Rieper-Kirchner 1990 Algae Decomposition With Laboratory Studies

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HELGOLANDER MEERESUNTERSUCHUNGENHelgol/inder Meeresunters. 44,397-410 (1990)

M a c r o a l g a l d e c o m p o s i t i o n : l a b o r a to r y s tu d i e s w i t h

p a r ti cu l ar r eg a r d t o m i c r o o r g a n i s m s a n d m e i o f a u n a

M. R i e p e r - K i r c h n e r

Biologische Anstalt Helgoland, Meeresstation; D-W-2192 Helgoland, Ger man y

ABSTRACT: The microbial degradation of North Sea macroalgae was studied in laboratory micro-cosms, conta ining autoclaved seawater and a mixture of equal parts of air-dried Delesseria san-guinea, Ulva lactuca, and Laminaria saccharina (red, green and brown algae, respectively}. Todetermine the influence of different organisms on the decomposition rate (expressed in terms ofalgal dry weight loss relative to the material present at time zero) and their development duringdecomposition processes, yeast, flagellates, ciliates, nematodes and a harpacticoid copepod specieswere introduced to the microcosms. Results show that microbial degradation compared to thecontrols was enhanced in the presence of non-axenic nematodes (Monhystera sp.) and protozoans,including bacterivorous cfliates (Euplotes sp. and a Uronema-hke sp.) and flagellates. No enhance-ment occurred with yeast (Debaryomyces hansenii) or with the harpacticoid copepod Tisbe

holothunae. The most rapid algal dry weight loss (78.7 % after 14 d at 18~ occurred with theaddition of raw seawater sampled near benthic algal vegetation and containing only the naturalmicroorganisms present. These consisted mainly of bacteria with different morphological properties,whereby their numbers alone (viable counts) could not be correlated with algal dry weight loss.Although no single dominant species could be determined, lemon yellow pigmented colonies werefrequent ly found. During decomposition in all microcosms the formation of algal particles 40-400 Fmwas observed, which were rapidly colonized by the other organisms present.

INTRODUCTION

During storms large amounts of macroalgae may be uprooted and fragmented by

wave action. In the surf zone algal fragments and particles may accumulate which

support large bacteria populations capable of utihzing algal products such as mannitol,

alginate, cellulose, and agar (Wolter & Rheinheimer, 1977; Rieper-Kirchner, 1989).

Through the activities of bacteria an d fungi, which are the pr imary a gents in deco mposi-

tion and remin eralizat ion processes in aquatic envi ron ment s (Rheinheimer, 1981),

nutrients are rapidly regenerated and mad e available again for the primary producers

(Linley et al., 1981; Lucas et al., 1981; Koop et al., 1982a, b). Diss olve d org ani c com-

pounds may also be converted by bacteria into aggregates, which may in turn be taken

up by larger organisms (Lush & Hynes, 1973; Robertson et al., 1982; Biddanda, 1985;

Musc hen hei m et al., 1989). It is believed that most of the ma crophy te produ ction (over

90 %) in coastal waters of the tempe rate zones is not directly consu med by grazing

herbivores, but goes into the detrital food web (Mann, 1972; Fenc he l & Jo rge nse n, 1977;

Lfining, 1985).

9 Biologische Anstal t Helgoland, Hamburg



3 9 8 M . R i e p e r - K i r c h n e r

A l g a e c a s t u p o n t h e b e a c h m a y b e r a p i d ly c o lo n i z e d a n d c o n s u m e d b y a m p h i p o d s

a n d d i p t e r a n l a r v a e ( G r i f f i t h s & Stenton-Dozey, 1 9 8 1 ; I n g l i s , 1 9 8 9 ) ; l a r g e n u m b e r s o f

m e i o f a u n a l n e m a t o d e s m a y a ls o b e a s s o c i a t e d w i th r o t ti n g a lg a e ( R i e m a n n , 1 9 68 ;

L o r e n z e n e t al ., 1 9 8 7 ; I n g li s , 1 9 89 ; a n d p e t s . o b s .) . T h e o c c u r r e n c e o f m e m b e r s o f a n o t h e r

l a r g e m e i o f a u n a t a x o n , h a r p a c t i c o i d c o p e p o d s , o n f r a g m e n t i n g a l g a e i n t h e s u r f z o n e a n d

i n s e a f o a m h a s a l s o b e e n r e c o r d e d ( R o b e r ts o n & H a n s e n , 1 9 8 2; A r m o n i e s , 1 9 8 9; R i e p e r-

K i r c h n er , 1 9 89 ). A m o n g t h e m e i o f a u n a , o r g a n i s m s 4 2 - 1 0 0 0 b tm i n s iz e ( H i g g i n s & T h i el ,

1 9 88 ), p a r ti c u l a r ly t h e n e m a t o d e s a n d h a r p a c t ic o i d s , a r e k n o w n t o f e e d o n d e t ri tu s ,

microorganisms a n d a ls o p r o t o z o a n s ( s ee R e v i e w s b y H i c k s & C o ul l, 1 9 83 , a n d H e i p e t al .,

1985) .

A l t h o u g h i t h a s b e e n s h o w n t h a t s o m e p r o t o z o a n s m a y f a c il it at e m i c r o b i a l d e c o m -

p o s i t i o n p r o c e s s e s ( J a v o rn i c k ~ ' & P r o k e ~o v f i, 1 9 6 3 ; J o h a n n e s , 1 9 6 5 ; S t r a ~ k r a b o v f i - P r o -

k e ~ o v h & L e g n e r , 1 9 6 6 ; B a r s d a t e e t a l. , 1 9 74 ; H a r r i s o n & M a n n , 1 9 7 5 ; F e n c h e l &H a r r i s o n , 1 9 7 6 ; B r i g g s e t a l. , 19 7 9) , t h e r e h a v e b e e n f e w i n v e s t i g a t i o n s o n t h e i n f l u e n c e

o f s m a l l m e t a z o a n s o n d e c o m p o s i t i o n a n d r e m i n e r a l i z a t io n p r o c e s s e s ( T e n o r e e t al. , 1 9 77 ;

F i n d l a y & T e n o r e , 1 9 8 2 ; R i e p e r - K i r c li n e r , 1 9 89 ). I n t h i s p r e s e n t s t u d y , t h e e f f e c t s o f t h e

p r e s e n c e o f s m a l l m e t a z o a n s a s w e ll a s p r o t o z o a n s a n d m i c r o o rg a n i s m s o n t h e d e c o m p o s -

i ti o n o f N o r t h S e a m a c r o a l g a e h a v e b e e n i n v e s t i g a t e d i n t h e l a b o r a to r y .

M A T E R IA L S A N D M E T H O D S

A l l l a b o r a to r y d e c o m p o s i t i o n e x p e r i m e n t s w e r e p e r f o r m e d w i t h 1 0 0 -m l s c r e w - c a p

b o t tl e s. I n a d d i t i o n t o t h e s e a w a t e r a n d o r g a n i s m s d e s c r i b e d b e l o w , e a c h b o t t le o r

m i c r o c o s m c o n t a i n e d 0 .1 g d r ie d a l g a e m i x t u r e c o n s i s t i n g o f e q u a l p a r t s o f Delesseriasanguinea, Ulva lactuca, a n d Laminaria saccharina { r e d , g r e e n a n d b r o w n a l g a e , r e s p e c -

t iv e ly ). T h e a l g a e w e r e c o l l ec t e d f ro m t h e s u r f z o n e o f ' H e l g o l a n d , r i n s e d b r i e f l y w i t h t a p

w a t e r , a i r - d r i e d a n d c u t i n t o p i e c e s 0 . 2 t o 1 .0 c m l o n g ; t h e p i e c e s w e r e n o t s t e r il i ze d .

T h r e e t y p e s o f e x p e r i m e n t s w e r e p e r f o rm e d :

(1 ) t o e x a m i n e t h e i n f l u e n c e o f d i f fe r e n t o r g a n i s m s o n a l g a l d e c o m p o s i t i o n , e x p r e s s e d i n

t e r m s o f p e r c e n t a l g a l d r y w e i g h t l o s s (r e la t iv e t o th e m a t e r i a l i n t r o d u c e d a t ti m e z e r o )

a t a g i v e n t i m e a n d t e m p e r a t u r e ;

(2 ) t o e x a m i n e t h e i n f l u e n c e o f u n t r e a t e d ( ra w ) a n d t r e a t e d s e a w a t e r o n a l g a l d e c o m p o s i -

t i o n ;

(3 ) t o e x a m i n e t h e i n f l u e n c e o f a h a r p a c t i c o i d c o p e p o d s p e c i e s a d d e d t o t h e m i c r o c o s m s

a f t e r a l g a l d e c o m p o s i t i o n w a s a l r e a d y i n p r o g r e s s .

(1 ) I n t h e f ir st e x p e r im e n t , 5 r e p l i c a te m i c r o c o s m s w e r e p r e p a r e d f o r e a c h t r e a t m e n t .

C o n t r o l s c o n s i s t e d o f t h e a i r - d ri e d a l g a e i n 5 0 m l a g e d seawater, a u t o c l a v e d a n d f i l t e r e d

t h r o u g h a 0 . 4 5 ~tm c e l l u l o s e n i t r a t e m e m b r a n e f i lt e r ( S a rt o r iu s , G 6 t t i n g e n , F R G ) to

r e m o v e p a r t ic u l a te m a t te r . T h e y e a s t a d d e d w a s a p u r e c u l t u re o f t h e c o m m o n N o r t h S e a

s p e c i e s Debaryomyces hansenii ( M e y e r s e t a l . , 1 9 6 7 ) o b t a i n e d f r o m P r o f . D r . W . G u n k e l ,

H e l g o l a n d . T h e y e a s t w a s c u l t i v a t e d o n n u t r i e n t a g a r ( G u n k e l e t a l., 1 9 8 3). A f t e r growth,

t h e y e a s t c e ll s w e r e r e m o v e d f r o m th e a g a r p l a te s , s u s p e n d e d i n a b o u t 1 0 m l s t er il e

s e a w a t e r , a n d a d d e d i n 1 .5 m l a li q u o t s to t h e m i c r o c o s m s . E n u m e r a t i o n o f t h e y e a s t c e l ls

w a s m a d e o n 0 . 4 5 ~tm m e m b r a n e f i l te r s (M e y e r s e t al ., 1 9 6 7) . H e t e r o t r o p h i c m i c r o f l a g e l -

l a te s o r i g i n a t e d f r o m a s u r fa c e s a m p l e o f s e a w a t e r t a k e n f r o m a p i e r a t H e l g o l a n d i n

N o v e m b e r 1 98 8, w h i c h w a s e n r i c h e d w i t h d i l u te d Z o B e l l 2 2 1 6E m e d i u m ( c o n ta i n in g



Macroalgal decomposition 399

pepto ne and yeast extract). After several days incubat ion at 18 ~ in the dark with gent le

agitation, a dense culture of flagellates appeared (method of Dr. K. Poremba, pets.

comm.). Flagellates were enu mera ted with a Petroff-Hausser coun ting chamber; 10 fields

were co unte d at 400• magnification, each field conta ining one large square with a

vol ume of 8 • 10 -~ ml (see Reichardt, 1978). Ciliates an d n ema tod es we re i sola ted from

fresh algal fragments, primarily red algae, collected from the be ach at Helgol and at low

tide in Novemb er 1988. The algal fragments were t ransferred imme diate ly onto cellulose

agar plates (Rieper-Kirchner, 1989), flooded with raw seawater from the sampling site

and incub ate d at 16~ After about 7 d a large numb er of nem ato des (mostly Monflystera

sp.) an d ciliates (a mixt ure of large Euplotes sp. 60 ~tm long , a nd a Uronema-like species

20-30 ~tm long) developed, which were sub sequ entl y used in the exper iments. All

nematodes were counted live with a Pasteur pipette. Ciliates were isolated from the

cellulose-ag ar plates with a Pasteur pipette a nd t ransferred to fresh sterilized seawater.Ciliates were cou nte d as follows: 0.5 to 1.0 ml aliquots of seawa ter con tai nin g ciliates

were fixed with formali n (1 ml 37 % form aldeh yde + samp le + 5 ml sterilized, filtered

seaw ater for grea ter volu me). The fixed sample was imm edi ate ly filtered ontO a 0.45 ~tm

me mb ra ne filter and stained with 2 % erythrosine in a 5 % aqueo us phen ol solution

(Reichardt, 1978, modified). A 1 cm 2 piece of the filter was the n cut out, pl aced on a shde,

rendere d transparent with immersion oil and counted und er a standard Zeiss microscope

at 160-400• magnification. Ten fields per slide were counted, with a maxi mum of 20

ciliates per field. Stai ned ciliates retain their shape and are readily distin guish able from

detritus particles present.

Yeast cells, flagellates, nemat ode s an d ciliates, with a bou t 1.5 to 5 ml of their c ultur e

fluid, were added to 50 ml autoclaved, filtered seawater in each microcosm. The cultureswere not axenic; bacteria adhering to the dried algal particles were also present in all

microcosms. In addition, microcosms were also set up cont aini ng 5 ml raw, u ntr eat ed

(unenriched) seawater sampled November 1988 and 50 ml autoclaved filtered seawater

as above; no other organis ms were added. The bact eria in the microcosms were enu mer -

ated o n ZoBeU 2216E plates after suitable dilution (spread plates); plates wer e inc uba ted

14 d at 20 ~ in the dark.

Exper imenta l conditions: controls and microcosms conta ining yeast, flagellates,

nematod es, cihates, and untrea ted seawater alone were kept 14 d in the dark at 18 ~ All

were c ontinu ously agitated on a table with gentle mov eme nt (50 imp rain -l). The caps on

the bottles were loosely placed to facilitate oxygen ex change . At the end of the experi-

ment, the al gal mate rial was rinsed with distilled water, dried 4 h at 65 ~ an d loss of dry

weight was determined. The organisms were counted and the pH monitored in each

microcosm at the end as at the beg inn ing of the expe riment.

(2) For the second experiment, raw untreated seawater was taken from the pier at

Helgoland (surface water) in January 1989. One aliquot of the sample remained untrea-

ted, an oth er was imm edi ate ly filtered thr oug h a sterile 0.45 ~tm filter, an d a thir d was

autoclaved. From each aliquot, 5 ml were removed and added to 50 ml autoclaved,

filtered seawater with 0.1 g dried algae mixture as above. Five replicates were set up for

each treatment. The durati on and conditions were the same as und er (1).

(3) For the third experiment, adult and late copepodid stages of the harpacticoid

copepod Tisbe holothuriae from the author's stock cultures were used (Rieper, 1978). All

copepods were counted live by means of Pasteur pipettes. For the first part of the



400 M. Rieper -Kirchn er

experiment, 5 ml of raw un trea ted sea water were added to 9 microcosms con tai nin g dried

algae and 50 ml autoclaved seawater as above. The untreat ed seawater originated from

the same sample used in the second experiment described above, but had been stored

over nigh t at 5 ~ before use. The 9 microcosms were kept 21 d at 18 ~ in the da rk with

con tinu ous gent le a gitat ion of 50 imp m in -1. After 21 d, 75 Tisbe individuals were added

to each of 3 microcosms, with about 10 ml culture water. To another 3 microcosms, 10 ml

copepod culture water without the copepods were added; the copep od cultures were not

axenic and contained ciliates as a contaminant (a small Euplotes sp.) and microflagel-

lates. The re mai nin g 3 microcosms received no additio nal organisms.

After another 5 to 6 d under the same conditions, totalling 26-27 d experimental

duration, the study was ended and analyses were performed as with the preceding

experiments.

At the end of every experimental series, all meiofauna organisms were carefullyremoved from the algae by Pasteur pipette under a dissecting microscope. The algae

fragments wer e rinsed with distilled water onto 180 ~tm mesh size nylon gau ze in order to

remove the protozoans as far as possible, before the algal dry weight was determined.

Small particles passing the 180 ~tm gauze could not be s epara ted from the protozoans and

were not considered in the dry weight determinations.

RESULTS

E x p e r i m e n t 1

The results of the first experiment are summarized in Table 1. In microcosms withdried algae alone (controls) with no organisms added except bacteria adhering to the

dried fragments, the mean algal dry weight loss after 14 d was 59.1%. The numbers of

bacteria, expr ess ed as colon y-fo rming units (cfu), inc rea sed from less th an 10 m1-1 at time

zero to an av era ge of 9 x 107 m1-1 in the sea wate r at the en d of the e xpe rim ent . Over 90 %

of the colonies on the plates were pigmented yellow-ochre and appeared morphologi-

cally identical.

Addition of a pure culture of the yeast Debaryomyces hansenii: the concentration of

yeast cells in each replicate after inoculati on at time zero was 4 x l0 s m1-1, and incre ased

after 14 d to a bou t 8.6 x 106 m1-1. Bacteria o rig ina ting from the algal fra gmen ts

dev elop ed after 14 d from less than 10 ml -t to an ave rag e of about 1 x 108 m1-1, wh er eb y

yellow-ochre pigme nted colonies dominated on the plates as above. The mea n algal dry

weight loss after 14 d amou nte d to 57.0 %. No other organ isms were present .

Addition of heterotrophic microflagellates from enriched raw seawater sampled

Nove mber 1988: the initial concent ration of flagellates in the replicate micr ocosms was

abo ut 1 x 105 m1-1 and in cr ea se d after 14 d to a m ea n of 4 x 106 m1-1 (r ang e 1.8 to

5.6 x 106 ml-1). The me an algal dry wei ght loss was 66.2 %. The bacter ia num ber s

pre sen t with the flagellat es at time zero were 2 x 104 cfu m1-1 and in cre as ed after 14 d to

about 3 x 106 m1-1. Non-p igm ent ed colonies domina ted; pi gme nte d colonies were mostly

lemon yellow.

Addition of nematode-cihate mixture: 30 nematodes, primarily Monhystera sp., with

a small nu mb er of mixed cihate species as contam inants , were int rodu ced to the

microcosms at time zero. After 14 d, in 4 of the 5 rephcates there was an increase in the



M a c r o a l g a l d e c o m p o s i t i o n 401

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n u m b e r s o f n e m a t o d e s ( to 2 0 0 - 5 9 5 ); i n o n e r e p l i c a t e t h e r e w a s n o c h a n g e . ( A ll t h e

i n d i v i d u a l n e m a t o d e s w e r e n o t a t t h e s a m e s t a g e o f d e v e l o p m e n t w h e n i n t r o d u c e d t o t h e

m i c r o c o s m s . ) T h e c i l ia t e n u m b e r s (Euplotes a n d Uronema-like s p p .) i n c r e a s e d f ro m

a b o u t 1 7 0 m 1 -1 to 1 4 0 0 - 6 4 0 0 m 1 -1 a f t e r 14 d . ' T h e m i c r o c o s m s w i t h t h e h i g h e s t n u m b e r s o f

n e m a t o d e s h a d t h e f e w e s t c i l i a te s . T h e m e a n a l g a l d r y w e i g h t l o s s a f t e r 1 4 d w a s 7 3 . 1 % .

T h e a v e r a g e n u m b e r s o f b a c t e r i a p r e s e n t r a n g e d f r o m 3.5 x 104 m 1 - 1 a t t i m e z e r o t o

2 .4 • 1 06 m 1 - 1 a f t e r 1 4 d , a n d c o n s i s t e d o f f o r m s w i t h d i f f e r e n t m o r p h o l o g i c a l c h a r a c t e r i s -

t ic s, t h e m a j o r i t y o f w h i c h w e r e n o t p i g m e n t e d .

A d d i t i o n o f c i l i a t e s : a t t i m e z e r o , c il i a te s f ro m t h e n e m a t o d e c u l t u r e s w e r e i n t r o d u c e d

t o t h e m i c r o c o s m s a t a c o n c e n t r a t i o n o f a b o u t 3 0 0 0 c ~ a t e i n d i v i d u a l s m l - I . A f t e r 1 4 d,

d i f fe r e nt ~ i a t e p o p u l a t i o n s d e v e l o p e d i n e a c h r ep h c a t e , th e i r n u m b e r s r a n g i n g f r om

7 x 1 03 t o 5 x 1 04 m 1 - 1 . D i n o f l a g e l l a t e s , n o t d e t e c t e d a t t i m e z e r o , a ls o d e v e l o p e d i n e a c h

r e p l i c a t e a n d a t t a i n e d a n a v e r a g e n u m b e r o f 1 • 1 05 m l - t . D e s p i t e t h e v a r i o u s c i l i a t es p e c i e s a n d d e n s i t i e s w h i c h d e v e l o p e d , t h e b a c t e r i a n u m b e r s a n d f o rm s i n a l l r e p l i c a te s

a f t er 1 4 d w e r e q u i t e u n i f o rm . T h e a v e r a g e n u m b e r w a s 4 • 1 0 ~ m 1 -1 , m o s t o f w h i c h w e r e

l e m o n y e l l o w p i g m e n t e d { 8 7 -9 8 % ) . In i t ia l c o n c e n t r a t i o n s w e r e 3 p o w e r s o f t e n l o w e r .

T h e m e a n a l g a l d r y w e i g h t l o ss a f te r 1 4 d w a s 7 5 .4 % .

A d d i t i o n of r a w u n t r e a t e d s e a w a t e r s a m p l e d N o v e m b e r 1 98 8: T h e i n i ti a l b a c t e r i a

c o u n t s i n t h e r e p h c a t e s w e r e 7 0 0 m l - t . A f t e r 14 d t h e n u m b e r s i n c r e a s e d , b u t a t g r e a t l y

d i f f e r i n g r a te s . T h e f i n a l c o u n t s v a r i e d b e t w e e n 5 • 1 06 m l - t a n d 1 • 1 08 m 1 -1 . T h e s e

l a r g e d i f fe r e n c es w e r e a ls o a c c o m p a n i e d b y v a r i a t i o n s in t h e m o r p h o l o g y o f t h e b a c t e r i a

c o lo n i es : p i g m e n t e d c o lo n ie s , f or e x a m p l e , w h i c h w e r e m o s t l y l e m o n y e l l o w , r a n g e d

f r o m 4 % i n o n e r e p h c a t e t o a s m u c h a s 70 % i n a n o t h e r . H e t e r o t r o p h i c m i c r o f l a g e l l a t e s

d e v e l o p e d i n 2 o f t h e 5 r e p h c a t e s . N o c i h a te s , d i n o f l a g e l l a t e s o r o t h e r o r g a n i s m s w e r eo b s e r v e d . T h e m e a n a l g a l d r y w e i g h t l o ss af t e r 14 d w a s 7 8 .7 % . N o c o r r e l a t i o n w a s

a p p a r e n t b e t w e e n t h e b a c t e r i a co l o n ie s , p r e s e n c e o r a b s e n c e o f f l a g e ll a t e s , a n d a m o u n t

o f a l g a l d r y w e i g h t l o ss , F o r e x a m p l e , i n t h e 2 r e p l i c a t e s w h e r e m i c r o f l a g e l l a t e s w e r e

n u m e r o u s e n o u g h t o b e d e t e r m i n e d w i t h a c o u n t i n g c h a m b e r (6 x l 0 s a n d 7 x 1 05 m l - 1 ) ,

5 . 3 x 1 0 6 a n d 9 . 2 • 1 07 c fu m l - t , r e s p e c t i v e l y , w e r e f o u n d . I n t h e f o r m e r , 7 2 % o f t h e c f u

w e r e y e l l o w p i g m e n t e d , a n d l e s s t h a n 1 0 % i n t h e l at t er .

T h e p H v a l u e s i n a ll m i c r o c o s m s r e m a i n e d s t ab l e , r a n g i n g b e t w e e n 7 .9 6 a n d 8 .2 6

a f t e r 14 d . A l l m i c r o c o s m s w e r e e x a m i n e d m i c r o s c o p i c a l l y a t t h e e n d o f t h e e x p e r i m e n t .

D u r i n g d e c o m p o s i t io n , th e m a c r o a l g a l f r a g m e n t s b e c a m e i n c r e a s i n g l y t r a n s p a r e n t , a n d

t h e e d g e s b e g a n t o d i s i n t eg r a t e . S m a l l p a r t i c le s i n t h e s e a w a t e r w e r e o b s e r v e d , t h e s i ze s

o f w h i c h w e r e m o s t l y b e t w e e n 40---400 ~ tm . T h e s e p a r t i c le s a p p a r e n t l y w e r e a g g r e g a t e s o f

a l g a l m a t e r i a l a n d m i c r o o r g a n i s m s , c i l i a te s , f l a g e l l a t e s a n d a l s o n e m a t o d e s . S m a l l e r

p a r t i c l e s o f a b o u t 2 0 ~tm d o m i n a t e d i n t h e c o n t r o l m i c r o c o s m s a n d t h o s e c o n t a i n i n g y e a s t .


I n t h e s e c o n d e x p e r i m e n t , t h e e f f e ct s o f u n t r e a t e d a n d t r e a t e d s e a w a t e r ( f il t e re d o r

a u t o c la v e d ) o n m a c r o a l g a l d e c o m p o s i t i o n w e r e c o m p a r e d . T h e r e s u l t s a r e p r e s e n t e d i n

T a b l e 2 .

A d d i t i o n o f r a w u n t r e a t e d s e a w a t e r ( c ol le c te d J a n u a r y 1 98 9) : t h e a v e r a g e b a c t e r i a

n u m b e r s a t t i m e z e r o w e r e a b o u t 3 0 0 m 1 -1 a n d i n c r e a s e d a f t e r 14 d t o 1 • 108 m l - 1 ; n o n -

p i g m e n t e d f o r m s d o m i n a t e d . P i g m e n t e d c o lo n i es w e r e y e l l o w o r b r o w n , a n d r a n g e d f ro m




Table 2. Macroalgal degradation in laboratory microcosms after 14 d at 18 ~ inf luence of rawuntreated and treated seawater (sampled Jan. 1989) (Experiment 2; 5 rephcates for each treatment)

Raw untreated 0.45 gainfiltered Autoclaved

% Algal dry wt lossrange 67.3-77.4 59.0-64.5 53.3-56.3{mean} (72.3} {61.9) {55.0}

B a ct e ri a n u m b e r s

after 14 d

c f u x 1 0 6 m l - I

range 52-187 13.3-44 51.5-155(mean} (101) {25.1} {89.8}

Dominant bact mostly yellow yellow-ochre yellow-ochrepopulations on colonies; colonies coloniesagar plates total pigm. 14-100 % 74-100 %after 14 d < 1-28 %

O r g a n i s m s p r e s en t o c c as i o na l n o p r o t o z o a n s n o p r o t o z o a n s

after 14 d flagellates< l0 s m1-1

less than 1% to about 30% of the total numbers. As with untreated seawater from

Nove mber 1988, heterotrophic micro flagellates d evelope d in some but not in all

rephcates; their numbers were too few to be counted accurately with the countingchamber (<105 ml-t}. The mean algal dry weight loss after 14 d was 72.3%. In

compariso n to the microcosms conta inin g seawater samplecl Nove mber 1988, those with

Jan uar y 1989 seawater generally contai ned after 14 d higher nu mbe rs of bacteri a with a

lower percentage of pigmented forms, and the occurrence of microflagellates was

neghgible. The mean algal dry weight loss was lower than for the microcosms with

November seawater (78.7 % as mean value with November seawater). Due to the large

differences in the rephcates conta ining seawater from November, however, a possible

influ ence of the micro flagellates on bacteria n umb ers a nd algal degrada tion could not be

determined.

Addition of 0.45 ~tm-filtered seawater {from January 1989): bacteria counts at time

zero in the microcosms were less tha n 10 m1-1, and i ncr eas ed to 2.5 x 107 m1-1 after 14 d.While the cfu num ber s were similar to the unfiltered samples, a much larger prop ortion of

the forms present was yellow-ochre pigmented, and presumably originated from those

bacteria ad herin g to the dried algal fragments. The me an dry weight loss was 61.9%. No

protozoans developed in any of the rephcates.

Addition of autoclaved seawater (from Jan uary 1989): the bacteria in the microcosms

at time zero were less tha n 10 m1-1. After 14 d, cfu nu mb er s ran ge d from 5 to 15 • 107

m1-1, 74-100 % of which were yellow-ochre pig men ted as above. The me an algal dry

weight loss amo unt ed to 55.0 %. No protozoans develo ped in the microcosms.

The pH values in all replicates of Experiment 2 remained stable between 7.8 and

8.26. Microscopical exa min ati on of the a lgal frag ment s after 14 d reve ale d small particles

40--400 ~tm. The particles in the rephcates with autocl aved seawa ter ten ded to be finer.



404 M. Rieper-Kir chner

The bacteria which developed in the microcosms with fi l tered and autoclaved seawater

we re gen era ll y large (1 btm x 1.8 ~tm, oval) and non- motil e. So me we re coryn efor m. Th e

bacte ria in the untr eated seawater, on the other hand, w ere smaller (about 0.5 ~tm) and

more diverse forms were observed.


In the third experiment, the macroalgal fragments were firs t incubated in raw

unt rea ted seaw ater (from the January 1989 sample) 21 d at 18 ~ After deg rad ati on was

thus already in progress, the harpacticoid copepod T i s b e h o l o t h u r i a e and protozoans

were introduce d to 3 microcosms, 3 other microcosms received the copepo d culture water

with the protozoans but without T i s b e , and 3 microcosms were left unchanged. The

experiment was terminated after another 5 to 6 d under the same conditions. The results

are hsted in Table 3.

Untreated seawater without addition of copepods or copepod culture water: after a

total of 26/27 d (analyses could not be completed on one day) the numbers of bacteria in

the 3 replicates show ed large differences, rang ing from 4.5 to 170 x 106 ml -i . Non-

pigmented colonies dominated. No protozoans could be detected. The mean algal dry

weight loss amounted to 78.4 %. pH values were between 8.08 und 8.26.

Untreated seawater with copepods ( T i s b e h o l o t h u r i a e } added, including T i s b e

culture wate r with ciliates and micr oflagellates: from the 75 copepods in tro duce d to each

microcosm, the numbers remaining after 5 d were 68, 65 and 71, respectively. Ciliates

initially pres ent at a density of less than 100 ml -I were only occasionally obs erve d an d

appar ently did not increase. Th e final concentrations of flagellat es were 2 to 4 x 106 ml -t.

Table 3. Macroalgal degradat ion in laboratory microcosms after 26/27 d at 18 ~ influence oforganisms introduced after 21 d (Experiment 3; 3 replicates for each treatment)

Untreated seawateralone

Untreated seawater+ T i sbe ho lo thur iae

+ ciliates, flagellates

Untreated seawater+ copepod culture water

+ ciliates, flagellates

% Algal dry wt lossrange 74.7-82.0 74.3-83.9 78.3-87.1(mean) (78.4) (80.2) (81.5)

Bacteria numbersafter 26/27 d

cfu x 106 m1-1

range 4.5-170 0.9-5.7 1.0-2.3(mean) (110) (2.5) (1.6)

Dominant bact. non-pigmented non-pigmented diff. pigm ente dpopulat ions on colonies colonies coloniesagar plates 74-94 % 67-97 % 31-74 %after 26/27 d

Organisms present no copepods copepods (T isbe) no copepodsafter 26/27 d no dliate s very few ciliates very few ciliates

no flagellates flag. 2-4 x 106 m1-1 flag. 2-7 x 106 ml -i




The numbe rs of bacter ia were betw een 0.9 and 5.7 x 106 ml -t . Non- pigm ente d colonies

dominated although different yellow and orange forms were not uncommon. The mean

algal dry weight loss of 80.2 % was not much greater than that without copepods and

protozoans. The pH values were between 7.81 and 7.92.

Untreate d sea water with cope pod culture water, cihates and microflagellates: at the

end of this part of the experiment, the numbe rs of ciliates were too few to be enumer ated,

whe rea s the fl agell ates rea che d a density of 2 to 7 • 106 m1-1. The ba cte ria counts ra nge d

from I to 2.3 x 106 ml -I and pig men ted colonies (brown, gold-ochr e, pink) we re fre-

quently observed. The m ean algal dry weight loss was 81.5 %. The pH values were stable

bet we en 8.13 and 8.20. Alg al particle s 40-400 ~m wer e obse rved in all microcosms, as in

the previous experiments.

DISCUSSION

As shown in Table 1, with only air-dried macroalgal fragments pre sent in sterile

seawater, over half the algal dry weight is lost after 14 d, apparently due to initial

leaching processes and the activity of bacteria adhering to the fragments. During this

period high numbers of bacter ia developed, over 90 % of which wer e uniformly yellow-

ochre pigment ed and appare ntly morphologically identical.

Although yeasts have often been reported in the marine environment and may

rapi dly multiply in the pr ese nce of alg ae in th e laborat ory, for exam ple from 103 to 10 s

cells m1-1 w ithin 3 we eks with Desmarestia ~dndis (Gunk el et al., 1983), the addi tion of

the common North Sea yeast Debaryomyces hansenii did not increase the rate of algal

decomposition. Instead, with yeast added, a lower percentage of algal dry weight loss

was note d c ompared to the controls above. It is possible that the ra pid deve lopme nt ofyeast cells in the microcosms to several million ml -1 excee ding values enc ounte red in the

field (maximally 500 cells cm 3 fresh se dime nt a nd less tha n 100 m1-1 in surf wat er with

algal fragments: author's unpubl, data), interfere d with the bac terial activity.

According to results of investigations on macrophyte material by workers such as

Fenchel (I970) and Robertson et al. (1982), who employed the acridine orange direct

counting method for enumeratin g flagellates, the densities of 4 ~m flagellates in the

microcosms in this stud y (10 s to 106 m1-1) may be cons ider ed realistic. Com par ed to the

controls, a higher mean algal dry weight loss and lower numbers of bacteria occurred

(Table 1). Similar results have also bee n r epo rte d by Joh ann es (1965), w ho f ound the

regeneration of dissolved organic phosphate from detritus proceeded faster in the

pres ence of colorless flagel lates 1--4 ~m as well as ciliates. The microbia l deco mposi tionof dead Peridinium (dinoflagellate) cells was also accelerated in the presence of bac-

terivorous 2-10 ~m microfl agellat es (Sherr et al., 1982). On t he ot her hand, Javor nick~ &

Proke~ov~ (1963) show ed tha t while the dev elo pme nt of ciliates and lar ger fla gella tes in

freshwater samples reduce d bacterial numbers and incr eased the oxidation processes,

the pre sence of minute colorless flagellates did not greatly reduce the n umber s of

bacteria or significantly influence the oxygen consumption. The role of microftagellates

in decomposition processes will no doubt dep end not only on the ba cteria an d dissolved

nutrients in a given body of water, but also on the regulatory mechanism of larger

protozoans present.

Indisputable is the stimulation of bacteria l activity report ed for ciliated protozoans

(Bick, 1967; Bar sda te et al., 1974; Briggs et al., 1979; Roge rson & Berger, 1983; Rie per -



406 M. Rieper -Kirch ner

Kirchner, 1989, and the present study). What are the mechanisms of protozoan stimula-

tion of bacterial activity? Protozoan predation reduce s the numbe rs of bact eria a nd may

thus kee p the bac ter ia in an active met abohc state {Javornick~ & Proke~ov~, 1963}. It has

also bee n s ugge sted that protozoans releas e metabohtes into the en vironme nt which are

util ized by bact er ia {Stra~krabov~-Proke~ov~ & Legner , 1966; Legne r, 1973}. Prot ozoan

stimulation of bacterial activity could also be due to the release of nutrients from the

bacterial cells themselves, which are preyed upon (Huang et al,, 1981; Taylor et al.,

1985).

Similar mechanism s may also apply to bacterial stimulation in the pres ence of small

metazoans, although in this respect data is sparse. Over 25 years ago, Javornick~ &

Proke~ova (1963) sugges ted that "Higher zooplankton may decr ease bac teria l numbers

and thus sti mulate the oxidation process in a similar way to Protozoa". This is support ed

by the findings of Tenore et al. (1977), F indl ay & Tenore (1982) and Riepe r-Ki rchne r(1989) with various species of free-hyin g nematodes. In the pres ent study, the n emat odes

in the decomposition experiments were introduced with their accompanying ciliates,

since laboratory stock cultures of nematodes ap peare d less robust und dege ner ated more

rapidly than those with bacterivorous cihates present. The mea n algal dry weig ht loss,

however, was greater with higher numbers of mixed ciliate species without the

nemat odes (Table 1). Possibly the ciliates and n ematod es wer e competi ng for nutrients in

the small closed systems (Stenson, 1984).

Although these results appear to demonstrate an enhancement of bacterial activity

due to the presence of protozoans and nematodes, unexpectedly the highest algal dry

wei ght losses were found with raw se awa ter a lone ( Tables 1 and 2). 78.7 % with the

samp le from Nov emb er 1988 and 72.3 % from the sa me site take n Jan uar y 1989. Filter ingthrough a 0.45 ~m memb rane filter remove d much of the sa mple 's effect on algal dry

weight loss, and autoclaving the seawater reduced the weight loss to 55.0%. The

different results from the November an d Januar y sea wate r samples may be due to

seasonal variations in the microorganisms prese nt which are active in algal decomposi -

tion (Rieper-Kirchner, 1989). Although during the 14-d experiments some flagellates

devel oped in several rephcates, their presence could not be corr elated with the algal dry

weight losses in these microcosms. Large differences in the numbers of bacteria (cfu) as

well as in the proportion of pigm ente d colonies were found which could not be correlated

with either algal dry weight loss or presence of flagellates. The organisms primarily

responsible for the algal decomposition in this experimental series are presumably

bact eri a from raw sea wat er which do not pass a 0.45 ~tm filter due to a lar ger cell size or to

the formation of filaments or extracellular shme. These are appar entl y mixed populations

of opportunists including the lemon yellow forms observed, which are able to r eplace the

large yellow- ochre forms originally adheri ng to the drie d algal fragments. These bacteri a

should have bee n pr esent in the f lagell ate-e nriche d microcosms (Table 1), since the

flagellates were cultivated in raw sea wate r from the same samp hng site. Did the process

of enrichment put the actively degrading bacteria at a disadvantage? If these bacteria

were outcomp eted or ingested by the microflagellates, then the decomposition may have

been actually imped ed rather than enhanced by these protozoans. Was the spread plate

method suitable for enumeration of bacteria in these studies? Although higher bacteria

numbers may be obt ained with direct counting methods, the sapr ophytes which develop

on 2216E medi um are primarily those which are actively involved in the decomposition of




easily decomposable organic matter such as protein and carbohydrates (Rheinheimer,

1984). When bacteria numbers from a stranded M a c r o c y s t i s kelp bed were compared

using acridine orange direct counts and viable cell counts in 2216E medium (MPN, most

probable numbers), Bouvy et al. (1986) found the ratio of direct counts to viable counts

rea che d values close to 1. Similarly, Corre et al. (1989) found good a gre eme nt for bacteri a

counts on Lam/nar/a digi ta ta debris determined with scanning electron microscopy and

2216E plate counts. This suggests that the discrepancy between direct and viable counts

may be n eghgible when a sufficient nutrient supply is available. A complete agr eeme nt

with direct and viable counts, however, is unlikely, due to the occurrence of inactive

bacteria cells.

In this present study no attempt was made to identify taxonomically the bacterial

colonies which developed during algal decomposition. Numerous investigations on

bacteria associated with macroalgae indicate that the genera V i b n o , P s e u d o m o n a s ,F l a v o b a c t e r i u m , and L e u c o t h r i x are frequently represented; yellow ("flavobacteria") a nd

brow n pigmen ted forms frequentl y occur (Chan & McManus, 1969; Laycock, 1974;

Cundell et al., 1977; Hollohan et al., 1986; Bohnches et al., 1988; Corre et ai., 1989).

With regard to the meiofauna, next to nematodes harpacticoid copepods are the most

abu nda nt in sedimen t biotopes as well as in the phyta l (Coull, 1988). Althou gh a few

species of harpacticoids may feed directly on macroalgal tissue, detritus and the associ-

ated microbiota is considered one of their major food sources (Hicks & Coull, 1983; Mey er

& Bell, 1989). Specific strains of bacteria may also be preferred (Rieper, 1982). Recently,

harpacticoids have been reported in sea foam, where they may feed on microorganisms

or on other organic components of the foam itself (Armonies, 1989). Some data indicate

that meiofauna, in particular nematodes and possibly also harpacticoids, play a role inmaki ng detritus available to macrof auna (Tenore et al., 1977). Preliminary investigati ons

on the rote of harpacticoids in algal decomposition indicate that, at least in closed

systems, these organisms do not survive initial degradation processes (Rieper-Kirchner,

1989), due perhaps to harmful algal leachates, bacterial metabohc products or oxygen

deficit. In the present study (part of Experiment 3), T i s b e h o l o t h u r i a e introduced to

microcosms after degrada tion had been in progress for 3 weeks were able to survive, but

their effect on algal dry weight loss was neghgible (Table 3). A shght stimulatory effect

may have be en due to the presence of the contaminant protozoans in the cop epod culture

water. This apparent lack of influence by T i s b e compared to that of the nematodes was

unexpected, considering the role of detritus and microorganisms in the natural diet of

harpacticoids. In other studies, the harpacticoid copepods T . h o l o t h u r i a e and P a r a m -p h i a s c e l l a v a r a r e n s i s readily consumed bacterial aggregates produced in the laboratory

by bacterial growth on dissolved organic matter derived from macroalgae (method of

Biddanda, 1985), as evidenced by the large numbers of fecal pellets produced (Rieper-

Kirchner et al., in prep.). The extent to which the bacteria are digested has not been

determined, although these harpacticoid species are able to survive in the labora tory on a

diet of bacteria a lone (Rieper, 1978).

The results of the present study may be summarized as follows:

(1) Decomposit ion rates of North Sea macroa lgae were studied in labora tory microcosms.

The me an amounts of algal dry weight loss after 14 d at 18 ~ range d from 55 to 80 %,

and are comparable to those found for North Sea algae in the field (Rieper-Kirchner,

1989).




(2 ) T h e a d d i t i o n o f y e a s t d i d n o t i n c r e a s e t h e a l g a l d e c o m p o s i t i o n r a t e .

(3 ) T h e p r e s e n c e o f p r o t o z o a n s ( b a c t e r i v o r o u s c i h a t e s , f l a g e l l a t e s ) m a y e n h a n c e m i c r o -

b i a l d e c o m p o s i t i o n p r o c e s s e s , d e p e n d i n g o n t h e p o p u l a t i o n s o f b a c t e r i a o r i g i n a l l y

p r e s e n t i n t h e i n o c u l u m .

(4 ) M e i o f a u n a l o r g a n i s m s s u c h a s n e m a t o d e s m a y a l s o f a c i l i ta t e b a c t e r i a l d e c o m p o s i -

t io n ; t h e i n f l u e n c e o f t h e h a r p a c t i c o i d c o p e p o d T i s b e h o l o t h u r i a e , o n t h e o t h e r h a n d ,

c o u l d n o t b e d e m o n s t r a t e d .

(5 ) P r i m a r y a g e n t s i n t h e m a c r o a l g a l d e c o m p o s i t i o n a r e m i x e d s p e c i e s o f o p p o r t u n i s t i c

b a c t e r i a o c c u r r i n g i n n a t u r a l s e a w a t e r , l a r g e r t h a n 0 . 4 5 btm , a n d f r e q u e n t l y y e l l o w

p i g m e n t e d .

(6 ) I n a l l m i c r o c o s m s d u r i n g t h e d e g r a d a t i o n e x p e r i m e n t s , t h e f o r m a t i o n o f a l g a l p a r t i c -

l e s 4 0 - 4 0 0 ~ m w a s o b s e r v e d , w h i c h w e r e r a p i d l y c o l o n i z e d b y t h e o t h e r o r g a n i s m s

p r e s e n t . T h e s e e n r i c h e d p a r t i c l e s m a y c o n s t i t u t e f o o d f o r m a c r o c o n s u m e r s i n t h em a r i n e e n v i r o n m e n t .

L I T E R A T U R E C I T E D

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3 0 5 - 3 0 9 .

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3 4 5 - 3 5 7 .

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d e g r a d a t i o n p r o c e s s o f s u b a n t a r c t i c k e l p b e d s (Macrocys t i s pyr i f era ) . - P o l a r B i o l. 5, 2 4 9 - 2 5 3 .

B r i g g s , K . B ,, T e n o r e , K . R . & H a n s o n , R . B ., 1 9 7 9 . T h e r o l e o f m i c r o f a u n a i n d e t r i t a l u t i l i z a t i o n b y t h e

p o l y c h a e t e , N e r e i s s u c c i n e a ( F r e y a n d L e u c k a r t ) . - J . e x p . m a r . B i o l . E c o l . 3 6 , 2 2 5 - 2 3 4 .

C h a n , E . C . S . & M c M a n u s . E . A . , 1 9 69 . D i s t r i b u t i o n , c h a r a c t e r i z a t i o n , a n d n u t r i t i o n o f m a r i n e

m i c r o o r g a n i s m s f r o m t h e a l g a e P o l y s i p h o n i a l a n o s a a n d A s c o p h y l l u m n o d o s u m . - C a n . J .

M i c r o b i o l . 15 , 4 0 9 - -4 2 0 .

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Rieper-Kirchner 1990 Algae Decomposition With Laboratory Studies