determine the development stage of their reproductive organs. ... The study was conducted on the tidal flats of the Nord-Sylter Wattenmeer. The tidal range is ...
HELGOL,~NDER MEERESUNTERSUCHUNGEN Hetgol~nder Meeresunters. 50, 337-351 (1996)
R e p r o d u c t i o n of
Amphiporus lactifloreus
( H o p l o n e m e r t i n i ) o n t i d a l ilats: i m p l i c a t i o n s i o r s t u d i e s o n t h e p o p u l a t i o n b i o l o g y of n e m e r t i n e s Martin Thiel 1' 2," & Thorsten Dernedde 1, 3 1Biologische Anstalt Helgoland, Wattenmeerstation Silt; D-25992 I_ust, Germany 2Universit~t Kiel, Zoologisches Institut, Arbeitsgruppe Marine Okologie und Systematik; Olshausenstr. 40-60, D-24118 Kiel, Germany 3Universit~t IQ'el, Institut ffJr Haustierkunde; Olshausenstr. 40-60, D-24118 IQ'el, Germany
ABSTRACT: The reproductive period and life-history parameters were investigated for the hoplonemertine Amphiporus lactifloreus found on the tidal flats of the island of Sylt in the northern W a d d e n Sea. Every six weeks 20 individuals were collected and then histologically e x a m i n e d to determine the development stage of their reproductive organs. A. lactifforeus reproduces in the late autumn, its peak reproduction b e i n g in the second half of November. Individuals from all size classes > 20 mm body length produced gametes. Individuals of the cohorts that reproduced in the late autumn of 1992 persisted and grew until July 1993, indicating that A. lactifloreus is an iteroparous species. The length of relaxed individuals was significantly correlated with their length u n d e r anaesthetized conditions, but the regression c h a n g e d significantly after the reproductive period. Length under 'relaxed' conditions was significantly correlated with weight (wet weight, dry weight, and ash-free dry weight); these relationships did not vary significantly before or after the reproductive period. Our results show that important life-history data of intertidal nemertines can b e obtained without time-consuming histological studies. On the basis of these findings, recommendations for future studies on the population biology of intertidal nemertines are given. Regular length measurements of nemertines u n d e r 'relaxed' conditions are proposed as a useful tool for tracking the growth a n d survival of a n n u a l cohorts of intertidal nemertines.
INTRODUCTION N e m e r t i n e s a r e i m p o r t a n t e n d o b e n t h i c p r e d a t o r s i n e s t u a r i n e e c o s y s t e m s (Roe, 1970, 1976, 1993; Reise, 1985; M c D e r m o t t , 1984, 1993; A m b r o s e , 1991). T h e y m a y h a v e a s i g n i f i c a n t p r e d a t i o n e f f e c t o n t h e i r p r e y p o p u l a t i o n s (Roe, 1976; N o r d h a u s e n , 1988; R o w e l l & Woo, 1990), or t h e y m a y p r o v o k e p r e y m o v e m e n t s w i t h i n t i d a l fiats ( T h i e l & Reise, 1993). To u n d e r s t a n d t h e role of n e m e r t i n e s i n b e n t h i c a s s e m b l a g e s , a b a s i c k n o w l e d g e of t h e i r p o p u l a t i o n b i o l o g y is crucial. H o w e v e r , t h e r e a r e o n l y s c a t t e r e d r e c o r d s of t h e o c c u r r e n c e of i n t e r t i d a l n e m e r t i n e s , a n d a p a r t f r o m t h e s t u d i e s b y Roe (1970, 1976, 1993) d e t a i l e d s t u d i e s o n t h e p o p u l a t i o n b i o l o g y of i n t e r t i d a l n e m e r t i n e s do
9 Present address: Darling Marine Center, University of Maine; Walpole, ME 04573, USA 9 Biologische Anstalt Helgoland, H a m b u r g
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Gullmar Fjord, Sweden North Sea & British tsles British Isles French Atlantic Coast Britanny, French Atlantic Coast Mediterranean
Fig. 1. Reproductive periods of Amphiporus lactifloreus in different regions of the northern hemisphere
not exist. Our p r e s e n t k n o w l e d g e of i n t e r a n n u a l variations in n e m e r t i n e a b u n d a n c e is very limited. W h e n looking for information on recruitment processes an d the factors that influence them, one must fall b a c k on reports of an observational nature (e.g. Coe, 1943; Riser, 1974). In the case of most n e m e r t i n e species it is u n k n o w n w h e t h e r t h e y r e p r o d u c e more than once during their lifetime. Apart from a few historical reports on individuals surviving for several years in the laboratory (McIntosh, 1873/74), nothing is k n o w n about their life-span (Gibson, 1972). This elucidates the n e e d to foster our k n o w l e d g e of basic life-history information of nemertines. As a step in this direction, we i n v e s t i g a t e d the reproductive biology of A m p h i p o r u s lactifloreus. This h o p l o n e m e r t i n e is a c o m m o n e n d o b e n t h i c predator in m a n y coastal areas of Europe (Gibson, 1972, 1982), and it can frequently be found on the tidal flats of the Nord-Sylter W a t t e n m e e r (Reise, 1985; Thiel & Reise, 1993; Albrecht & Reise, 1994). In order to reveal basic information on the life-history of this species and to p r o v i d e m e t h o d s to improve studies of the population biology of this and other intertidal n e m e r t i n e species, we ad d r e s s e d the following questions: W h e n is the reproductive period of A. Mcti[loreus? - The available data on the reproductive period of this n e m e r t i n e species in Europe vary considerably (Fig. 1). Do all individuals of the population participate in a reproduction e v e n t ? - For population studies it is of prime i m p o r t a n c e to k n o w w h e n a species a c h i e v e s maturity. Is A. lacti[loreus s e m e l p a r o u s or iteroparous? - Coe (1943) m e n t i o n s that large n e m e r t i n e species probably r e p r o d u c e in several successive years (iteroparous), w h e r e a s smaller species probably die after their first reproduction. Riser (1974) r e c o r d e d that individuals of L i n e u s viridis die as a c o n s e q u e n c e of spawning, a n d that after the reproductive period only very small individuals can be found on tidal fiats. Furthermore, in order to facilitate future studies on the population b i o l o g y of A. lactifloreus (and other nemertines), w e e x a m i n e d w h e t h e r l e n g t h is a m e a s u r e potentially indicative of different a g e classes.
MATERIAL AND M E T H O D S The study was c o n d u c t e d on the tidal flats of the Nord-Sylter W a t t e n m e e r . Th e tidal r a n g e is about 1.8 m (Reise, 1985), In this area, A m p h i p o r u s ]actifloreus can r each densities of up to 250 individuals / m 2 (Thiel & Reise, 1993). Mussel clumps, w h i c h are an important micro-habitat of this n e m e r t i n e , are very a b u n d a n t in the study a r e a (Reise et al., 1989; Albrecht, 1991).
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E x a m i n a t i o n of t h e r e p r o d u c t i v e s t a g e of A m phi porus lactifloreus We collected A. lactifloreus from the tidal fiats of the island of Sylt in the n o r t h e r n W a d d e n Sea b e t w e e n August 1992 a n d July 1993 every 6-8 weeks. On each s a m p l i n g date we collected 20-24 individuals which were separated from mussel clumps in the field. We m e a s u r e d their length by allowing them to crawl along a ruler (described below in 'Biometrics of A. lactifloreus'). N e m e r t i n e s were g r o u p e d into 7 different l e n g t h classes according to the m e a s u r e m e n t s u n d e r 'relaxed' conditions (- 70 ram). Before fixation, the n e m e r t i n e s were anaesthetized with 7.5 % MgC12-solution. Specimens were fixed in Bouin's fluid for 24 h a n d then transferred to 70% alcohol. Animals were e m b e d d e d in 54 ~ paraffin wax for sectioning. In order to e x a m i n e the reproductive stage of the gonads, we prepared sections (6-8 ,um) from the middle part of every a n i m a l ' s body. The sections were stained using the Mallory-trichrome-method. We e x a m i n e d 50 sections of each individual u n d e r the microscope, d e t e r m i n e d its sex w h e n possible, and classified the d e v e l o p m e n t a l stage of the gonads in every section according to the description p r e s e n t e d in Table 1. The latest stage of d e v e l o p m e n t that was found to be in majority after 50 sections of an individual were e x a m i n e d was used to classify its reproductive stage. B i o m e t r i c s of A m p h i p o r u s lactifloreus In order to e x a m i n e the general biometrics of Amphiporus lactifloreus a n d to test w h e t h e r relationships b e t w e e n different, easily m e a s u r a b l e parameters r e m a i n e d consistent, we collected n e m e r t i n e s in the a u t u m n of 1991 (October) and in the spring of 1992 (March). We d e t e r m i n e d their natural l e n g t h by allowing them to crawl along a ruler a n d r e a d i n g the l e n g t h w h e n they were fully relaxed (= 'relaxed' nemertines; see also Gibson & Young, 1976). As it proved to be a t i m e - c o n s u m i n g task to get the n e m e r t i n e s to crawl along the ruler a n d to be more or less relaxed, we a n a e s t h e t i z e d the n e m e r t i n e s in a 7.5 % MgC12-solution. After anaesthetizing the n e m e r t i n e s for about 10 minutes in the MgClzsolution we a g a i n m e a s u r e d their l e n g t h (= 'anaesthetized' nemertines) to establish a
Table 1. Classification of the reproductive stages of the hoplonemertine Amphiporus lactitloreus as recognizable in histological sections (6-8 ~tm thick) Stage
Term
Short description
0 1
undeveloped resting
2
maturing
3
mature
4
post-reproductive
No gonads visible in the section Gonads visible but still adhering close to the body wall; oocytes and spermatogonia visible Gonads visibly protruding into the body lumen; oocytes increasing in size, spermatocytes increasing in number Gonads filling most of the body lumen; oocytes and sperm densely packed in the gonads, gonopores opening Gonads empty, only very few gametes remaining in the gonad lumen; gonopores still opened
Martin Thiel & Thorsten D e r n e d d e
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Fig. 2. Mature female (bottom) and male (top) individuals of Amphiporus lactifloreus. During the reproductive period, the ovaries with the eggs and the testes are easily recognizable in the field with the naked eye or with the aid of a hand lens relationship b e t w e e n living a n d anaesthetized individuals. We then d e t e r m i n e d the wet weight, dry weight (after drying them for 3 clays at 80 ~ ash weight (muffle furnace for 4 hours at 510~ a n d ash-free-dry-weight (afdw = dry weight - ash weight). RESULTS R e p r o d u c t i v e s t a g e s a n d r e p r o d u c t i v e p e r i o d of A m p h i p o r u s lactifloreus
Amphiporus lactifloreus is dioecious. Females a n d males can be d i s t i n g u i s h e d in the field only during the reproductive period. The reproductive products of m a t u r e individuals can be seen through the body wall. Mature eggs have a g r e e n i s h - w h i t e a p p e a r a n c e , a n d the observer in the field can easily recognize b e t w e e n 4 to 10 m a t u r e eggs in one ovary (Fig. 2). Male gonads c o n t a i n i n g sperm appear white. The mature m a l e g o n a d s are heavily folded, a n d in the field the borders b e t w e e n individual testes c a n n o t be distinguished. Outside the reproductive period, males a n d females can only b e d i s t i n g u i s h e d b y histological examination. Animals collected b e t w e e n April a n d July sometimes had a bright o r a n g e or dark grey coloration, b u t the histological e x a m i n a t i o n of these individuals s h o w e d that they did not contain mature eggs or sperm. During the rest of the year the a n i m a l s a p p e a r e d greyish-white. In the histological sections, the gonads of n e m e r t i n e s that were in r e p r o d u c t i v e stage 1 (Table 1) were pressed close to the body wall. The intestinal l u m e n a n d the intestinal tissues occupied most of the body volume (Figs 3a, 4a). Gonads of females in stage 1 c o n t a i n e d previtellogenic oocytes (Fig. 3b). The n u c l e u s appears translucent, a n d chromosomes are visible (Fig. 3b). Up to 15 of t h e s e previtellogenic oocytes can be found in one section of an ovary. Gonopores can be r e c o g n i z e d in the sections, b u t their o p e n i n g to the outside is very narrow. D u r i n g the vitellogenic phase, the oocytes increase in size, the n u c l e u s is no longer translucent in sections, a n d
R e p r o d u c t i o n of Amphiporus lactifloreus
341
b
Figt 3. Cross sections of female Amphiporus lactifloreus, a: overview; b: ovary in stage I; c: ovary in stage 2; d: ovary with mature eggs. G gonads; g gonopores; I intestine; L lateral nerve cord; M longitudinal muscles; R rhynchocoel. Scale bar = 0.1 mm in a-d t h e o v a r i e s p r o t r u d e into t h e b o d y (stage 2 - Fig. 3c). A f t e r m a t u r a t i o n , o v a r i e s c o n t a i n i n g o o c y t e s a l m o s t c o m p l e t e l y o c c u p y t h e b o d y v o l u m e (stage 3 - Fig. 3d). Up to 5 m a t u r e o o c y t e s can b e s e e n in o n e section of an ovary. M a t u r e o o c y t e s are c o v e r e d b y a thin, h a r d layer, w h i c h is difficult to section a n d often c a u s e s artifacts in t h e s e c t i o n s (Fig. 3d). G o n a d s of m a l e s in s t a g e 1 c o n t a i n s p e r m a t o g o n i a (Fig. 4a). D u r i n g s p e r m a t o g e n e s i s the n u m b e r of s p e r m a t o c y t e s r a p i d l y i n c r e a s e s , a n d s u b s e q u e n t l y the g o n a d s e x t e n d into
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Martin Thiel & Thorsten Dernedde
Fig. 4. Cross sections of male Amptnporus lactifloreus, a: testes in s t a g e 1 (resting); b: t e s t e s in stage 2; c: testes w i t h m a t u r e s p e r m - s t a g e 3; d: e m p t y testes i m m e d i a t e l y after the r e p r o d u c t i v e period s t a g e 4. G g o n a d s ; g gonopores; I intestine; L lateral n e r v e cord. Scale b a r -- 0.1 m m in a - d
Reproduction of Amphiporus lactifloreus
343
~-~ stage 0
B
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D
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stage 1 stage 2
Number of nemertines
20
Aug
Oct 1992
Dec I I
Feb
April 1993
June
Fig. 5. Numbers of Amphiporus lactifloreus from the Nord-Sylter Wattenmeer in the respective reproductive stages during the 8 sampling periods. Stage 0 - undeveloped; stage 1 - resting; stage 2 - maturing; stage 3 - mature; stage 4 - post-reproductive. For further explanation see Table 1 the body cavity (stage 2 - Fig. 4b). W h e n spermiogenesis is completed (stage 3), the gonads occupy most of the body volume (Fig. 4c). After the reproductive period, empty gonads are visible in the sections a n d the gonopores, both in male and female individuals, are still open (stage 4 - Fig. 4d). Outside the reproductive period the c o l u m n a r cells of the intestine are filled with m a n y fat droplets (Figs 3b, 4a). During the reproductive period these c o l u m n a r cells may be completely empty (Figs 3c, 4c). Amphiporus lactifloreus has a clearly confined reproductive period in the NordSylter W a t t e n m e e r (Fig. 5). Maturation of the gonads does not b e g i n until August. In October 1992 almost all of the n e m e r t i n e s that were collected were in stage 2, a n d the ovaries and testes were m a t u r i n g (Fig. 5). At the e n d of N o v e m b e r (27th N o v e m b e r 1992) more than half of the n e m e r t i n e s that were collected contained fully mature gametes, a n d 7 of 24 n e m e r t i n e s had already released their reproductive products. By the e n d of J a n u a r y (31st J a n u a r y 1993), all of the n e m e r t i n e s had spawned, a n d the gonads were a g a i n in stage 1. B i o m e t r i c s of A m p h i p o r u s lactifloreus N e m e r t i n e s were found in all l e n g t h classes. Both sexes were r e p r e s e n t e d in all length classes more or less equally (Fig. 6), except in the class _< 20 mm, in which only
344
Martin Thiel & Thorsten Dernedde
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346
Martin Thiel & Thorsten D e r n e d d e
one male was found. M a l e A m p h i p o r u s lactifloreus w e r e in the majority b e f o r e the reproductive period, w h e r e a s females d o m i n a t e d after the reproductive p e r i o d (Fig. 6). In J a n u a r y 1993, the n u m b e r s in the different l e n g t h classes w e r e a l m o s t the s a m e as in N o v e m b e r 1992. Thus it can b e c o n c l u d e d that the majority of n e m e r t i n e s survived the reproductive period. B e t w e e n A u g u s t 1992 a n d J a n u a r y 1993, the distribution of nemertines in different l e n g t h classes indicates a cohort with a m o d a l size b e t w e e n 40 a n d 60 m m (Fig. 6). B e g i n n i n g in M a r c h 1993, this cohort s e e m e d to grow further, a n d in July 1993 most of the n e m e r t i n e s w e r e l o n g e r t h a n 60 mm. Both in N o v e m b e r I991 a n d M a r c h 1992, there was a strong correlation b e t w e e n the l e n g t h of the n e m e r t i n e s m e a s u r e d w h e n they w e r e crawling along t h e ruler u n d e r ' r e l a x e d ' conditions a n d their l e n g t h m e a s u r e d after b e i n g a n a e s t h e t i z e d (Fig. 7a). A significant relationship existed b e t w e e n the r e l a x e d l e n g t h a n d the w e i g h t - d a t a (ww, dw a n d afdw) of A. lactifloreus (Fig. 7b, c, d). No significant differences for a n y of the e x a m i n e d ' r e l a x e d ' l e n g t h - w e i g h t relationships w e r e found b e t w e e n the two s a m p l i n g dates of O c t o b e r 1991 a n d M a r c h 1992 (t-test; p > 0.05). However, t h e relationship b e t w e e n the l e n g t h of ' r e l a x e d ' a n d a n a e s t h e t i z e d n e m e r t i n e s c h a n g e d significantly after the r e p r o d u c t i v e p e r i o d (t-test; p < 0.02). The relationship b e t w e e n a n a e s t h e t i z e d length a n d wet w e i g h t also c h a n g e d significantly from October 1991 to M a r c h 1992 (t-test; p < 0.001), w h e r e a s the other l e n g t h - w e i g h t relationships (dw, afdw) u n d e r a n a e s t h e tized conditions did not c h a n g e in this time p e r i o d (p > 0.05). DISCUSSION R e p r o d u c t i v e p e r i o d of A m p h i p o r u s l a c t i f l o r e u s The h o p l o n e m e r t i n e A m p h i p o r u s lactifloreus in the W a d d e n Sea r e p r o d u c e s during the late autumn. This is in clear contrast to most other reports of the r e p r o d u c t i v e period of this species (McIntosh, 1873-74; Bfirger, 1897-1907; Franzen, 1956, 1983; Gibson, 1972). Bierne & Ru6 (1979), who also e x a m i n e d histological sections, f o u n d a r e p r o d u c tive p e r i o d in A. lactifloreus on the F r e n c h C h a n n e l coast that is similar to t h a t o b s e r v e d by us in the W a d d e n Sea. In April a n d J u n e of 1993 w e found individuals that m a t c h e d the colour description given by Gibson (1972) for A. lactifloreus d u r i n g t h e i r p r e s u m p t i v e r e p r o d u c t i v e period, b u t n o n e of our individuals r e v e a l e d m a t u r i n g or m a t u r e g o n a d s during the histological e x a m i n a t i o n (Fig 5). Individuals collected in N o v e m b e r 1992 c o n t a i n e d m a t u r e gonads. T h e y could clearly b e r e c o g n i z e d as m a t u r e i n d i v i d u a l s in the field with the n a k e d eye or with the aid of a h a n d lens. Interestingly, in n o n e of the abovem e n t i o n e d reports is a description of m a t u r e individuals given that m a t c h e s our observations. This l e a d s us to suspect that in most cases the r e p o r t e d r e p r o d u c t i v e p e r i o d of A. lactifloreus was not a c c u r a t e l y identified. M a t u r e individuals can easily b e r e c o g n i z e d in the field, p r o v i d i n g an easy tool for r e - e x a m i n i n g the reproductive p e r i o d of A. lactifloreus along the E u r o p e a n coasts. Most other n e m e r t i n e s from t e m p e r a t e r e g i o n s of the n o r t h e r n h e m i s p h e r e , for which r e p r o d u c t i v e d a t a are available, r e p r o d u c e d u r i n g the spring a n d s u m m e r m o n t h s (Fig. 8). The majority of n e m e r t i n e s are b e n t h i c predators, so it can b e a s s u m e d that developing j u v e n i l e s will find a b u n d a n t p r e y resources during the s u m m e r a n d e a r l y autumn. Very few n e m e r t i n e s other t h a n A. lactifloreus r e p r o d u c e during the a u t u m n (Friedrich,
Reproduction of A m p h i p o r u s lactifloreus
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-
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m
~
~
n
- -
Fig. 8. Reproductive periods of 53 nemertine species from the temperate regions of the northern hemisphere. Horizontal lines separate the different species from each other. Information from various geographical areas or different authors may be given for particular species (see also Fig. 1). Where several reports are available for one species, the thickness of the horizontal columns is decreased
1979). No unifying character can be identified a m o n g these different groups of nemertines which reproduce in a u t u m n . During the reproductive period a n d following it, high n u m b e r s of A. lactifloreus could be observed at the s e d i m e n t surface d u r i n g nocturnal low tides (Thiel, 1992; ThieI et al., 1995}. T h r o u g h o u t our observations a n d sample-collecting trips we f o u n d no indication of how A. lactifloreus r e p r o d u c t i o n might function. Some authors m e n t i o n that A. lactifloreus deposits fertilized eggs in a cocoon-like mass on the bottom w h e r e they u n d e r g o direct d e v e l o p m e n t (Thorson, 1950, 1957), whereas other authors report that the gametes are freely shed into the water c o l u m n (Bierne, 1983). Intensive field observations
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during n i g h t - t i m e low tides in N o v e m b e r are a p r o m i s i n g project that m a y s h e d more light on how r e p r o d u c t i o n functions in A. lactifloreus. L i f e - h i s t o r y of A m p h i p o r u s l a c t i f l o r e u s The h o p l o n e m e r t i n e Amphiporus lactifloreus is a very common intertidal n e m e r t i n e along E u r o p e a n coasts (Gibson, 1982). It feeds p r e f e r e n t i a l l y on a m p h i p o d s of the g e n u s Gammarus (Jennings & Gibson, 1969; M c D e r m o t t & Roe, 1985). A. lactifloreus can b e found in a g g r e g a t i o n s comprising s e v e r a l i n t e r m i n g l e d individuals within mussel clumps. Densities m a y be as h i g h as 250 i n d i v i d u a l s / m 2 within these m i c r o - h a b i t a t s (Thiel & Reise, 1993). The a v e r a g e food r e q u i r e m e n t of an adult individual A. lactifloreus was e s t i m a t e d from laboratory e x p e r i m e n t s to b e a b o u t 0.15 a m p h i p o d s / d a y (Thiel, 1992), a value w h i c h corresponds with v a l u e s p r o v i d e d by McDermott (1984, 1993) for a n o t h e r h o p l o n e m e r t i n e f e e d i n g on a m p h i p o d s of a size similar to those p r e y e d u p o n b y A. lactifloreus. The n e m e r t i n e A. lactifloreus has the c a p a c i t y to r e p r o d u c e several times in subseq u e n t reproductive periods, as can b e c o n c l u d e d from our data. To our k n o w l e d g e the p r e s e n t study is the first to show that a relatively small n e m e r t i n e species is iteroparous. We conclude that in the field A. lactifloreus can r e a c h an a g e of 2 years, b e c a u s e some individuals of the cohort that r e p r o d u c e d in N o v e m b e r 1992 persisted in t h e field until July 1993 (see Figs 5 a n d 6). The e x p l a n a t i o n s for A. lactifloreus r e p r o d u c i n g in a u t u m n r e m a i n speculative. G a m m a r i d a m p h i p o d s in the N o r d - S y l t e r W a t t e n m e e r and along the n o r t h e r n E u r o p e a n coasts reach their h i g h e s t densities in spring a n d a u t u m n (personal obs.). T h e r e p r o d u c tive period of A. lactifloreus i m m e d i a t e l y follows the period w h e n g a m m a r i d s r e a c h e d p e a k n u m b e r s in autumn. This l e a d s to the a s s u m p t i o n that food availability m a y be a factor influencing the timing of r e p r o d u c t i o n in A. lactifloreus. An alternative hypothesis w o u l d b e the l a c k of potential p r e d a t o r s of A. lactifloreus in its m i c r o - h a b i t a t d u r i n g a u t u m n a n d winter months. A. lactifloreus p r e f e r e n t i a l l y inhabits m u s s e l clumps on tidal flats a n d lives in large n u m b e r s u n d e r s m a l l rocks on rocky shores. The n e m e r t i n e shares this h a b i t a t with m a n y other i n v e r t e b r a t e s . Despite the w i d e s p r e a d notion that n e m e r t i n e s h a v e few or no enemies, shore c r a b s p r e y u p o n small n e m e r t i n e s (Gibson, pers. comm.; Thiel, 1992). Juvenile shore c r a b s (Carcinus maenas), w h i c h inhabit mussel clumps in l a r g e numbers, l e a v e this h a b i t a t d u r i n g the late fall (Thlel & D e r n e d d e , 1994). Thus, d u r i n g the winter, small j u v e n i l e s of A. lactifloreus w o u l d h a v e a relatively p r e d a t o r - f r e e h a b i t a t in mussel clumps. B i o m e t r i c s of A m p h i p o r u s l a c t i f l o r e u s M e a s u r e m e n t s of l e n g t h p r o v e d to b e a relatively useful tool for i n v e s t i g a t i n g the p o p u l a t i o n b i o l o g y of the n e m e r t i n e A. lactifloreus. Despite the fact that the size a n d s h a p e of n e m e r t i n e s are highly v a r i a b l e (Gibson, 1972, 1982; Riser, 1974), t h e i r l e n g t h is a g o o d a n d consistent m e a s u r e of their condition u n d e r both the ' r e l a x e d ' a n d a n a e s t h e tized condition, w h i c h is also true for the h e t e r o n e m e r t i n e Lineus viridis (Thlel, unpubl. data). In t h e n e m e r t i n e Nipponemertes pulcher, b o d y l e n g t h is a consistent m e a s u r e for the n u m b e r of eyes (Berg, 1972), a n d H e i n e et al. (1991) report the b o d y l e n g t h of
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Parborlasia corrugatus to be correlated with w e t weight. The study of Roe (1976) shows that l e n g t h m e a s u r e m e n t s of 'relaxed' n e m e r t i n e s are a good tool for tracking annual cohorts over various time periods. Gibson (1983) and Roe (1976) d e m o n s t r a t e d that 'body bulk' (length* m a x i m u m width) is a good m e a s u r e for w et weight. Figure 5 shows that with the help of the l e n g t h m e a s u r e m e n t s of 'relaxed' individuals, cohorts from different years can also be followed in the n e m e r t i n e A. lactifloreus. As l e n g t h m e a s u r e m e n t s of a n a e s t h e t i z e d individuals do not s e e m to be as consistent over time as those of 'relaxed' nemertines, we p r o p o s e the latter m e a s u r e for future studies on their population biology.
F u t u r e s t u d i e s o n t h e p o p u l a t i o n b i o l o g y of i n t e r t i d a l n e m e r t i n e s Ready access a n d the relatively high a b u n d a n c e s of n e m e r t i n e s found on the tidal flats invite studies on the population biology of intertidal species. Regular l e n g t h m e a s u r e m e n t s of n e m e r t i n e s promise to provide important information on the growth and survival of a n n u a l cohorts of nemertines. Furthermore, they will r e v e a l w h e t h e r the n e m e r t i n e u n d e r investigation is an annual species. Optical examinations of living s p eci m en s often allow a determination to be m a d e w h e t h e r individuals h a v e m a t u r e gonads, and w h e n c o m b i n e d with data from length m e a s u r e m e n t s , these data can indicate w h e t h e r it is an iteroparous or s e m e lp ar o u s nemertine, and w h e t h e r all m e m b e r s of the population p r o d u c e gametes. The most difficult p r o b l e m in future studies on the population biology of intertidal n e m e r t i n e s is to d e t e r m i n e the r e c r u i tm e nt process and the factors i n f l u en ci n g its success. Future studies should first focus on those species that produce cocoons, as in these species the small juveniles hatch directly from the cocoon, e.g. in L m e u s viridis (Bartolomaeus, 1984). Not surprisingly, L. viridis is one of the very few n e m e r t i n e s for wh i ch the j u v e n i l e habitat and d e v e l o p m e n t are known, but no data on j u v e n i l e growth and mortality are available at p r e s e n t (Cantell, 1989). Prime factors to be i n v e s t i g a t e d with respect to the recruitment success of n e m e r t i n e s should be the food of small juveniles, their susceptibility to potential predators, and the reproductive potential of the adult population. Our study shows that important life-history data of intertidal n e m e r t i n e s can be relatively easily o b t a i n e d without t i m e - c o n s u m i n g histological investigations. T h e s e data p r o v i d e the basic information n e c e s s a r y for a better u n d e r s t a n d i n g of i n t e r a n n u a l variations in n e m e r t i n e a b u n d a n c e and may s u b s e q u e n t l y help to u n d e r s t a n d the fluctuations in the a b u n d a n c e of their prey species.
Acknowledgements. We thank particularly R. Gibson who introduced us to the histological techniques used in this study, invited one of us to work for 2 months in his lab, and was always a source of important information. We thank K. Eckelbarger for allowing us to use the histology lab at the Darling Marine Center. Very special thanks go to S. Sampson for never losing patience when we bothered him with questions for help, material and technical advice. R. Gibson, K. Reise, P. Roe and S. Sampson commented on the manuscript. We are grateful to K. Reise and S. Lorenzen who gave initial advice and helped us to locate financial resources. Financial support was provided by the Federal Ministry for Research and Technology, by travel funds from the University of Kiel and the 'Universit6tsgesellschaft Kiel', and a fellowship grant by the Ministry of Education of SchleswigHolstein.
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