HELGOL,~,IDER MEERESUNTERSUCHUNGEN Helgolfinder M e e r e s u n t e r s u c h u n g e n 35, 47-63 (1982)

O n t h e b i o l o g y a n d f o o d of s m a l l - s i z e d fish f r o m N o r t h a n d Baltic S e a areas. IV. I n v e s t i g a t i o n s o n a n e u l i t t o r a l m u d flat at Sylt Island C Dieter Z a n d e r & Eike Hartwig Zoologisches Institut und Zoologisches Museum; Martin-Luther-King-Platz 3, D-2000 Hamburg I3, Federal Republic of Germany

ABSTRACT: The fish fauna of a n eulittoral m u d flat was investigated at Sylt Island (North Sea) with special regard to its food uptake. During the course of a year the following species were caught: Pomatoschistus microps, Anguilla anguilla (elvers), Zoarces viviparus, a n d Gasterosteus aculeatus. Considering the potentially available food, the most a b u n d a n t organisms of the benthos were harpacticoids a n d nematodes, w h e r e a s in the phytal layer gastropods a n d gammarids were dominant. The b e n t h i c biomass was found to b e greatest in spring, while phytal organisms were most a b u n d a n t in late summer. The greatest fish density was stated in September 1974 though only P. microps was present. The fish biomass was highest in spring w h e n the elvers appeared. The m a i n food of P. microps was epibenthos; in the diet of A. anguilla phytal organisms dominated over epibenthos, in G. aculeatus s u p r a b e n t h i c organisms were also present. The most prominent food c o m p o n e n t by biomass was g a m m a r i d s in all investigated fish, whereas harpacticoids were only d o m i n a n t in number. During the course of the year the biomass of ingested food yielded highest values in s u m m e r a n d autumn, but lowest in winter. A very great predatory activity was found i n S e p t e m b e r 1974, w h i c h possibly c a u s e d a grazing effect on harpacticoids. An estimation of the turnover rate of small-sized fish in this m o n t h led to a value of 70 m g dry w e i g h t m -2 - d -1.

INTRODUCTION Marine mud fiats are ecosystems which are characterized by high productivities. T h e i r i m p o r t a n c e a s n u r s e r i e s for c o m m e r c i a l f i s h a n d h a b i t a t s for s m a l l - s i z e d f i s h is generally acknowledged. They are extreme biotopes which are strongly affected by the t i d e s . D u r i n g l o w t i d e t h e o r g a n i s m s a r e e x p o s e d to t h e i n f l u e n c e of a i r t e m p e r a t u r e , c h a n g i n g w a t e r l e v e l s a n d , i n c a s e of r a i n or s o l a r r a d i a t i o n , to s t r o n g l y c h a n g i n g salinities in the remaining mud puddles. These climatic conditions favour the existence of a v e r y s p e c i a l i z e d f a u n a a n d f l o r a w h i c h is r e l a t i v e l y p o o r i n s p e c i e s b u t r i c h i n individuals. Y o u n g a n d s m a l l - s i z e d f i s h p l a y a r o l e i n t h e t u r n o v e r r a t e of m u d fiats s i n c e t h e y a r e u s e d a s f o o d b y p r e d a t o r y f i s h a n d b i r d s . T h e r e f o r e , it is t h e a i m of t h i s i n v e s t i g a t i o n to a s s e s s t h e i m p o r t a n c e of s m a l l - s i z e d f i s h as l i n k s i n t h e f o o d w e b of a m a r i n e m u d flat. T h e u p p e r e u l i t t o r a l z o n e of t h e K e i t u m m u d f l a t o n Sylt I s l a n d ( F e d e r a l R e p u b l i c of G e r m a n y , N o r t h F r i e s i a n coast) a p p e a r e d w e l l s u i t e d for s t u d i e s of t h i s t y p e . I n p r e v i o u s © Biologische Anstalt Helgoland

0174-3597/82/0035/0047/$ 02.00

48

C. Dieter Z a n d e r & Eike Hartwig

papers (Zander, 1979a, 1979b; H e n n i g & Zander, 1981) only the total b i o m a s s i n g e s t e d b y the caught fish was calculated; here the density of fish per u n i t area could b e counted. This method gave a better estimate of productivity a n d turnover rate i n m u d fiats. MATERIAL AND METHODS The samples were t a k e n every two m o n t h s b e g i n n i n g i n May 1974. O n e earlier s a m p l e from May 1973 was i n c l u d e d for comparison i n this analysis. The small-sized fish were caught with the aid of a square "frame" that h a d single walls of plexiglass (Fig. 1), At first it e n c o m p a s s e d a n area of 1 m s b u t this frame proved to b e too unwieldy. Later on, the walls were shortened to 0.71 m y i e l d i n g a n area of 0.5 m 2 .

The frame was s u n k r o u g h l y 10 cm into t h e m u d flat. Afterwards the area was e m p t i e d of water, d r a w i n g it out b y m e a n s of a pail, a n d p o u r i n g it t h r o u g h a h a n d - n e t . Thus the yield of s m a l l - s i z e d fish could b e quantified. After d r a i n i n g the interior of the frame the r e m a i n i n g fish were collected from the bottom a n d fixed i n 4 % formalin.

Fig. 1. Plexiglass frame for quantitative sampling of small-sized fish, comprising an area of 0.5 m2

Phytal samples, p u t into plastic b a g s u n d e r water, were fixed i n 4 % formalin. The m a i n species was F u c u s s e r r a t u s with v o l u m e s b e t w e e n 66 a n d 295 cm 3. Benthos was s a m p l e d b y m e a n s of a plexiglass frame (10 cm edge length; 0.01 m 2 s a m p l i n g area) from a s e d i m e n t depth of 1 cm (cf. Giere, 1973). Finally, the 100 cm 3 s a m p l e s were fixed i n 4 % formalin. Since no p a r a l l e l s a m p l e s were taken, statistical calculations could not b e made. In the fishes sampled, body l e n g t h a n d formalin wet w e i g h t w e r e d e t e r m i n e d . For analysis of the i n g e s t e d food, the guts were dissected a n d w e t w e i g h t of the contents determined. The relation of gut content to fish wet w e i g h t s y i e l d e d the fullness i n d e x (Hureau, 1969). The single c o m p o n e n t s were c o u n t e d a n d classified according to taxonomical or ecological units; a l g a e a n d detritus w e r e c o u n t e d i n r e l a t i o n to w i d t h of

Biology and food of small-sized fish

49

the mouth of the respective fish (Zander, 1979a, 1979b). The calculation of abundance, frequency, and ingested biomass was described earlier (Zander, 1979b). The fauna of the phytal samples were grouped according to taxonomic units, counted, dried at 60 °C until w e i g h t constancy, and w e i g h e d on a microscale. Dry weights of molluscs without shells were determined as follows: In the case of large bivalves and gastropods the soft b o d y was separated from the shell and dry weighed; in the case of small molluscs, e.g. Hydrobia, the entire bodies were dry weighed, then m a d e ash free (6 h at 540 °C) and w e i g h e d again; the difference of both figures y i e l d e d the dry w e i g h t of the soft body. The benthal sample~ were stained with bengal-rose, s u s p e n d e d in a fluid containing water and phenole, and the fauna separated. Using three sieves, the following size groups were distinguished: > 400 ~m, 150--400 ~m, and < 150 ~m. The single components were counted and dry weight determined (see above). Only for foraminifers were the known dry weights of Ankar & Elmgren (1976) used. Sieving of meiofauna y i e l d e d only an approach to size groups since not all organisms r e m a i n e d extended after fixing in formalin. All a b u n d a n c e and biomass values refer to an area of 1 m 2. BIOTOPE The investigation site was previously described by Giere (1970) in his examinations of the meiofauna. The site was in the u p p e r eulittoral zone at the e n d of a b r e a k w a t e r and was roughly 4 hours without water cover at low tide. The bottom consisted mainly of silt with a thin sand layer; occasionally small stones were present which m a d e a slight overgrowth with Pucus serratus possible. At places with thick sand layers Zostera was present. At low tide many pools of up to 10 cm depth r e m a i n e d in the m u d flat. The range of water temperatures during the sampling days was 6 °C in January to 16 °C in September. Fluctuations of 6 °C after strong solar radiation were possible during a day. Salinity was b e t w e e n 23 a n d 28 %0; in cases where the shallow pools h e a t e d up, these values increased by 5 %0 S. On July 15th 1974 heavy rainfall caused a lowering of salinity to below 20 %0. ABUNDANCE AND BIOMASS OF POTENTIAL FOOD ORGANISMS The analysis of benthos and of phytal samples shows a high diversity of potential food organisms. The numbers of endo- and epifauna were greatest in April 1975 and lowest in S e p t e m b e r 1974 (Fig. 2). Harpacticoids and nematodes were always present, ranging b e t w e e n 72 and 93 % of total abundance. Whereas harpacticoids dominated in Sept e m b e r a n d November 1974, n e m a t o d e s had the greatest proportions in the other months. M e d i u m - s i z e d nematodes r e a c h e d 75 % in January and April 1975, at other times small individuals dominated (Fig. 3). The population density of harpacticoids was high in November 1974 and April 1975, but low in S e p t e m b e r 1974, in spite of constituting 54 % of the total benthos (Fig. 2). Similar to the situation in nematodes, the medium-sized harpacticoids dominated in January and April 1975, but at other times the small ones p r e v a i l e d (disregarding nauplii) (Fig. 4).

50

C. D i e t e r Z a n d e r & E i k e Hart-wig

Nov,19th1974 (333400)

Sept., 24th1974 (27700}

Harpacticoideo Polychaeta~ Gastro~richo 0slracodo

Nemotoda Nematode

Jan., 17th 1975 (283100)

Aug.,12 th 1975 (335600)

Ap~,lSt 1975

Nematode

Others

Foraminifera

Gestrc

Fig. 2. Proportions of benthos organisms in relation to density. In parentheses: Total numbers of individuals m -2

8o ~° N e m a t o d a

8o °% H a r p a c t i c o i d e a

70.

70-

5O2

50 -

40 -

40 -

30 -

30-

20-

20 -

100

10I

123 123 ~ 123 24,9. 19.11. [ 17.1. 1974

t23 1.4. 1975

123 t2.8.

0

123 24.9.

123 1 1 2 3 I9.1t. I 17~I. 1974

123 1.4. 1975

123 12.8.

Fig. 3 (left). Size distribution of nematodes in the benthos samples. 1: > 400 ~m, 2:400-150 ~tm, 3: < 150 ~ n Fig. 4 (right). Size distribution of harpacticoids in the benthos samples. 1: > 400 ~m, 2:400-150 ~m, 3: < 150 ~tm

Biology a n d food of small-sized fish Sept.24th 1974 (95.6) - ° °

51

Nov,19th 197/, (390)

~ i Gost~oiric

~rpocli¢oide°

OstI~cOd~ For-amLqlfe,ra~

oi~haeJa Gestro{l'iche ~urbeliaria

Jan.,17th1975

(132&9)

Ap~.l st 1975

Aug,12 th 1975

(40983)

{23583)

O~hers

Poiychaeta

Forom{n{~ero Foraminifera

Fig. 5. Proportions of benthos organisms in relation to biomass. In parentheses: Total biomass (rag DW m-2)

A m o n g the r e m a i n i n g c o m p o n e n t s foraminifers were the most a b u n d a n t group with proportions b e t w e e n 1 a n d 17 % (September 1974) (Fig. 2). Polychaetes were most prevalent, 8 %, i n April 1975, w h e n total a b u n d a n c e was greatest (Fig. 2); 83 % of this group were larger t h a n 400 ~m. Other b e n t h o s organisms - ostracods, turbellarians, gastrotrichs - as well as single m a c r o f a u n a c o m p o n e n t s - eggs, diverse larvae - play only a m i n o r role a n d therefore are s u m m a r i z e d as "rest fauna". Variation i n total biomass of b e n t h o s corresponds to the variation i n a b u n d a n c e : Lowest v a l u e s i n S e p t e m b e r 1974 a n d h i g h e s t values of a b o u t 4 g m -2 i n April 1975 (Fig. 5). T h e proportion of n e m a t o d e s was h i g h e s t i n S e p t e m b e r 1974 (34 %), w h e r e a s harpacticoids d o m i n a t e d i n N o v e m b e r 1974 (36 %) (Fig. 5). I n d i v i d u a l s of more t h a n 400 tzm size c o n t r i b u t e d a n i m p o r t a n t part of biomass, a m o n g polychaetes as w e l l as a m o n g the rest f a u n a (Fig. 5). The total n u m b e r s of organisms from the phytal s a m p l e s fluctuated strongly s h o w i n g a m i n i m u m i n M a y 1975 a n d a m a x i m u m i n A u g u s t 1975 (Fig. 6). The most p r o m i n e n t c o m p o n e n t i n n u m b e r were gastropods consisting m a i n l y of L i t t o r i n a l i t t o r e a a n d H y d r o b i a sp. Their densities decreased c o n t i n u o u s l y from May 1974 to April 1975, b u t h a d the h i g h e s t v a l u e s i n A u g u s t 1975 (Fig. 6). The proportion of b i v a l v e s - m a i n l y M y t i l u s e d u f i s - was only worth m e n t i o n i n g i n S e p t e m b e r 1974 with 12 % of the total fauna. In M a y 1975 g a m m a r i d s (30 %) a n d J a e r a a l b i f r o n s (34 %) dominated, w h e r e a s i n April 1975 I d o t h e a sp. was the most a b u n d a n t species (28 %). The isopods showed the highest densities i n April a n d May 1975. Decapods - m a i n l y C a r c i n u s m a e n a s - m i g h t be i m p o r t a n t only i n summer, as i n d i c a t e d b y h i g h densities a n d proportions of 8 % (July

52

C. Dieter Zander & Eike Hartwig Mey,16th 1974 (1426)

J~a

c~trc=o~

July,t5th1974 (994)

SepL 24th 197& (905)

Jan..17th 1975 (470)

Coelenlerala

~motodo

t POlyChaeta t 0s~racodQ

Oligocheeta Nemotoda

Bivolvia

Ap~,I st 1975 (1504)

Bivalvia I~:'olychaet o

Jaero

Aug.,12th 1975 (2522)

May,29th1975 (332)

Bivelvio PlacophorQ

oce~

Polychoeta

Coelentera@3

C

Fig. 6. Proportions of phytal organisms in relation to denstiy. In parentheses: Total numbers of individuals m-2 1974) and 14 % (August 1975). The very vagile mysids were only notable in July 1974 {19 %). Single meiofauna components occasionally reached relatively high proportions, e.g. nematodes in May 1974 (15 %) or harpacticoids in April 1975 (21%) (Pig. 6}. The total biomass of the phytal-dwelling fauna rose from May to September 1974, reaching 47 g m -2, and declined thereafter until May 1975; in August 1975, again, a very high value of 33 g in-2 was found (Fig. 7A). In this calculation molluscs dominated to a degree of 89 to 99 %, gastropods alone maximally reached 94 %. Only in September 1974, when total biomass was greatest, did the bivalves surpass the gastropods (Fig. 7A). Using this kind of differentiation decapods achieved at most only 6 %, whereas all other groups only appeared in April and May 1975. Therefore, these organisms were treated separately (Fig. 7B). Then, gammarids usually constituted the greatest proportion, which was highest in May 1975 at 94 %. Idothea sp. was present in considerable amounts, to a degree of 90 % in April 1975. In May 1974 otigochaetes (31%) and coelenterates (43 %) had some importance, as well as in September 1974 nemertines (19 %) and polychaetes (14 %). Meiofauna played, as expected, no role regarding biomass (Pig. 7B). ABUNDANCE AND BIOMASS OF FISH The fish species caught - the common goby Pomatoschistus microps (Kroyer), the eel Anguilla anguilla L., the eelpout Zoarces viviparus (L.), and the threespined stickleback Gasterosteus aculeatus L. - showed the greatest abundance in September 1974 and lowest values in July 1974 and May 1975. In May 1974 only elvers of A. anguilla appeared, whereas the greatest density of fish colonization in September 1974 was caused only by P. microps.

B i o l o g y a n d f o o d of s m a l l - s i z e d f i s h A

Nay~16th 197/. ( 7113.0)

Oh te (23./*)

~

Copepoda A

Sept,2/. th 197/. (/.6736.7)

July,15th 1974 (151/.7.0)

Oh ters B

Nemotoda

C o O m tso cd ap~epoda

Oligochaela

(2/.5. 8]

Nemootda

Jan.,17th 1975 (12362./.)

~

Apr.,1st 1975 (/.5076)

(11701 tP ~oyer~ tchQe~o (634.7)

Nemaotdo Poylchaeo t

Turbel~ria

oe

(3 83. 8)

Noepr~ toddo C ecpo a O s r a t Joe~eoda

Jaera Nay, 29 th 1975 (1106.9)

other) B

53

Aug.,12th1975 (33141.0)

Gostropodo / Plocophom

CoeelnetraQ t ( 1175 )

Coeelnetmot

Fig. 7. Proportions of phytaI organisms in relation to biomass. In parentheses: Total biomass (rag DW m-2). Row A includes all components found, row B disregards molluscs

54

C. Dieter Z a n d e r & t!ike H a r t w i g mg(VVW)/rn2 0.~ tow fish

ooo

/

50001 4000- I

30o01

/

2000 i 1000

t

/~micr~s ~ ' - .

197/,Apdl

July

0kt

Jan.

Apff~ 1975

Fig. 8. Biomass of small-sized fish during the investigation time. Interrupted line: Pomatoschistus microps only

Noy73

15

a @

July 74

', W..L~L

Sept 7/,

:

Nov, 7/,

a

5

~Tt-n

14

. •

~

16 10

Jan, 75 April 75 i'

:

rlrh

o

~o

May 73

do

do

I

17

Lo [--

range July 74 t ~ Sept.7/*

I

I

['-~--

1

i

Nov, 7/* ~ Jan. 75

,~4-rl~

,

April 75

~

:

i .............

0

,

,.

D

100 200 360 /*00 500 600 700 800 mgWw

Fig. 9. Variability of size (above) and wet weight (below) of the caught Pomatoschistus microps. Right: Number of specimens. Explanation: x = mean value, m = mean error, s = standard deviation The respective v a l u e s of biomass (wet weight) m a k e these results clearer (Fig. 8). T h e total b i o m a s s w a s h i g h i n s p r i n g a n d d e c l i n e d slowly towards s u m m e r b u t steeply i n a u t u m n a n d e s p e c i a l l y i n winter. In the following spring, 1975, rest p o p u l a t i o n s of gobies w e r e present, w h i c h d i s a p p e a r e d i n M a y 1975 a n d w e r e r e p l a c e d b y elvers. Only for gobies were r o u g h s t a t e m e n t s o n the p o p u l a t i o n structure possible (Fig. 9). T h e catch of J u l y 1974 comprised j u v e n i l e s w h i c h h a d a p p a r e n t l y h a t c h e d at the b e g i n n i n g of the s p a w n i n g period i n May. After r e p r o d u c t i o n h a d f i n i s h e d i n September, y o u n g i n d i v i d u a l s as well as y e a r l i n g s were found, as the g r a p h of size variability indicates (Fig, 9). From N o v e m b e r to April 1975, a c o n t i n u a l d e c l i n e of m e a n size a n d w e i g h t was observed, w h i c h m a y lie i n the c o n t i n u o u s d y i n g off of the oldest individuals. D u r i n g the first i n v e s t i g a t i o n of the area i n May 1973, y e a r l i n g s of P. microps were also

Biology a n d food of s m a l l - s i z e d fish

55

caught; h o w e v e r , t h e s e w e r e a b s e n t in the s a m e m o n t h s of t h e y e a r s 1974 a n d 1975 (Fig. 9). F O O D INGESTED BY THE F I S H

Fullness of guts T h e c a l c u l a t i o n of fullness i n d i c e s (Hureau, 1969) of the P. m i c r o p s catches y i e l d e d h i g h v a l u e s in summer, w h i c h d e c l i n e d to n o r m a l o n e s (about 1) from a u t u m n to w i n t e r (Fig. 10). A g a i n , an i n c r e a s e w a s f o u n d in A p r i l 1975 (Fig. 10). Nay 73 p [

~

i

P micrqp_s

July 7z~ ,i: "

Sept.74

i

I iiilI-

L_L.J

;

I

Nov 74 Jan, 75 April75

,

i

LJ_J.,

I

.......

I

i

0 A. a.__.~nguill_.~a

M~ 741.....

],,, I

~

......

Fig. 10. Variability of fullness indices of the investigated Pomatoschistus microps and Anguilla anguilla. Further explanations see Fig. 9

Nay 1973 50% I

C~rnn~e H~c~c~c CL~macea

Sept.1974

July 1974. 100% 50% I

100% s

•

50% !

P

Nov.1974 100% 50% !

Jan.1975

100%

J

!

!

J

I0~ I

t

]

I

.......l

April 1975 50%

50% 100% !

]

Crangon 3 Cypr;s-Lar',,,ae] Pdychae'b Turbelloria F~sh eggs Detritus Others Algae

-7 ]

t

-1 -'1

!

3

" '.'|

I

I

,t

I

1

] -q

Fig. l l . Frequency of occurrence of food organisms in Pomatoschistus microps during the investigation time A m o n g eels, o n l y the catch of M a y 1974 w a s a n a l y z e d ; the fish s h o w e d h i g h d e g r e e s of v a r i a b i l i t y a n d a h i g h p r o p o r t i o n of e m p t y guts (Fig. 10). T h e only two e e l p o u t s from J a n u a r y a n d A p r i l 1975 h a d i n d i c e s of 2.9 a n d 4.2, respectively. The catch of four Gasterosteus aculeatus from M a y 1973 y i e l d e d v a l u e s b e t w e e n 3.0 a n d 7.8.

56

C. Dieter Zander & Eike Hartwig F r e q u e n c y of o c c u r r e n c e

In every sample a high percentage of P. microps had preyed on harpacticoids (Fig. 11); gammarids were also regularly present but mostly at low frequencies. Relatively many gobies had ingested detritus and algae which, however, were absent in some catches. All other components were not fed on regularly (Fig. 11). The question of the preferred feeding habitat of P. microps was answered by the method of summing up the respective components. By this, epibenthos proved to be the main food source (100 % in every sample) and phytal fauna played an important role (100-20 %), whereas plankton organisms were absent. The analysis of the elvers caught in May 1974 showed a wide variability of prey organisms among which Mytilus and turbellarians were the most frequent ones. A b u n d a n c e analysis After analysing the numbers of all ingested components of a sample, the great proportion of harpacticoids {87-95 %) in the guts of P. microps is conspicuous (Fig. 12). Algae and detritus, which were fed on relatively frequent (Fig. 11), were present only in small percentages by abundance. The same is valid for gammarids (Fig. 12). The sample of May 1973 contained, contrary to those of the years 1974 and 1975, oal.y 68 % harpacticoids but a relatively large number of macrofauna components. Considering these results, it can be concluded that P. microps did not change its feeding habits during ontogeny, since in September (high mean size) as well as in July 1974 (low mean size) roughly equal parts of macro- and meiofauna were fed on, respectively (Fig. 12). The food of the other species is less exactly interpretable, because large series are absent. In spite of this, it was apparent that the elvers fed on great parts of harpacticoids in May 1974, whereas the larger specimens of July 1974 ingested exclusively gammarids (Fig. 12). The two eelpouts caught in January and April 1975 preyed on identical food, which consisted mainly of harpacticoids (Fig. 12). The same statement is valid for the stickleback catch of May 1973. Biomass of food For the c.alculation of the ingested biomass, the mean dry weights (DW} of the potentially available food organisms were used; these were applied to the components found in the guts. Though this method allows only an approximation of the real conditions, its use is more exact than that of weighing the damaged and differently digested components directly from the guts. The relation of ingested food to total fish biomass does not reflect the results got by means of the fullness index (Fig. 13}. In spring, biomass was low but in autumn very high. Considering single components by weight yields results, differing from those attained by abundance analysis (Fig. 14). Organisms of the macrofauna, especially gammarids, dominate by far, whereas harpacticoids, which prevailed in number, played an inferior, and to some extent an unimportant role. Furthermore, it is remarkable that (1) Crangon crangon was important as food for P. microps in autumn; (2) Jaera albifrons was a great energy supplier for P. microps and, especially, Z. viviparus in spring; (3) Mytilus constituted more than 90 % of biomass for the young A. anguilla in May 1974 (Fig. 14).

Biology a n d food of small-sized fish May16th 7z, p m~crq.p_.._&s

July 15ti~

57 Sept, 24th

A.anquilla

Others

Nov19th

Jen.lSth75

April 1th

Gomrnoridae

Z.viv!parus

Fig. 12. Abundance analysis (numbers) of the food organisms in Pomatoschistus microps, Anguilta anguilla, and Zoarces vivipams during the investigation time

mg food

0

~a L~'

'0k~.

~o~'

~p~

Fig. 13. R e l a t i o n s h i p b e t w e e n w e i g h t s of ingested food (DW) a n d fish (WW) d u r i n g the t i m e of investigation

58

C. Dieter Zander & Eike Hartwig May 16thTz. Pmicrop~

July15th

s~t.24~

Jan,15th75

April 1th

N~rc,~cticokJeo A.anguiUa

Nov19th

~Others~

Turbellaria ,Z.vMparu $

Nsheggs Fig. 14. Proportion of food biomass in Pornatoschistus microps, Anguilla anguilla, and Zoarces viviparus during the time of investigation The total biomass i n g e s t e d by all fish decreased slightly from May to July 1974 but increased steeply in September; during winter very low values were found. Considering the biomass of distinct food components separately, their relative significance becomes evident (Pig. 15). Most gammarids were p r e y e d on in July, while the highest biomass of harpacticoids was found in September 1974. The latter result coincides directly with the abundance of harpacticoids in the benthos samples. Therefore, the high food uptake of these organisms in September p r o b a b l y achieved a supply of them which was more than 50 % below that of the following months (Fig. 16). Regarding gammarids, for example, in July 1974 a high supply as well as a high feeding rate were found (Fig. 16). Together with a decrease in

Biology and food of small-sized fish

59

mg(OW)/m 2

20.

o

Fig. 15. Biomass of food (gammarids, harpacticoids and other components) ingested by the fish during the time of investigation mg(DW]/m2 '~ 10050-

Harpacticoidea .-

~

available ,,"

1051. 0.5.

0.10.05-

0.01

197& July'

()ktl

Jon:

J~oril

July '1975

mg(DW)/m 2 ,i , Gammaridae

1005010 5 1, 0,5, 0.1

July'1975

Fig. 16. Relationship between available and ingested harpacticoids (above) and gammarids (below) during the time of investigation food uptake, only irregular fluctuations of gammarid supply were found in the next samples. DISCUSSION Fluctuation of p o t e n t i a l f o o d o r g a n i s m s Abundance and biomass of benthos show minima in September 1974 and maxima in April 1975 (Figs 2, 5). Density and size group variability of nematodes, harpacticoids {Figs 3, 4), and polychaetes, especially in April 1975, are responsible for this phenome-

60

C. Dieter Z a n d e r & E i k e H a r t w i g

non. T h e fluctuations of n e m a t o d e a b u n d a n c e in the Keitunl m u d fiat w e r e c o n f i r m e d b y s t u d i e s in o t h e r eulittoral a n d sublittoral b i o t o p e s (M511er et aL, 1976; S k o o l m u n & G e r l a c h , 1971). R e g a r d i n g h a r p a c t i c o i d s , M S l l e r et al. {1976) f o u n d situations s i m i l a r to that on Sylt i s l a n d in t h e n e a r s h o r e sublittoral zone. T h e so c a l l e d rest f a u n a w h i c h w a s f o u n d to b e i n s i g n i f i c a n t i n n u m b e r {Fig. 2) m a y constitute a g r e a t p a r t of b e n t h o s b i o m a s s (Fig. 5); this m o s t l y d e p e n d s on s p e c i m e n s w h i c h w e r e l a r g e r t h a n 400 ~tm. T h e a b u n d a n c e a n a l y s i s of o r g a n i s m s from t h e p h y t a l l a y e r d i d not s h o w clear a n n u a l fluctuations. This m i g h t b e d u e to the difficulty in c o l l e c t i n g all v a g i l e m a c r o a n d m e i o f a u n a , e s p e c i a l l y mysids, isopods, g a m m a r i d s , a n d d e c a p o d s , or to t h e h a b i t s of some i n t e r t i d a l species, r e s p e c t i v e l y (Reise, 1977}. O u r results w e r e confirmed b y Grfindel (1976} w h o s t u d i e d s a m p l e s from shallows of the Baltic Sea. I n d e e d , b i o m a s s d y n a m i c s of p h y t a l o r g a n i s m s from K e i t u m (Fig. 7) do not c o r r e s p o n d to the a b u n d a n c e (Fig. 6} b u t are i n f l u e n c e d b y the a n n u a l p r o d u c t i o n of mollusc biomass, w h i c h account for 89-99 % of total biomass. W o r t h m a n n (1975) d e m o n s t r a t e d a s i m i l a r a n n u a l cycle of mollusc b i o m a s s in the Kiel Bight w i t h h i g h v a l u e s in s u m m e r a n d autumn, low ones in w i n t e r a n d spring. T h e a b u n d a n c e fluctuation of d e c a p o d s is c o r r e l a t e d w i t h the b i o m a s s cycle a n d is d e p e n d e n t on t h e m i g r a t i o n s of Carcinus maenas (Muus, 1967; Reise, 1977). After h i b e r n a t i n g in t h e sublittoral zone the y o u n g crabs m i g r a t e into t h e m u d flat in July; in S e p t e m b e r t h e y start to e m i g r a t e into d e e p e r waters. T h e i s o p o d stocks are s u b j e c t to strong fluctuations (Muus, 1967); this a u t h o r found the g r e a t e s t d e n s i t i e s in late s u m m e r a n d a u t u m n a n d therefore s u p p o r t e d the a s s u m p t i o n of H o w e s (1939), w h i c h c o r r e l a t e d i s o p o d d e n s i t y w i t h the a n n u a l course of t h e a u f w u c h s on t h e g r e a t algae. This a s s u m p t i o n c o u l d not b e confirmed in the K e i t u m m u d flat. T h e r e a s o n for this f i n d i n g m a y lie in the t i d a l l y d e p e n d e n t f e e d i n g m i g r a t i o n s of isopods. S i m i l a r b e h a v i o u r is k n o w n of g a m m a r i d s a n d m y s i d s (Reise, 1977). M y s i d s s h o w e d h i g h p e r c e n t a g e s of total a b u n d a n c e a n d b i o m a s s in the K e i t u m m u d flat. A m a s s i v e occurre n c e of these o r g a n i s m s w a s also o b s e r v e d b y Z a n d e r (1979a) on t h e H e l g o l a n d rock flat in August. P l u c t u a t i o n of f i s h D u r i n g the i n v e s t i g a t i o n s at K e i t u m m u d fiat o n l y a few fish s p e c i e s w e r e found: Pomatoschistus microps, elvers of Anguilla anguilla, Zoarces viviparus, and, e x c l u s i v e l y in M a y 1973, Gasterosteus aculeatus. T h e etvers only o c c u r r e d i n s p r i n g b u t w e r e p r e s e n t i n m a s s e s on t h e i r w a y to t h e Aver estuaries. A s i n g l e s p e c i m e n w a s c a u g h t in J u l y 1974, the size of w h i c h i n d i c a t e d it h a d d e l a y e d its m i g r a t i o n into fresh water. In this m o n t h c o m m o n g o b i e s a p p e a r e d for the first time, r e p r e s e n t e d only b y y o u n g s p e c i m e n s , w h e r e a s o n e y e a r o l d ones r e m a i n e d in t h e sublittoral zone for s p a w n i n g . Not until S e p t e m b e r d i d the c a t c h e s r e p r e s e n t a m i x t u r e of y o u n g a n d o n e y e a r o l d s p e c i m e n s . Since only few c o m m o n g o b i e s survive the s e c o n d winter, the s u c c e s s i v e d e c e a s e of t h e e l d e r s p e c i m e n s w i l l h a v e c a u s e d the c o n t i n u a l d e c r e a s e of m e a n size or w e i g h t in the f o l l o w i n g samples. In M a y 1975, all g o b i e s h a d e m i g r a t e d for s p a w n i n g into the sublittoral zone. O n l y single s p e c i m e n s of e e l p o u t s w e r e c a u g h t in J a n u a r y a n d A p r i l 1975; therefore w e a s s u m e that this s p e c i e s m i g r a t e s only r a r e l y into the eulittoral zone. T h e role of Gasterosteus aculeatus i n d i v i d u a l s in the Keitum m u d flat is not y e t clear, since t h e y w e r e c a u g h t only in M a y 1973.

Biology a n d food of s m a l l - s i z e d fish

61

W i t h the e x c e p t i o n of Zoarces viviparus, all s p e c i e s are also found in fresh water. A l l of t h e m are e u r y h a l i n e fish w i t h distinct s e a s o n a l m i g r a t i o n s from the s e a into fresh w a t e r or vice v e r s a ( H e n n i g & Zander, 1981). J u v e n i l e s of P. microps i n v a d e the rivers in late summer, as w a s o b s e r v e d in British w a t e r s (Miller, 1964; Kunz, 1969} a n d in the Elbe river ( H e n n i g & Zander, 1981). W h e n t e m p e r a t u r e s d e c r e a s e in late autumn, t h e y m i g r a t e d o w n t h e rivers into d e e p e r w a t e r s of t h e sea. T h e y o u n g G. aculeatus s w i m from the s p a w n i n g g r o u n d s in fresh w a t e r s into the s e a a n d r e t u r n w h e n 2 y e a r s o l d for s p a w n i n g . T h e y o u n g A. anguilla i n v a d e t h e rivers in s p r i n g and, after s o m e years, m i g r a t e b a c k to the S a r g o s s a S e a for s p a w n i n g (Mtitler, 1975}. The eelpout, on the o t h e r h a n d , is a g e n u i n e m a r i n e s p e c i e s w h i c h also i n h a b i t s b r a c k i s h waters. A c c o r d i n g to t h e s e results, t h e e x t e n s i v e s i m i l a r i t i e s b e t w e e n t h e s m a l l - s i z e d fish f a u n a in t h e rest pools of a m a r i n e a n d of a fresh w a t e r m u d flat b e c o m e evident. Besides G. aculeatus, P. microps, a n d A. anguilla, t h e fresh w a t e r m u d flat also i n c l u d e d Pungitius pungitius ( H e n n i g & Zander, 1981), w h i c h r e g u l a r l y m i g r a t e s into b r a c k i s h w a t e r (Miinzing, 1966). O n l y d u r i n g h i g h t i d e w e r e the m u d flat b i o t o p e s i n v a d e d b y g e n u i n e m a r i n e or fresh w a t e r fish, respectively. T h e m u d flats, therefore, are e x c l u s i v e l y f e e d i n g a n d nursery, p r o b a b l e h i d i n g p l a c e s b u t not s p a w n i n g g r o u n d s for t h e s t u d i e d fish. T h e latter s t a t e m e n t is v a l i d for P. microps in m a r i n e m u d flats as w e l l for the s t i c k l e b a c k s in fresh w a t e r ones.

Qualitative prey-predator

relationships

By c l a s s i f y i n g t h e i n g e s t e d food a c c o r d i n g to distinct m i c r o h a b i t a t s w i t h r e g a r d to its r e s p e c t i v e origin, o n l y slight differences a r e f o u n d b e t w e e n t h e i n v e s t i g a t e d fish species. P. microps c l e a r l y p r e f e r r e d e p i b e n t h o s to p h y t a l species, w h e r e a s s u p r a b e n t h i c c o m p o n e n t s w e r e absent. D u r i n g t h e course of t i m e a c o n t i n u a l d e c r e a s e of food i t e m s o r i g i n a t i n g from the p h y t a l zone w a s f o u n d in this species. In A. anguilIa p h y t a l - f a u n a d o m i n a t e d over e p i b e n t h o s ; in G. aculeatus from M a y 1973 s u p r a b e n t h i c o r g a n i s m s (mysids) w e r e also present. Therefore, differences in results from other i n v e s t i g a t i o n sites a r e evident. In the F ~ h r m a n n s a n d m u d flat of the E l b e river A. anguilla h a d m a i n l y fed on e n d o b e n t h o s w h i c h c o n s i s t e d p r e d o m i n a n t l y of oligochaetes, w h e r e a s G. aculeatus and, to a lesser d e g r e e , P. microps p r e f e r r e d p l a n k t o n ( H e n n i g & Zander, 1981}; e p i b e n t h o s o r g a n i s m s p l a y e d no role in the food of t h e s e fish. O n a stony g r o u n d in the Baltic Sea, on the other h a n d , s u p r a b e n t h o s w a s s e l d o m i n g e s t e d b y P. microps w h i c h p r e f e r r e d p h y t a l - l i v i n g f a u n a a n d e p i b e n t h o s t h e r e {Zander, 1979b). R e g a r d i n g s i n g l e food c o m p o n e n t s , two, f o u n d in P. microps from Keitum, a r e n o t a b l e : (1) Crangon crangon i n h a b i t i n g the e p i b e n t h a l l a y e r w a s fed on r e g u l a r l y b u t not a b u n d a n t l y . This s p e c i e s w a s f o u n d w i t h a r e l a t i v e l y h i g h b i o m a s s in c o m m o n g o b i e s from S c o t l a n d (Healey, 1972) a n d from t h e m o u t h of t h e E t b e river (Kfihl, 1972). (2) A l g a e w e r e not f o u n d in t h e p r e v i o u s i n v e s t i g a t i o n s of P. microps guts, b u t w e r e p r e s e n t in the r e l a t e d P. pictus (Zander, 1979a). In Keitum, a l g a e w e r e also i n g e s t e d r e g u l a r l y b u t in low biomass. P r e s u m a b l y t h e y w e r e f e d on, only b y chance, t o g e t h e r w i t h s m a l l v a g i l e organisms. On the o t h e r hand, in the P. microps from Keitum, c o m p o n e n t s are a b s e n t w h i c h w e r e f r e q u e n t l y p r e y e d on b y s p e c i m e n s at other sites, such as Corophium (Healey,

62

C. D i e t e r Z a n d e r & E i k e H a r t w i g

1972), c h i r o n o m i d l a r v a e a n d Idothea (Zander, 1979b). T h e r e a s o n m a y lie in t h e a b s e n c e or r a r e o c c u r r e n c e of the p o t e n t i a l l y a v a i l a b l e food. Quantitative

prey-predator

relationships

The most i m p o r t a n t nutritional c o m p o n e n t w i t h r e g a r d to w e i g h t w a s g a m m a r i d s in all i n v e s t i g a t e d fish of the K e i t u m m u d flat. T h e n e x t i m p o r t a n t foods, w i t h a n n u a l fluctuations, w e r e p o l y c h a e t e s , Crangon, or h a r p a c t i c o i d s in P. microps. O n l y the elvers of A. anguilla h a d i n g e s t e d g r e a t proportions of h4ytilus in M a y 1974, w h e r e a s , in Z. viviparus, J a e r a d o m i n a t e d in A p r i l 1975. T h e harpacticoids, w h i c h w e r e d o m i n a n t in n u m b e r b u t u n i m p o r t a n t in b i o m a s s are an i n d i c a t o r for the g r e a t f e e d i n g activity of P. microps. This result is in a g r e e m e n t w i t h other i n v e s t i g a t i o n s r e g a r d i n g this s p e c i e s ( C a s a b i a n c a & Kiener, 1969; Groth, 1978; Zander, 1979b; H e n n i g & Zander, 1981; S c h m i d t - M o s e r & W e s t p h a l , 1981). In G. aculeatus p l a n k t o n c o p e p o d s f r e q u e n t l y domin a t e d (Hynes, 1950; H e n n i g & Zander, 1981). D u r i n g t h e course of t h e y e a r the b i o m a s s of i n g e s t e d food w a s g r e a t e s t in s u m m e r a n d a u t u m n b u t l o w e s t in winter. No correlation w a s f o u n d b e t w e e n food s u p p l y a n d d e n s i t y or b i o m a s s of s m a l l - s i z e d fish w h i c h w a s g r e a t e s t in s p r i n g a n d summer. A v e r y g r e a t p r e d a t o r y a c t i v i t y w a s f o u n d in S e p t e m b e r 1974 (Fig. 15). T e m p e r a t u r e s d e c r e a s e d after S e p t e m b e r to 7 °C a n d r e d u c e d f e e d i n g activity. But in t h e N o v e m b e r catch a g r e a t p a r t of y o u n g fish w a s still p r e s e n t w h i c h a p p a r e n t l y n e e d e d a h i g h e n e r g y s u p p l y for growth. In S e p t e m b e r 1974, w h e n d e n s i t y of P. microps w a s greatest, a h i g h f e e d i n g rate on h a r p a c t i c o i d s c o i n c i d e d w i t h an e v i d e n t l y r e d u c e d s u p p l y of t h e s e organisms. This p h e n o m e n o n m a y b e d u e to g r a z i n g effect b u t other e x p l a n a t i o n s are also possible. In the f r e s h - w a t e r m u d flat F ~ h r m a n n s a n d (Elbe river), cyclopoids a n d h a r p a c t i c o i d s d e c r e a s e d at the t i m e w h e n y o u n g P. microps i m m i g r a t e d ( H e n n i g & Zander, 1981). This w a s also confirmed for the Baltic Sea fjord Schlei ( S c h m i d t - M o s e r & W e s t p h a l , 1981). Reise (1979), on the other hand, found P. microps to h a v e no i n f l u e n c e on m e i o f a n n a during cage experiments. T h e b i o m a s s i n g e s t e d b y s m a l l - s i z e d fish in the K e i t u m m u d flat w a s h i g h e s t in S e p t e m b e r 1974 w i t h 17.6 m g DW m -2, This v a l u e i m p l i e s o n l y a p a r t of t h e d i e l rate. In P. microps t h e d i g e s t i o n t i m e of food is u n k n o w n b u t w a s f o u n d in the r e l a t e d Gobiusculus flavescens to b e a b o u t 3 hours (Berg, pets. comm.). B a s e d on this r e s u l t one m a y e x p e c t a turnover r a t e of r o u g h l y 70 m g D W m -2 d -1 s i n c e the fish a r e active o n l y d u r i n g the day. As the b e n t h a l a n d phy~al l a y e r s offer a food b i o m a s s of 480 m g D W m -2 (without molluscs) this m e a n s that a l m o s t o n e s e v e n t h m i g h t b e t u r n e d over b y small, b o t t o m fish in a day.

Acknowledgements. We are indebted to A. Dowling, H. Lachnit, D. Lorenzen, and L. SeitzHildebrand for technical help and to M. H~inel for drawing the figures. The "Sonderforschungsbereich 94" of the University Hamburg supported the field studies by travel grants, the Deutsche Forschungsgemeinschaft by grants to the first author (Za 44/4).

B i o l o g y a n d f o o d of s m a l l - s i z e d f i s h

63

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