g s t o c k p e r d a y .

A l t h o u g h t h e d i l u t i o n t e c h n i q u e i s o n l y a p p r o p r i a t e f o rd e t e r m i n i n g t h e c o m m u n i t y g r a z in g i m p a c t o f m i c ro - z o o -p l a n k t o n , a r e a s o n a b l e f e e d i n g r a t e f o r a n i n d i v i d u a l m a yb e o b t a i n e d b y d i v i d in g t h e m e a s u r e d g r o u p i m p a c t b y t h en u m b e r o f g ra z e r s i n e a c h e x p e r i m e n t . I f w e a s s u m e , f o re x a m p l e , t h a t a l l m i c r o - z o o p l a n k t o n c o n t r i b u t e e q u a l l y t ot h e c o m m u n i t y g r a z i n g e f f ec t , t h e p e r i n d i v i d u a l c l e a r a n c era te es t im ates are 0 .6, 0 .1 , and 1 .6/~1 h -1 for Ex per im ent s 1 ,2 , and 3 , r e s pec t ive ly . T hes e e s t ima te s a re on the low end

o f f e e d i n g ra t e s f o r ti n t in n i d s r e p o r t e d b y H e i n b o k e l(1978a ) (1 to 5 /~ lh -1 ) in l ab o ra to ry s tud ie s a nd byH e i n b o k e l ( 1 9 7 8 b ) ( 0.6 t o 1 0 # l h - 1) a n d C a p r i u l o a n dCa rpe n te r (1980) (1 to 84 /~1 h -~) in f i e ld s tud ie s . H ow eve r ,v i r t u a l ly n o t h i n g i s k n o w n r e g a r d i n g t h e f e e d i n g r at e s a n db e h a v i o r o f n a k e d c il ia t es , w h i c h w e r e n u m e r i c a l l y d o m i -n a n t i n t h e d i l u t i o n e x p e r i m e n t . I f w e a s s u m e t h a t a l l g r az -i n g in t h e e x p e r i m e n t s w a s d u e t o c o p e p o d n a u p l i i a n d t i n-t inn ids , we ob ta in g raz ing ra t e e s t ima te s pe r ind iv idua l o f3 .5, 5 .4 , and 11.6/~I h -~, wh ich agre e w el l wi th oth er es -t i m a te s . D e s p i t e c o m p a r a b l e n u m b e r s o f n a k e d c i l ia t es ,p r e d o m i n a n t l y o l i g o tr i ch s , i n E x p e r i m e n t s 1 a n d 2 , t h ea m o u n t o f m i c r o - z o o p la n k t o n g r a zi n g w a s m u c h g r e a te r i nE x p e r i m e n t 1. T h e o b s e r v e d g r a z i n g e f f e c t w a s a l s o h i g h e ri n E x p e r i m e n t 3 t h a n 2 , e v e n t h o u g h n a k e d c i li a te s w e r e a no r d e r o f m a g n i t u d e l es s a b u n d a n t i n t h e f o r m e r . S u c h r e-s u l ts s ugges t t he hypo thes i s tha t s ma l l , naked c i l i at e s g razel i t t l e o n t h e d o m i n a n t p h y t o p l a n k t o n t y p e s ( e . g . d i a t o m s )in coas ta l a rea s. Pos s ib ly the i r g rea te s t imp ac t i s on bac te r -i a and mic ro f l age l l a t e s . De ta i l ed s tud ie s on the feed ing o ft h is m o s t n u m e r o u s f r a c t i o n o f t h e m a r i n e m i c r o - z o o p l a n k -t o n w o u l d b e a n i m p o r t a n t n e x t s t e p i n u n d e r s t a n d i n g t h ef e e d i n g r o le o f p e la g i c m i c r o - z o o p l a n k t o n . A n o t h e r a r e an e e d i n g s t u d y i s th e g r a z i n g i m p a c t o f m i c r o - z o o p l a n k t o ni n o l i g o t r o p h i c g y r e s y s t e m s . F r o m e n e r g e t i c c o n s i d e r a -t ions , Bee rs and S tewar t (1971) s ugges ted tha t t he mic ro -z o o p l a n k t o n m i g h t c o n s u m e a b o u t 7 0 % o f p r i m a r y p r o d u c -t ion in o l igo t roph ic reg ions a s oppo s ed to 20% inc o a s ta l a r e as . I t w o u l d b e i n t e r e s ti n g t o a p p l y t h e m e t h o d so f th e p r e s e n t s t u d y i n r e g i o n s o f t h e w o r l d o c e a n w h e r em i c r o - z o o p l a n k t o n h a v e b e e n p r e d i c t e d t o h a v e t h e i rg r e a t es t t r o p h o d y n a m i c i m p a c t .A c k n o w l e d g e m e n t s . W e g r a t e f u l l y a c k n o w l e d g e t h e e f f o r t so f t h e C a p t a i n a n d c r e w o f t h e R . V . " W e c o m a " i n s u p p o r to f t h is r e se a r c h . W e t h a n k M . M . M u l l in , R . W . E p p l e y ,a n d K . B a n s e f o r t h e i r e n c o u r a g e m e n t a n d v a l u a b l e c o m -m e n t s . P a r t i c u l a r th a n k s a r e d u e t o S . M o o r e o f O r e g o nS t a te U n i v e r s i t y , w h o p r o v i d e d a n a l y s es o f o u r n u t r i e n ts a m p le s . O u r w o r k w a s s u p p o r t e d b y D e p a r t m e n t o f E n e r -g y C o n t r a c t D E - A T 0 6 - 7 6 - E V - 7 5 0 2 6 ( D E - E V - 7 5 0 2 6 - 9 1 ).

L i t e r a t u r e C i t e d

Beers, J. R., F. M. H. Reid and G. L. Stewart: Microplankton ofthe No rth P acific Central Gyre. Population structure andabundan ce, June 1973. Int. Revue ges. Hydro biol. 60 , 607-638(1975)Beers, J. R. and G . L. Stewart: Micro-zoo plankton in the e uphoticzone at five locations across the California C urrent. J. Fish. Res.Bd Can. 24, 2053-2068 (1967)Beers, J . R. and G. L. Stewart: Numerical abundance and estimat-ed biomass of micro-zooplankton. In : The ecology of theplankton off La Jolla, California, in the period A pril throughSeptem ber, 1967, Par t VI. Bull. Scripps Instn Oce anogr. (NewSer.) 17, 67 87 (1970)Beers, J. R. and G . L. Stewart: Micro-zooplank ters in the planktoncommunities of the u pper w aters of the eastern tropical Pacific.Deep-Sea Res. 18 , 861-883 (1971)

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D a t e o f f i nal m a nus c r i p t a c c e p t a nc e : J a nua r y 25 , 1982 .C o m m u n i c a t e d b y N . D . H o l l an d , L a J o l l a