European and North American boreal brackish regions (Muus, 1967; Kendall, .... V. Vl. VII VIII. IX. X. Xl. Xll. Fig. 4. Mean densities (x __ sd) of M. aestuarina in the ...
HELGOLANDER MEERESUNTERSUCHUNGEN Helgolander Meeresunters. 50, 287-298 (1996)
Reproduction and larval development of Manayunkia aestuarina (Bourne, 1883) (Polychaeta, Sabellidae) in a coastal region of the southern Baltic A. Bick Universit~t Rostock, FB Biologie, Allgemeine & Spezielle Zoologie; Universit~tsplatz 5, D-18051 Rostock, Germany
ABSTRACT: The reproduction and larval development of Manayunkia aestuarina, a polychaete typical of brackish tenitic waters, was studied in a tideless shallow region on the south Baltic coast in 1990. Reaching abundances of up to 50000 ind./m 2, it is an important element of the benthic community in this area. Reproduction started in late March/early April, when the females deposited their eggs in the tubes. On the average, 4 (maximum: 16) developing embryos were found in a maternal tube during the reproduction period. The females probably produced a mean of about 12 eggs. Development in the maternal tube lasted about 8 weeks. The first juveniles were found outside the tubes in mid-May. The survival rate during the first few weeks was estimated to be 15-20 %. After reproducing, the adult animals survived until October. The changes involved in the development from eggs to juvenile animals are illustrated by drawings.
INTRODUCTION
Manayunkia aestuarina is a c h a r a c t e r s p e c i e s of s h a l l o w lenitic w a t e r s , e s p e c i a l l y in E u r o p e a n a n d N o r t h A m e r i c a n b o r e a l b r a c k i s h r e g i o n s (Muus, 1967; K e n d a l l , 1979; Bell, 1982; Bishop, 1984; J u n o y & Vi6itez, 1990). R e a c h i n g e n o r m o u s a b u n d a n c e s in s o m e p l a c e s (up to 1.5 x 106 ind./m2), the s p e c i e s is an i m p o r t a n t c o m p o n e n t of t h e b e n t h i c c o m m u n i t y . T o g e t h e r w i t h t h e o s t r a c o d e Cyprideis littoralis, it is c h a r a c t e r i s t i c of e u h t toral a n d s u p r a l i t t o r a l soft b o t t o m s in t h e N o r t h a n d Baltic S e a s ( R e m a n e , 1940). In v i e w of this, it is a s t o n i s h i n g that t h e b i o l o g y of M. aestuarina h a s r e c e i v e d little a t t e n t i o n in t h e past. A l t h o u g h L e w i s (1968) d e s c r i b e d its f e e d i n g m o d e a n d tube, a n d b o t h F o r s m a n n (1956) a n d Schiitz (1965) m e n t i o n e d s o m e a s p e c t s of its r e p r o d u c t i o n , r e p r o d u c t i o n a n d l a r v a l d e v e l o p m e n t h a v e n e v e r b e e n d e s c r i b e d in detail. T h e p r e s e n t p a p e r d e s c r i b e s l a r v a l d e v e l o p m e n t of N/. aestuarina w i t h i n t h e m a t e r n a l t u b e in a c o a s t a l w a t e r of the s o u t h Baltic. MATERIAL AND METHODS O u r s t u d i e s w e r e u n d e r t a k e n in a t i d e l e s s w a t e r in M e c k l e n b u r g Bay o n t h e s o u t h Baltic coast (Fig. 1) in 1990. S a m p l e s w e r e c o l l e c t e d at m o n t h l y i n t e r v a l s o u t s i d e of t h e r e p r o d u c t i o n period, a n d e v e r y two w e e k s f r o m April to A u g u s t . T h e s a m p l e s w e r e t a k e n b y c o r e r (2.83 cm2). T h e p a t c h i n e s s of t h e distribution w a s c o m p e n s a t e d for b y p o o l i n g four c o r e s at a t i m e to form a h a u l (-- 11.34 cm2). At l e a s t t h r e e h a u l s (i.e. 12 cores) w e r e 9 Biologische Anstalt Helgoland, Hamburg
288
A, Bick
~ :
",
~=!:'
ostock
5/'~
Wismar IOOE
ll o
12 ~
13 ~
Fig. 1. Location of the investigation area in the south Baltic Sea
t a k e n at each sampling. The hauls were fixed with borax-buffered f o r m a l d e h y d e (4 %) a n d sieved (0.1 m m mesh size) at the laboratory. The water t e m p e r a t u r e was measured, a n d s e d i m e n t samples were t a k e n for d e t e r m i n i n g grain size a n d organic c o n t e n t on each sampling date. After sieving, the animals were removed from the samples u n d e r a dissecting microscope (20 x magnification), a n d the age a n d sex were d e t e r m i n e d at a magnification of 100 x u n d e r a microscope. Age d e t e r m i n a t i o n was b a s e d on the n u m b e r of a b d o m i n a l hooks (Bick, 1995), b u t sexing was only possible after g a m e t o g e n e s i s w h e n eggs could b e s e e n i n the 4th sefiger, a n d w h e n the 6th to 8th thoracic s e g m e n t s of males were full of spermatozoa. The tubes of h/IanayunkJa aestuarina were also e x a m i n e d for the presence of eggs a n d larvae; the n u m b e r s per tube a n d the a v e r a g e n u m b e r per sample were calculated. The various d e v e l o p m e n t a l stages were also m e a s u r e d at a magnification of 100 • or 200 x.
RESULTS Both t e m p e r a t u r e a n d salinity in the investigation area are subject to a n n u a l variation (Pig. 2). The water t e m p e r a t u r e varied b e t w e e n 0.9 and 20.8 ~ d u r i n g the study, a n d the salinity b e t w e e n 10.6 a n d 16.7~ The organic content of the s e d i m e n t varied b e t w e e n 1.2 a n d 2.5 % DW, a n d the m e a n grain size b e t w e e n 0.14 a n d 0.25 ram. Manayunkia aestuarina (Pig. 3) was a m o n g the most c o m m o n m a c r o z o o b e n t h o s representatives in the investigation area. The a v e r a g e a b u n d a n c e d u r i n g the y e a r was a b o u t 35 000 i n d . / m 2 (Fig. 4). No distinct a n n u a l varia~on was found, b u t there was
Manazunkia aestuarina development --=
water
temperature
(~
289
----o---salinity
(ppt)
20
15
i0
5
I
Jan
L
Feb
I
Mar
I
Apr
I
May
~
Jun
L
Jul
I
Aug
L
Sep
I
Oct
I
Nov
t
Dec
Fig. 2. Seasonal temperature and salinity variations in the investigation area in 1990
considerable variation a m o n g sampling dates, a n d the standard deviations were also high. Analysis of the structure a n d d e v e l o p m e n t of the population showed that gametogenesis started in January. Males a p p e a r to reach sexual maturity prior to females, a n d the largest n u m b e r of mature males relative to the total population were recorded in March. However, the proportion of mature females continued to increase until m i d - M a y (Fig. 5). The first eggs were found in the tubes of females in March. Thereafter, the proportion of females with various d e v e l o p m e n t a l stages in their tubes i n c r e a s e d from 50 % in early April to 72 % at the e n d of May. Larvae were found in the tubes until 9th August. The reproduction period reached its climax in mid-May, w h e n it was possible to identify the sex of virtually all individuals. None of the tubes contained more t h a n 3 eggs at the e n d of March, which suggests that a clutch consists of about 3 eggs. O n the average, 4 eggs or 4 embryos were found in the tubes of females in April a n d May (Fig. 6). The largest n u m b e r of eggs a n d d e v e l o p i n g embryos found in a single tube was 16 in m i d - M a y (Figs 6, 9). This indicates that b e t w e e n 4 to 8 clutches had b e e n p r o d u c e d b y that time. The adult animals r e m a i n e d alive after releasing their sexual products, b u t sexing was t h e n no l o n g e r possible. The sex ratio was about 1:1. The first b u r r o w i n g juveniles were found in mid-May, i.e. d e v e l o p m e n t in the m a t e r n a l tube took about 8 weeks. The proportion of juveniles in the total p o p u l a t i o n i n c r e a s e d thereafter a n d exceeded 50 % b y mid-July. The y o u n g e s t d e v e l o p m e n t a l stages generally occupied the front part of the tube with the more a d v a n c e d embryos b e h i n d them. All larvae "faced" the t u b e mouth, a n d all eggs a n d larvae were joined by a m u c o u s coating (Fig. 7).
290
A. Bick
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Fig. 3. A4anayunkia aestuarina: male and female, both mature; about 4 mm long Growth d u r i n g d e v e l o p m e n t from eggs to, j u v e n i l e s in the m a t e r n a l t u b e is shown in the l e n g t h histograms (Fig. 8). The smallest stages (eggs) were 235 ~m long, a n d larvae longer than 660 ~m were rarely found in the tubes (maximum length: 760 ~m). The histograms show w h y the first juveniles were found outside the m a t e r n a l t u b e s in midM a y (Fig. 5): larvae from the first clutch did not reach their m a x i m u m l e n g t h until about this time. A second clutch was laid a b o u t 4 w e e k s after the first (cf. also Fig. 6). Since there was no synchronous d e v e l o p m e n t within clutches, a n d since the n u m b e r of eggs p e r clutch varied, it was not possible to ascertain just how m a n y clutches w e r e produced. The lengths of the 16 y o u n g A//. aestuarina d e v e l o p i n g within a single t u b e are shown in
M a n a y u n k i a aestuarina d e v e l o p m e n t
80
291
Ind./lO cm 2
60
/
40
20
I
L
II
I
I
III
I
IV
E
V
I
Vl
L
VII
I
VIII
~
IX
I
X
L
Xl
Xll
Fig. 4. Mean densities (x __ sd) of M. aestuarina in the investigation area in 1991
Figure 9. O w i n g to variability in e g g size and growth rate and to the possibility of mortality a m o n g embryos, w e cannot say exactly w h e n s u b s e q u e n t clutches w e r e p r o d u c e d and h o w large they were, but e g g s can obviously be p r o d u c e d until July at least.
100%
80%
60%
40%
20%
0% 20.3
3.4
20.4
3.5
16.5
28.5
13.6
1.7
19.7
9.8
Fig. 5. Population structure of Mr. aestuarina in the investigation area in 1990
28.8
292
16
A. Bick
Number of eggs and larvae
A
12
8
4 0
0
i
20.3
3.4
[
i
20.4
3.5
~
16.5
L
28.5
i
13.6
i
1.7
9
---.='Q
i
i
19.7
9.8
Fig. 6. M e a n and m a x i m u m n u m b e r s of e g g s and larvae per tube of female M. a e s t u a r i n a
Some of the d e v e l o p m e n t a l s t a g e s w e found are shown in Figure 10. Early ovoid d e v e l o p m e n t was m a r k e d b y i n c r e a s i n g l e n g t h and, initially, d e c r e a s i n g width. The tentacular crown started d e v e l o p i n g relatively early, its first signs b e i n g t h e a p p e a r a n c e of protuberances. External s e g m e n t a t i o n was a l r e a d y b e c o m i n g a p p a r e n t as the two trunks of the t e n t a c u l a r crown w e r e d e v e l o p i n g . T h e radioli a n d setae d e v e l o p e d more or less concurrently. Capillary s e t a e a p p e a r e d in the thoracic region, starting at the front end, before thoracic s e g m e n t a t i o n h a d b e e n c o m p l e t e d a n d a b d o m i n a l s e g m e n t a t i o n h a d started. Formation of the h o o k s started after s e g m e n t a t i o n h a d b e e n c o m p l e t e d . The juveniles left the m a t e r n a l t u b e at this point. Adult a n d juvenile i n d i v i d u a l s w e r e found side b y side after the e n d of t h e r e p r o d u c tion p e r i o d (Fig. 11), the a d u l t animals obviously surviving u n t i / O c t o b e r . By N o v e m b e r , juveniles h a d d e v e l o p e d almost the s a m e n u m b e r of a b d o m i n a l hooks as t h e adults a n d were also almost the s a m e size. Little g r o w t h took p l a c e in winter, the m e a n n u m b e r of a b d o m i n a l hooks i n c r e a s i n g only slightly from N o v e m b e r to F e b r u a r y . T h e correlation b e t w e e n the n u m b e r of hooks a n d t h e m a x i m u m width of the front third of the b o d y is shown in Figure 12. DISCUSSION Manayunkia aestuarina is a c h a r a c t e r species of eulittoral a n d supralittoral soft bottom communities in the b r a c k i s h b o r e a l w a t e r s of North A m e r i c a a n d Europe. Only Harris (1970) r e p o r t e d that stable p o p u l a t i o n s also exist in m a r i n e regions. H o w e v e r , his illustration of M. aestua~ina b e a r s little r e s e m b l a n c e to the species. M o r e specifically, the pinnules he shows in the t e n t a c u l a r c r o w n are too n u m e r o u s for M. aestuarina. T h e species he d e s c r i b e d is p r o b a b I y a different m e m b e r of t h e Fabricinae. The a b u n d a n c e s found in b o t h E u r o p e a n a n d North A m e r i c a n estuaries are of a level
M a n a y u n k i a aestuarina d e v e l o p m e n t
293
Fig. 7. Typical positions of developmental stages in the tubes of female A4. aestuarina; the stages are between 240 and 520 ~m long. The larvae are arranged with the front ends facing the tube mouth
normally r e a c h e d only by meiobenthic species. Bagheri & McLusky (1982) reported a b u n d a n c e s of up to 1.5 x 1 0 6 i n d . / m 2 in the Forth estuary, a n d E c k m a n n (1979) found up to 0.5 x 106 i n d . / m 2 in North America. A b u n d a n c e s of these m a g n i t u d e s are u n k n o w n in the Baltic Sea, where the species rarely exceeds 50000 i n d . / m 2. Nevertheless, M. aestuarina is also a character species of shallow lenitic regions in this area. The high standard deviations recorded in our investigation area despite pooled sampling indicate that the distribution of M. aestuarina is patchy (Fig. 4). Moreover, the considerable variation of the a b u n d a n c e in time also m a s k e d the a n n u a l population dynamics of the species in this area. However, n e i t h e r Bell (1982) nor Kendall (1979) reported m a r k e d seasonal variations in South Carolina a n d the Tee estuary, respectively. S e d i m e n t properties appear to be the decisive factor affecting the macroscale a n d mesoscale distribution of M. aestuarina. Previous studies in our investigation area have shown that c h a n g e s in the organic content of the s e d i m e n t lead to c h a n g e s in the
A. Bick
294
% 355.633.3 0 2010~
30
N=9
10 0
0
301 m70 20 t m m 10 0 30
13.6
3,4 N=IO
49.5
28.5
%
20.3
20 10 0
20.4
30
1.7
mmmmmm
,o
0
30
43.5
3.5
20 10 [ ~ m m m ~ m m l ~ ~
0 30 20 10 0
16.5
260
340
420
500
580
19.7
30
"--4 mmm
20 10 ~ m 0 30
660 IJm
9.8
[ m mmm
20 10 O - -
260
N=4
340- - 420
500
560
660 pm
Fig. 8. Length histograms for developmental stages in the tubes of M. aestuarina females (each sizeclass 40 [~m, arbitrarily choosen)
a b u n d a n c e of this species. Reduction of the organic content from a b o u t 1.8 % to 1.0 % was followed b y a reduction in a b u n d a n c e from a b o u t 16 000 to 6000 i n d . / m 2. S e d i m e n t quality also a p p e a r s to influence reproduction. Schfitz (1965) r e p o r t e d that M. aestuarina r e p r o d u c e s from late M a y to A u g u s t in the Baltic Sea, with some d e l a y in more northern latitudes o w i n g to the l o n g e r winters a n d lower w a t e r t e m p e r a t u r e s in spring. In the North Sea, reproduction r e p o r t e d l y starts in M a r c h a n d e n d s in summer. A l t h o u g h Bagheri & M c L u s k y (1982) stated t h a t r e c r u i t m e n t t a k e s p l a c e from M a y to July, Bell (1982) found the first juvenile w o r m s in April. This d i s c r e p a n c y in d a t e s is obviously d u e to differences in w a t e r t e m p e r a t u r e s , w h i c h rarely drop b e l o w 10 ~ e v e n in winter a l o n g the coast of South Carolina, a n d c a n r e a c h 20 ~ e v e n in April. Reproduction is obviously also i n f l u e n c e d b y t e m p e r a t u r e : low temp e r a t u r e s in w i n t e r a n d spring d e l a y both m a t u r a t i o n a n d the rate of larval d e v e l o p m e n t . The t e m p e r a t u r e s m e a s u r e d in the south Baltic in spring 1990 w e r e a b o u t t h e s a m e as the l o n g - t e r m mean, a n d the b e g i n n i n g a n d course of r e p r o d u c t i o n is p r o b a b l y similar in the estuaries of both the North Sea a n d the Baltic. The d e v e l o p m e n t a l times of 2 a n d 2 to 4 w e e k s in the m a t e r n a l tube r e p o r t e d for the r e l a t e d species Fabricia sabella a n d ~VI. caspia, respectively, (Nausch, 1982 a n d Marinescu, 1964) a n d for/t4 r. aestuarina in a salt m a r s h in Sot~th Carolina (Bell, 1982) are obviously shorter t h a n in b o r e a l regions, w h e r e a b r o o d i n g p e r i o d of 8 to 10 w e e k s is typical. A l t h o u g h t e m p e r a t u r e d o e s influence
Manayunkia aestuarina development
295
Number
size
(~m)
260 280 300 320 340 360 380 4 0 0 420 440 460 480 500 520 540 5 6 0 5 8 0 600
Fig. 9. Length distribution of developmental stages (N = 16) in the tubes of a female M. aestuarina on May 16th, 1991 (each size-class 20 ~m, arbitrarily chosen)
larval d e v e l o p m e n t (e.g. A n g e r et al., 1986), we do not think that a minor t e m p e r a t u r e increase would reduce the d e v e l o p m e n t time by half. The sex ratio (females:males) of 3-5:1 reported by Forsman (1956) a n d Schfitz (1965) could not be confirmed for our investigation area. The sex ratio r e m a i n e d about 1:1 d u r i n g the entire reproduction period. However, SchLitz (1965) also found a supralittoral population in which males formed a distinct majority. This discrepancy m a y signify regional differences. The 16 eggs a n d embryos, at different stages of development, that we found in a single tube is the highest n u m b e r ever reported. SchLitz (1965) a n d Bell (1982) n e v e r found more t h a n 8 a n d 12 embryos, respectively, in a single tube. However, our data permit no conclusions to be d r a w n r e g a r d i n g average fecundity. The m e a n n u m b e r of eggs or larvae f o u n d in a tube during the reproduction period was about 4. A s s u m i n g that the average clutch consists of three eggs a n d that one clutch is produced about every 4 w e e k s (cf. Fig. 8), we estimate that a female m a y produce about 12 eggs d u r i n g the reproduction period. However, the n u m b e r s that failed to develop or were lost during sample collection a n d h a n d l i n g are u n k n o w n . Figures 4 a n d 5 show, however, that the a b u n d a n c e of M . a e s t u a r i n a in the investigation area d o u b l e d after mid-July, a n d that a b o u t half the population consisted of juveniles. In view of the sex ratio of 1:1, this m e a n s that 2 juveniles per female had survived at that time. Since the investigation area is fairly sheltered, the e x c h a n g e of water is only slight a n d the juveniles settle a n d b u r r o w their t u b e s only shortly after l e a v i n g those of the females, i.e. apparently without significant migration. It is u n l i k e l y that large n u m b e r s immigrate or emigrate. Therefore, the survival rate of juveniles must have b e e n about 15 to 20 % at that time. At t e m p e r a t u r e s b e t w e e n 15 a n d 20 ~ d e v e l o p m e n t from the egg to a j u v e n i l e worm living on its o w n takes about 8 weeks. External segmentation, the formation of a
A. Bick
296
O.
b
C
Fig. 10. Developmental stages of M. aestuarina, a: early stage (276 • 138 ~m); b: start of tentacular crown development (388 x 125 ~m); c: onset of external segmentation, lateral view (480 • 140 ~m); d: gradual abdominal segmentation and onset of setal development (498 x 115 ~m)
tentacular crown and the a p p e a r a n c e of the first setae and hooks take p l a c e within this period. No cihary girdles w e r e o b s e r v e d g r o w i n g on the larval bodies. T h e cilia of the tentacular cr o w n and around the fecal pit obviously d ev el o p after the m a t e r n a l t u b e has b e e n left. T h e oral aperture is already p r e s e n t by this time, an d the animals start f e e d i n g actively. It s ee m s hkely that larval food r e s e r v e s are virtually e x h a u s t e d w h e n this transition t a k e s place. A b d o m i n a l s e g m e n t a t i o n an d setation are c o m p l e t e d after the m a t e r n a l t u b e has b e e n left. The n u m b e r of a b d o m i n a l hooks is a c o n v e n i e n t guide to age. H o w e v e r , in co n n ection with t ax on o m ic studies it is n e c e s s a r y to take into account the v a r i a t i o n in the n u m b e r of a b d o m i n a l hooks with i n c r e a s i n g ag e (Bick, 1995). This is particularly
297
Manayunkia aestuarina development Number
70
of
abdominal
hooks Adults
60 50
w'--'~~
40
.....
30 20
Juvenila?sl
_+///'~/'/'''
i0 0
I
J
I
F
I
M
I
A
I
M
I
J
I
J
I
I
A
S
I
0
I
N
I
D
Fig 11 Growth curve of A// aestuarina during the investigation period based on the number of abdominal hooks (x _+ sd, N = 559)
400 Width
(~m)
350 300
-.i;..-.
250
.
200
105,29
/
150
Ra =
0.57
N
=
149
I00 50 Number 0 0
)
l
i0
20
i
30
of i
40
50
abdominal i
60
hooks l
70
Fig 12 Correlation between the number of abdominal hooks and segment width of A//aestuarina in the investigation area
important in the case of the Fabricinae since the shape and number of certain hooks and setae are of diagnostic importance in this group (Annenkova, 1928; Banse, 1956; Fitzhugh, 1983). Acknowledgements. I thank Dr. H.-D. Franke of the Biologische Anstalt Helgoland for his interest~ ing comments, and B. Patchett for his help in translating the manuscript.
298
A. B i c k LITERATURE
CITED
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