Aug 1, 1983 - C. aflmanni larvae occur mainly around the English and Irish coasts and are ..... 1814. Larval occurrence of H. varians was restricted during the ...
HELGOI.~NDER MEERESUNTERSUCHUNGEN Helgol~inder Meeresunters. 43, 87-112 (1989)
Seasonal occurrence and abundance of caridean shrimp larvae at Helgoland, German Bight Ingo S. Wehrtmann Universit~t Hamburg, Zoologisches M u s e u m und Zoologisches Institut ( A b t e i l u n g Crustacea); Martin-Luther-King-Platz 3, D-2000 H a m b u r g 13, Federal Republic of G e r m a n y
ABSTRACT: Plankton samples were collected from January 1985 to January 1986 three times per week at Helgoland to study seasonal occurrence and abundance of caridean shrimp larvae. A total of eleven species were obtained. Ninety-one % of all larvae collected during the sample period belonged to Crangon crangon L. and Crangon allmanni Kinahan, 6 % to Philocheras tn'spinosus Hailstone a n d 3 % to the remaining eight species. Collections were generally dominated by C. crangon larvae. However, C. allmanni larvae were most abundant in June coinciding with hatching activities of the population near Helgoland. C. allmanni was observed to have the highest density of all species with approximately 8 larvae per m 3. Larvae of Eualus occultus (Lebour), Eualus pusiolus (Kroyer), Hippolyte vanans Leach and Athanas nitescens Leach were most hkely released by populations inhabiting the rocky intertidal zone around Helgoland. The presence of Processa modica Williamson & Rochanaburanon and Processa nouveli holthuisi A1-Adhub & Williamson in the German Bight was verified by observations of a series of different developmental stages. Larvae of the rare species Caridion steveni Lebour were also recorded. The observed shrimp species were placed into three different groups with respect to their seasonal'occurrence. Possible advantages of the timing of larval dispersal relative to predation and food availability are given. The results on seasonal occurrence and relative abundance are discussed in relation to environmental factors (temperature, salinity) as wetl as to the geographical distribution of the species.
INTRODUCTION Larvae r e p r e s e n t the " n e g l e c t e d link" (Costlow & Bookhout, 1970} b e t w e e n g e n e r a tions of adult organisms. In order to i n v e s t i g a t e processes influencing an d d e t e r m i n i n g their population dynamics, it is not sufficient to focus only on the biology of the adults. The different d e v e l o p m e n t a l stages are i m po r t an t since they are r esp o n si b l e for the r ecr u i t m en t of populations, dispersal of species an d the colonization of n e w environments. A m o n g coastal and estuafine b e n t h i c species g e n e - f l o w can be limited by larval dispersal. H o w e v e r , pelagic i n v e r t e b r a t e l a r v a e can b e transported over long distances by o c e a n currents, resulting in a g e n e t i c e x c h a n g e b e t w e e n widely s e p a r a t e d p o p u l ations (Scheltema, 1975, 1986). Although, m o r e than 70 years ago, W e d e m e y e r (1912) p r o v i d e d information on the occurrence an d distribution of shrimps in the North Sea, c a r i d e a n shrimps i n h a b i t i n g the G e r m a n Bight h a v e largely b e e n ignored. H o w e v e r , there h a v e b e e n historical (Dallafc~Biologische Anstalt Helgoland, Hamburg
88
Ingo S. W e h r t m a n n
Torre, 1889; Schellenberg, 1928; Caspers, 1939) a n d r e c e n t studies (Janke, 1986) on shrimps that i n h a b i t the H e l g o l a n d r e g i o n w h i c h is the only rocky island in the Southern North Sea. O t h e r studies concerning the biology of these d e c a p o d s h a v e b e e n c o n d u c t e d along the Dutch coast (Holthuis, 1950; A d e m a et al,, 1982). Several i n v e s t i g a t i o n s h a v e b e e n carried out on the occurrence a n d distribution of d e c a p o d larvae in t h e N o r t h S e a (Rees, 1952, 1955; B a a n et al., 1972; S a n k a r a n k u t t y , 1975; Lindley, 1987}. It h a s b e e n d e m o n s t r a t e d that the p l a n k t o n from the southern r e g i o n of the North S e a in s u m m e r is c h a r a c t e r i z e d b y l a r g e quantities of d e c a p o d l a r v a e a n d fish l a r v a e (MSller, 1980}. Most studies on c a r i d e a n shrimps in the North Sea d e a l with the c o m m o n shrimp, Crangon crangon, d u e to its commercial value for the coastal fisheries of this region. This is true for the adults (for r e c e n t reviews on l a n d i n g a n d hfe cycle see, for e x a m p l e , Tiews, 1970, 1983; H e n d e r s o n & Holmes, 1987} as well as for their larvae. Descriptions of the different d e v e l o p m e n t a l stages m a i n l y o b t a i n e d from p l a n k t o n s a m p l e s (Kingsley, 1886; E h r e n b a u m , 1890; Williamson, 1901} a n d more r e c e n t l y by l a b o r a t o r y - r e a r e d l a r v a e are a v a i l a b l e (Gurney, 1982; Criales, 1985}. Studies on the s e a s o n a l occurrence a n d distribution of C. crangon l a r v a e in the G e r m a n Bight a n d a d j a c e n t estuaries w e r e carried out b y Kfihl & M a n n (1963a, 1963b, 1963c, 1968, 1969, 1971), Plett (1965} a n d EIss (1973}. H o w e v e r , information of shrimp l a r v a e other t h a n C. crangon for this part of the North Sea is still u n a v a i l a b l e . This study focuses on the s p e c i e s composition at H e l g o l a n d in o r d e r to confirm or e x t e n d the k n o w n g e o g r a p h i c a l distribution of different species. T h e results m a y serve as a b a s i s for further investigations d o c u m e n t i n g c h a n g e s in species composition a n d r e l a t i v e a b u n d a n c e . Based on a o n e - y e a r s a m p l i n g period, this p a p e r is the first of its k i n d to r e p o r t on the s e a s o n a l occurrence a n d relative a b u n d a n c e of different shrimp l a r v a e at H e l g o l a n d . MATERIAL AND M E T H O D S S a m p l e c o l l e c t i o n s a n d h a n d l i n g of m a t e r i a l D e p e n d i n g on the w e a t h e r conditions, s a m p l i n g was g e n e r a l l y c o n d u c t e d three times a w e e k n e a r H e l g o l a n d ( " H e t g o l a n d - R e e d e " ) from J a n u a r y 1985 to J a n u a r y 1986, n o r m a l l y in the morning' b e t w e e n 7 a n d 10 a.m. at one of the three stations s h o w n in Figure 1. A C A L C O F I - n e t ("California C o o p e r a t i v e O c e a n i c Fisheries Investigations") with a m e s h size of 500 ~tm was used. O b l i q u e tows w e r e t a k e n at stations with an a v e r a g e d e p t h of 10 meters. T h e n e t w a s e q u i p p e d with a flow meter. A n a v e r a g e w a t e r v o l u m e of a p p r o x i m a t e l y 75 m 3 p e r s a m p l e w a s filtered. However, d u e to t h e fluctuating n u m b e r s of shrimp l a r v a e during the different seasons, the filtered v o l u m e p e r collections r a n g e d from a p p r o x i m a t e l y 32 m 3 to 136 m 3. T e m p e r a t u r e a n d salinity w e r e m e a s u r e d at the surface. P l a n k t o n s a m p l e s w e r e c o n c e n t r a t e d a n d p r e s e r v e d in a b u f f e r e d solution of 4 % f o r m a l d e h y d e in s e a water. In the laboratory, all shrimp l a r v a e from the entire s a m p l e w e r e s o r t e d a n d c o u n t e d u n d e r a dissecting microscope. The d e t e r m i n a t i o n of the larval stages w a s carried out with a light microscope.
Caridean shrimp larvae a t Helgoland
I
I
I 9 Tonne
~
89
GERMAN
BIGHT
6
" "
,
Helgoland
~
*
....
54 ~ 11'"
.
1
= Kringe~
7'52.
'
0
~
~=,=====~
9 Sl3dhafen
'
~
500m ,
55'
Pig. 1. Location of the sample stations at Helgoland Identification of s h r i m p l a r v a e a n d their d e v e l o p m e n t a l s t a g e s Identification to the family level was performed using the key provided by Wflhamson (1957a). When available, larval descriptions of species and their developmental stages were consulted: Crangon crangon (Williamson, 1960; Gurney, 1982; Criales, 1985), Crangon allmanni (Williamson, 1960; Criales, 1985), Philocheras bispinosus (Wilhamson, 1960; Pike & Wilhamson, 1961a), Phflocheras trispinosus (Williamson, 1960; Pike & Wilhamson, 1961a), Eualus pusiolus and Eualus occultus (Wilhamson, 1957b; Pike & WiIhamson, 1961b), Processa modica and Processa nouveli holthuisi [Wilhamson & Rochanaburanon, 1979), Hippolyte varians (Sars, 1912; Lebour, 1931; Williamson, 1957b), Athanas nitescens (Sars, 1906; Webb, 1921; Lebour, 1932; WiUiamson, 1957b) and Caridion steveni (Lebour, 1930; Williamson, 1957b). For C. crangon and C. allmanni, no separation of different forms in each larval stage, as described by Criales (1985), was conducted. Pike & Williamson (1961a) differentiated between P. b. bispinosus and P. bispinosus neglectus, All larvae of this species identified in the present study belonged to P. b. bispinosus. No detailed larval descriptions (only for stage I and V) were available for P. trispinosus. Therefore, larval stages were distinguished by the development of the telson as described for P. Mspinosus (Pike & Williamson, 1961a). Identification of the first two stages of A. nitescens larvae was performed following descriptions by Webb (1921). All the other stages were identified using characteristics provided by Sars (1906) and Lebour (1932).
90
Ingo S. W e h r t m a n n RESULTS A N D D I S C U S S I O N Hydrography
T h e m o n t h l y a v e r a g e t e m p e r a t u r e s at H e l g o l a n d - R e e d e (Fig. 2) from J a n u a r y to April 1985 w e r e e x t r a o r d i n a r i l y cold c o m p a r e d with l o n g - t e r m m e a n t e m p e r a t u r e s from the s a m e a r e a (Reichard, 1910; G o e d e c k e , 1952, 1954; Weigel, 1976). The spring rise in t e m p e r a t u r e started in May. V a l u e s i n c r e a s e d t h r o u g h August, p e a k i n g a t 16.4 ~ a n d t h e n d e c r e a s e d t h r o u g h J a n u a r y 19869 O c t o b e r a n d N o v e m b e r w e r e c h a r a c t e r i z e d b y a r a p i d decline in temperature 9
o.o Saflmty 15
,..~~',.
- - Temperature
~
"* Long-term mean temperature ( 1 9 6 5 - 7 5 )
,"
,//
3z.
,~.
12 e
",
32 U~ 9 oa 13L
E a,
I.--
o.~ =
30 =---
6
28 0
i
l
J
F
J
i
i
l
J
!
i
N
A
N
J
J
A
S
,i
0
i
N
i
D
!
J
1985 - 1986
Fig. 2. Mean monthly temperatures and salinities during the sample period at Helgoland compared with long-term average temperatures, 1965-1975 (Weigel, 1976), from the same location The a v e r a g e monthly salinities did not exhibit a very clear p a t t e m (Fig. 2). However, d u r i n g w i n t e r the m e a n v a l u e w a s g e n e r a l l y h i g h e r t h a n in summer. T h e lowest m e a n v a l u e w a s in M a y (30.11%0), p r o b a b l y i n d i c a t i n g a fresh w a t e r i n p u t o r i g i n a t i n g from the a d j a c e n t rivers Elbe a n d Weser. In August, the salinity w a s fairly c o n s t a n t at 32.25 %o, while during most other months daily c h a n g e s w e r e observed.
Seasonal a b u n d a n c e of the collected species
Crangon crangon (Linnaeus, 1758) Seasonal occurrence started in early M a y 1985 (Fig,3)9 Larvae were found throughout the remainder of the entire sampling period, although very few were collected in the
91
C a r i d e a n shrimp l a r v a e at H e l g o l a n d
7.5
Crangon crangon All stages
6.0
4.5 O~ "O ~
> c
"O
3.0
1.5
0.0 MAY
JUN
JUL
AUG
SEP
OCT
NOV
DEC
JAN
1985-1986 Fig. 3. Concentration of Crangon crangon larvae and juveniles during the study period at Helgoland last two months ( D e c e m b e r 1985 a n d J a n u a r y 1986). Larvae w e r e v e r y c o m m o n from J u n e to S e p t e m b e r 1985 with p e a k a b u n d a n c e (approx. 7 larvae p e r m 3) in August. The p l a n k t o n s a m p l e s contained all larval stages as well as juveniles. H o w e v e r , the most a b u n d a n t l a r v a e w e r e in stage VII (Fig. 4) comprising 3 1 % of the total n u m b e r of C. crangon larvae. Stage I larvae h a d a distinct p e a k in June, while all o t h e r larval stages a n d juveniles r e a c h e d their m a x i m u m in A u g u s t (Fig. 5). Stage I l a r v a e a p p e a r e d for the first time in the p l a n k t o n in the s e c o n d w e e k of M a y 1985 w h e n w a t e r t e m p e r a t u r e r e a c h e d 7.8 ~ a n d i n c r e a s e d in n u m b e r s in M a y a n d J u n e with i n c r e a s i n g t e m p e r a t u r e . B e t w e e n A u g u s t 2 a n d 23 no s t a g e I larvae w e r e found, but t h e y occurred r e g u l a r l y until October 1985. T h e last stage I l a r v a e w e r e t a k e n in early D e c e m b e r at a t e m p e r a t u r e of 6.4 ~ The results of the present study concerning seasonal abundance of C. crangon larvae are generally in agreement with the findings of previous investigations (Table 1). K~ihl (1972) reported Crangon larvae occurring in the Elbe estuary from February to December. The late beginning of C. crangon occurrence at He]goland in 1985 may be explained by the extremely cold winter in 1984/1985 reported for the German coast of the North Sea (Koslowski, 1985) and by the resulting low temperatures in the first part of the year. After the exceptionally severe winter in 1962/1963, C. crangon larvae were not found in April 1963 probably due to low temperature of 4~ (Plett, 1965). However, plankton samples taken in April 1964 at temperatures between 4.0~ and 5.5 ~ contained shrimp larvae. Elss (1973) reported C. crangon larvae from April 1967 collected at
92
Ingo S. W e h r t m a n n
%
50 Crangon crangon
/~0 /-7
30 20 10
I
II
III
IV
V
VI
VII
JUV
Developmental stages Fig. 4. Crangon crangon. Percentage of larval stages and juveniles collected during the sample period at Helgoland (n = 5247)
t e m p e r a t u r e s b e t w e e n 6.6~ a n d 7.0~ After a mild winter in 1982, G e r d e s (1985) o b t a i n e d the larvae as early as M a r c h 1983 at an a v e r a g e t e m p e r a t u r e of 4.5 ~ Previous investigations on C. crangon l a r v a e in the G e r m a n Bight confirm the results of the p r e s e n t study concerning m a x i m u m concentration d u r i n g the s e a s o n a l occurrence: both Elss (1973) a n d Plett (1965) r e p o r t e d h i g h e s t d e n s i t y of the l a r v a e in August, while Kiihl & M a n n (1963a) o b t a i n e d p e a k a b u n d a n c e in the Elbe estuary in J u n e . In the North Sea, p l a n k t o n samples collected in S e p t e m b e r c o n t a i n e d the h i g h e s t n u m b e r of C. crangon l a r v a e (Lindley, 1987). Contrary to the p r e s e n t study, Rees (1952) o b s e r v e d a m a x i m u m of larval a b u n d a n c e in January. H o w e v e r , those d a t a m a y not b e r e p r e s e n t a tive, as t h e y are b a s e d u p o n only 150 l a r v a e collected within three years. M a x i m u m n u m b e r s of C. crangon larvae collected in I 9 8 5 - 8 6 w e r e relatively high c o m p a r e d with other results from the Southern N o r t h Sea; Lindley (pets. comm.) f o u n d a m a x i m u m concentration of 1 larva p e r m 3 in April 1981 a n d S e p t e m b e r 1983. The difference in time b e t w e e n the first p e a k of a b u n d a n c e of s t a g e I a n d II was 7 days (Fig. 6), which r e p r e s e n t s the duration of d e v e l o p m e n t of s t a g e I . . T h e m e a n t e m p e r a t u r e in this p e r i o d w a s 11.0~ T h e s e field d a t a are in good a g r e e m e n t with l a b o r a t o r y studies on larval stage d e v e l o p m e n t in C. crangon b y Criales & A n g e r (1986). T h e y e x p r e s s e d the n u m b e r of larval moults (M) as a function of both t e m p e r a t u r e (T; ~ a n d time of d e v e l o p m e n t (D; days): M = 0.00584 9 D
9 T 1'347
Based on the 1985 field d a t a (T = 11.0~ M = 1), the e s t i m a t e d larval d e v e l o p m e n t (D) using this equation w a s also a p p r o x i m a t e l y 7 days.
C a r i d e a n s h r i m p l a r v a e at H e l g o l a n d %
Crangon
%
crangon
~
60 Stage 1
LO 20 0 60
Stage
93
9
~
StageV
60
, L0
20
II
StogeVl
aO 20
20
0
StageIII
60'
CDF
0 50
.
StageVll
i
20
~ z:~;~/-~7 StageIV
./--7[~
0 Juvenile LO
20'
2()
~2~ MAY JUN JUL AUG SEP OCT NOV DEC JAN MAY JUN JUL AUG SEP OCT NOV DEC JAN
Fig. 5. Crangon crangon. Seasonal occurrence of larval stages, and juveniles during the sample period at Helgoland (n = 5247). The values of all bars for each developmental stage add up to 100 %, representing the total number of collected larvae and juveniles per stage during the study period
Table I. Seasonal occurrence of C. crangon larvae in the North Sea based upon the findings of different authors Author (year)
Location
Lebour (1947) Rees (1952) Jorgensen (1923} Thorson {1945} Kfihl & Mann (1963a} Kfinne (1952} Lindley (1987) Present study
British coast North Sea British coast Danish coast Elbe estuary German Bight North Sea Helgoland
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec X X
X X
X X
-
X X
X X
X X
X X X
X X X X X X X X
X X X X X X X X
X X X X X X X X
X X X X X X X X
X
X
X
X
X X X X X X
X X X X X
X X X X
X X X
94
Ingo S. Wehrtmann
1"00 I
Crangon crangon
Stage I 0 75
% 0.50 q~
..J
0.25
0.00
JUN
MAY 1.8
JUL
AUG
SEP
OCT
NOV
DEC
JAN
Crangon crangon 1.5
%
Stage I1
1.2
0.9 o
0.6
0.3
0:0
i
MAY
I
JUN
JUL
AUG
SEP
OCT
NOV
DEC
1985-1986 Fig. 6. Crangon crangon. Concentration of stage I and II larvae at Helgoland
JAN
Caridean shrimp larvae at Helgoland
95
The findings of the present study on larval abundance of stage I (Fig. 6) suggest that there have been at least two main hatching periods in 1985 at Helgoland. The first period extending from early May to early August and the second from late August until October. The absence of newly hatched larvae during the first three weeks in August supports the separation of these hatching periods. Crangon crangon populations around England spawn normally twice per annum (Meredith, 1952; Henderson & Holmes, 1987). For the German Bight, Tiews (1954) reported three spawning periods at Bfisum and observed very few egg-carrying females during September and October. However, the data of the present study do not allow a decision concerning the number of broods at Helgoland. Furthermore, the offshore sample station is not a favourable area for the common shrimp. According to Tiews (1970), C. crangon prefers Wadden Sea areas, especially highly productive estuaries with strong tidal movements of brackish water masses.
Crangon allmanni Kinahan, 1857 Larvae of C. allmanni were found in the plankton samples at Helgoland from May to September 1985 with a distinct peak in June (Fig. 7). In this month, 63 % of the total number of larvae occurred, while only 1% was obtained in May and September and 25 % and 10 % in July and August, respectively. Maximum concentration was observed in the second half of June with approximately 8 larvae per m 3.
8 Crangon allmanni All stages
6
% Q. 4 "0 > -o o ~
. m
0 MAY
JUN
JUL
AUG
SEP
OCT
NOV
DEC
JAN
1985-1986 Fig. 7. Crangon allmanni Concentration of. larvae and juveniles during the sample period at Helgoland
96
Ingo S. W e h r t m a n n
All d e v e l o p m e n t a l s t a g e s i n c l u d i n g j u v e n i l e s were collected. H o w e v e r , a p r e d o m i n a n c e of the first three s t a g e s comprising a p p r o x i m a t e l y 82 % of the total n u m b e r was o b s e r v e d (Fig. 8). Stage I l a r v a e w e r e collected from m i d - M a y to the e n d of August, r e a c h i n g p e a k a b u n d a n c e at t h e e n d of J u n e with a p p r o x i m a t e l y 6 l a r v a e p e r ms. The r a n g e of t e m p e r a t u r e in w h i c h the stage I l a r v a e w e r e collected w a s 9.4 ~ to 16.3 ~ All larvae t a k e n in M a y w e r e either in s t a g e I or II, while 54 % of the C. allmanni l a r v a e in J u l y a n d A u g u s t w e r e s t a g e III. P e a k occurrence of stage IV was in J u n e a n d July. Stage V r e a c h e d a distinct p e a k in A u g u s t that r e p r e s e n t e d more t h a n 60 % of t h e total l a r v a e of that stage. The older d e v e l o p m e n t a l s t a g e s a n d juveniles occurred from l a t e J u n e to early September.
% 60
Crangon allmanni
f-7
/-,0 20 I I
J
I
II
Ill
IV V Vl VII Developmental stages
VIII
JUV
Fig. 8. Crangon allmanni. Percentage of larval stages and juveniles collected during the sample period at Helgoland (n = 1682) Due to their similarity, l a r v a e of C. crangon a n d C. allmanni h a v e often not b e e n s e p a r a t e d (e.g. Baan et al. 1972; W e b e r , 1984); d e t a i l e d information on the l a r v a l p h a s e of C. allmanni is sparse. The results c o n c e r n i n g seasonal occurrence of C. allrnanni confirm g e n e r a l l y the findings of p r e v i o u s studies (Rees, 1952; Allen, 1960; Lindley, 1987). P e a k a b u n d a n c e of C. allmanni l a r v a e in the North Sea occur in M a y / J u n e (Allen, 1960; Lindley, 1987). In the Danish W a d d e n S e a area, Thorson (1946) r e p o r t e d the l a r v a e b e t w e e n m i d - A p r i l a n d late June. It is n o t e w o r t h y that in most of the studies on C. allmanni cited a b o v e , the p e r i o d of larval occurrence extends t h r o u g h S e p t e m b e r . This m a y b e e x p l a i n e d b y t h e p a t t e r n of reproduction; in both a r e a s of the Dutch coast (Creutzberg & L e e u w e n , 1980) a n d off the N o r t h u m b e r l a n d coast (Allen, 1960) C. allmanni has a b r e e d i n g s e a s o n from D e c e m b e r to July. In autumn, no e g g - b e a r i n g females w e r e found. The m a x i m u m c o n c e n t r a t i o n of C. allmanni l a r v a e (8 s p e c i m e n s p e r m 3) r e p r e s e n t s the h i g h e s t d e n s i t y of all species o b t a i n e d d u r i n g the study period. Lindley (pets. comm.) o b t a i n e d a c o n s i d e r a b l y lower concentration of these l a r v a e in the S o u t h e r n North Sea with a m a x i m u m of 1.3 l a r v a e p e r m 3 in J u l y 1983. The complete larval d e v e l o p m e n t (until stage VIII) of C. aflmanni r e q u i r e s approxim a t e l y 46 days at a t e m p e r a t u r e of 12 ~ (Criales, 1985; Criales & A n g e r , 1986). In the p r e s e n t study, the first s t a g e I l a r v a e occurred on M a y 15 a n d stage VIII l a r v a e w e r e first
C a r i d e a n shrimp larvae at H e l g o l a n d
97
o b t a i n e d on July 26 at an a v e r a g e t e m p e r a t u r e of 11.2~ The time difference b e t w e e n the occurrence of t h e s e two stages is 46 days, w h i c h r e p r e s e n t s exactly the findings from the r e a r i n g experiments, even t h o u g h the w a t e r t e m p e r a t u r e at H e l g o l a n d v a r i e d from 8.1 ~ a n d 14.2~ during the six w e e k s . C. aflmanni larvae occur m a i n l y a r o u n d the English a n d Irish coasts a n d are u n c o m m o n in the e a s t e r n part of the North S e a (Lindley, 1987). T h e only k n o w n p o p u l a t i o n of C. alImanni in the G e r m a n Bight is l o c a t e d n e a r H e l g o l a n d (Caspers, I939). The p r e d o m i n a n c e of the first larval stages (Fig. 8) indicates a h a t c h i n g a r e a of this species. T h e h a t c h e d l a r v a e w e r e p r o b a b l y t r a n s p o r t e d a w a y from t h e p a r e n t p o p u l a t i o n by the current system. Because of the low a b u n d a n c e of larvae in a d v a n c e d d e v e l o p m e n tal stages, it s e e m s unlikely that recruitment to the p o p u l a t i o n n e a r H e l g o l a n d is exclusively by larvae. There m a y also be an immigration of j u v e n i l e s a n d adults from other parts of the North Sea. Observations from other Crangon p o p u l a t i o n s c o n c e r n i n g a n n u a l migrations (Alien, 1960, 1966; Boddeke, 1975, 1976) a n d r e s t o c k i n g of p a r e n t populations b y i m m i g r a t i o n of animals (Sandifer, 1975) support this hypothesis.
Philocheras bispinosus (Hailstone, 1835) Larval occurrence of this species e x t e n d e d from July to D e c e m b e r with a p e a k in August, S e p t e m b e r a n d O c t o b e r (Fig. 9). In D e c e m b e r , the p l a n k t o n s a m p l e s c o n t a i n e d very few larvae, while in J a n u a r y 1986 no P. bispinosus larvae w e r e taken. T h e r a n g e of w a t e r t e m p e r a t u r e s in which these larvae w e r e found was 7.3 ~ to 16.4 ~ M a x i m u m
1.2
Philocheras bispinosus All s t a g e s 0.9
E r 0.6 ..(D > . m
t0.3
0.0 MAY
JUN
JUL
AUG
SEP
OCT
NOV
DEC
JAN
1985-1986 Fig. 9. Philocheras bispinosus. Concentration of the larvae and the juveniles during the sample period at Helgoland
98
Ingo S. W e h r t m a n n
concentration w a s a p p r o x i m a t e l y 1 l a r v a e p e r m 3 in early October. S t a g e V w a s most a b u n d a n t , comprising m o r e t h a n 40 % of the collected P. bispinosus l a r v a e (Fig. 10). In genera/, the n u m b e r of collected larvae i n c r e a s e d with d e v e l o p m e n t a l s t a g e . However, only few j u v e n i l e s w e r e found b e t w e e n the e n d of O c t o b e r a n d m i d - N o v e m b e r . Larvae in s t a g e I occurred from July to early N o v e m b e r , a n d s p e c i m e n s in the last d e v e l o p m e n t a l s t a g e w e r e t a k e n b e t w e e n the e n d of J u l y a n d m i d - D e c e m b e r .
%
60
Philocheras bispinosus
/-7 z.O
20
I
II
III IV V Developmental stages
JUV
Fig. 10. Philocheras bispinosus. Percentage of larval stages and juveniles collected during the
sample period at Helgoland (n = 479) Several other investigators h a v e n o t e d P. bispinosus l a r v a e from the p l a n k t o n ; larvae occurred rather late in the year, a n d p e a k a b u n d a n c e has b e e n found b e t w e e n Sept e m b e r a n d N o v e m b e r (Thorson, 1946; Rees, 1952, 1955; Lindley, 1987). P. bispinosus l a r v a e in the Adriatic Sea are p r e s e n t the w h o l e y e a r in low a b u n d a n c e , r e a c h i n g the m a x i m u m in J a n u a r y (Kurian, 1965). At the s o u t h - w e s t e r n coast of Portugal, P. bispinosus larvae occur from October to March, in June, July a n d S e p t e m b e r (Paula, 1987). A p r e d o m i n a n c e of older larval s t a g e s in the Danish W a d d e n Sea is d o c u m e n t e d b y Thorson (1946).
Philocheras trispinosus (Hailstone, 1835) Figure 11 shows that larvae w e r e not n u m e r o u s but w e r e r e g u l a r l y t a k e n b e t w e e n m i d - J u l y a n d early November. The p e a k in J a n u a r y 1986 r e p r e s e n t s o n e juvenile. M a x i m u m concentration with a p p r o x i m a t e l y 0.1 l a r v a e p e r m 3 w a s in e a r l y October. P. trispinosus l a r v a e r e a c h e d p e a k a b u n d a n c e in A u g u s t a n d a g a i n in October. The
C a r i d e a n shrimp l a r v a e at H e l g o l a n d
99
0.10
Philocheras trispinosus All s t a g e s
0.08
0.06 I
-o 9 > "o t. m
0.04
I
0.02
m
i
0.00 MAY
9 _ JUN
'
1/ JUL
I/A 1 .
9
AUG
1
SEP
--
OCT
9
J
H
1
NOV
DEC
JAN
1985-1986
Pig. 11, Philocheras trispinosus. Concentration of larvae and juveniles during the sample period at Helgoland l a r v a e collected in A u g u s t a n d O c t o b e r c o m p r i s e d more than 70 % of the total n u m b e r of P. trispinosus larvae. Only l a r v a e in s t a g e s III, IV a n d V w e r e found, with s t a g e V b e i n g most a b u n d a n t (Fig. 12). Hitherto, no information on larval occurrence of P. trispinosus from the G e r m a n Bight has b e e n available. Baan et al. (1972) found Philocheras-larvae in the Southern North Sea n e a r "Texel" lightship from July to January, b u t did not distinguish b e t w e e n P. bispinosus a n d P. tfispinosus. However, the authors stated that the majority of the collected s p e c i m e n s b e l o n g e d to the postlarval s t a g e of P. trispinosus. Lindley (1987) o b s e r v e d the larvae of this species in the North Sea in July a n d August, a n d in the a r e a of the English C h a n n e l from July to December 9 M a x i m u m a b u n d a n c e in t h e English C h a n n e l occurred in A u g u s t followed b y the major p e a k in N o v e m b e r . Information c o n c e r n i n g seasonal occurrence of P. trispinosus larvae in the Mediterraz,ean Sea a n d the coast of Portugal has b e e n p r o v i d e d b y Labat (1984} a n d Paula (1987), respectively.
Eualus pusiolus (Kroyer, 1844) The few collected l a r v a e of this species found within the s a m p l e p e r i o d occurred from m i d - J u n e to July. A p p r o x i m a t e l y 0.2 larvae p e r m 3 r e p r e s e n t e d the m a x i m u m concentration o b s e r v e d in m i d - J u l y (Fig. 13). A p p r o x i m a t e l y 80 % of the total n u m b e r of the collected E. pusiolus l a r v a e b e l o n g e d to stages I a n d II. The larvae w e r e c a p t u r e d over a t e m p e r a t u r e r a n g e of 11.5 ~ to 15.5 ~ T h e a v e r a g e t e m p e r a t u r e d u r i n g the occurrence of E. pusiolus l a r v a e w a s 13.8~ T h e r e h a v e b e e n no previous records from
Ingo S. Wehrtmann
100
%
Philocheras trispinosus
80
/--7
50
40 20 0 I
II
III
IV
JUV
V
Developmental stages Fig. 12. Phflocheras tdspinosus. Percentage of larval stages and juveniles collected during the sample period at Helgoland (n = 53)
0.25
Eualus pusiolus All stages
0.20 E 13.
0.15
"O
0.10 "O
0.05
0.00
.
.
.
.
.
.
.
.
MAY JUN
.
.
.
JUL
.
AUG
.
.
SEP
.
.
OCT
.
.
NOV
.
DEC
JAN
1985-1986 Fig, 13. Eualuspusiolus. Concentration of larvae during the sample period at Helgoland (n = 30)
Caridean shrimp larvae at Helgoland
i01
E. pusiolus at Helgoland. However, during the study period several adult specimens were collected near Helgoland. On March 6th 1986 an egg-bearing female was caught in Helgoland Harbour. These findings, as well as the predominance of the first two larval stages indicate that a population of E. pusiolus is located around Helgoland and that the study region represents a hatching area for this shrimp. Larval occurrence extends in both the Irish Sea and the Firth of Clyde from February to August or September (Pike & Williamson, 1961b). IAndley (1987) reported E. pusiolus larvae from the Irish Sea and the English Channel in February and May, respectively. These results may indicate an earher hatching period of E. pusiolus larvae around the Atlantic coast of Great Britain and Ireland than at Helgoland, probably due to the generally higher temperature in early spring. June and July represent the beginning of the planktonic period of E. pusiolus larvae in the German Bight, indicated by the presence of newly hatched larvae. This may explain the difference in the length of seasonal occurrence compared with other studies (Bull, 1939; Pike & Wilhamson, 1961b). Eualus occultus (Lebour, 1936) Figure 14 shows the seasonal occurrence of E. occultus larvae, starting in the second half of July and ending in early October. The majority of the larvae were collected in August (58 %) and September (39 %), while in July and October oniy 7 % and 2 % were taken, respectively. During the occurrence of g. occultus larvae the temperature varied from 14.5 ~ to 17.0 ~ with a mean temperature of 15.5 ~ Larval abundance was always
0.35 Eualus occultus 0.30
All stages
0.25 Q.
0.20
m
"a , m
0.15
"o
c
0.10 0.05 00C
,-
MAY
'
. . . . . . . . . .
JUN
JUL
AUG
SEP
OCT
NOV
DEC
JAN
1985-1986 Fig. 14. Eualus occultus. Concentration of larvae and juveniles during the sample period at Helgoland
102
Ingo S. Wehrtmann
low and reached maximum density in late August (ca 0.3 larvae per m3). Except stage V, all developmental stages and juveniles occurred during the sample period at Helgoland (Fig. 15). The older stages were found earlier (from mid-June) than the y o u n g e r ones, which were taken from August to October.
% 80 Eualus occultus
60 Z.O 20 0
I
II
III
IV V VI VII Developmental stages
VIII
IX
JUV
Fig. 15. Eualus occultus. Percentage of larval stages and juveniles collected during the sample period at Helgoland (n = 103) Due to their similarity, adult E. occultus and Thoralus cranchii (Leach) have often been confused. In contrast, larvae of these species can'be easily distinguished by a pair of lateral spines on the 5th abdominal somite, which occurs only in T. cranchii larvae (Lebour, 1936; Pike & Williamson, 1961b). Recently, Janke (1986) p r o v i d e d the first information of adult E. occultus from the rocky intertidal at Helgoland. This record can be supported by four a d u l t s p e c i m e n s which were collected by other investigators during the sample period from test panels at Helgoland Harbour as well as by the presence of their larvae. The presence of older stages of E. occultus followed by the later occurrence of younger stages indicates an immigration of the advanced stages from other places, where the hatching period started earlier than in the German Bight. The p a r e n t population of these larvae may be located in the English Channel or the Irish Sea. Processa modica Williamson & Rochanaburanon, 1979
Larvae of this shrimp occurred from mid-June to early November (Fig. 16). They were never numerous with p e a k concentration observed on August 12 of approximately 0.1 larvae per m 3. P. modica larvae were first caught when the temperature increased in 1985 to 15-16~ larvae reached p e a k abundance in August (58 %). More t h a n 80 % of all larvae occurred in August and September, with 12 % in July and the remainder in October and November. All larval stages were found at Helgoland (Fig. 17). Larvae in stages I to IV were collected from July to September, and the older stages were obtained from August to November.
C a r i d e a n shrimp l a r v a e at H e l g o l a n d
103
0.12
Processa rnodica 0,10 e~
E
All stages
0.08
Q.
0.06 -I
t- 0.04
0.02
0.00
,
,
MAY
JUN
JUL
AUG
SEP
A
OCT
,
NOV
9
DEC
JAN
1985-1986 Pig. 16. Processa modica. Concentration of larvae during the sample period at Helgoland
%
Processa m o d i c a
LO
20 0
"'--~ I
II
III
IV
V
VI
VII
Larval stages Pig. 17. Processa modica. Percentage of larval stages collected during the sample period at Helgoland (n = 36) A m o n g other locations, W i l h a m s o n & R o c h a n a b u r a n o n (1979) r e p o r t e d P. m o d i c a larvae from the Southern North Sea, r a n g i n g from the D o g g e r Bank to the coast of the N e t h e r l a n d s a n d Belgium. The p r e s e n c e of all larval stages n e a r H e l g o l a n d indicates that the distribution of this shrimp in the S o u t h e r n North Sea e x t e n d s the r a n g e g i v e n b y W i l h a m s o n & R o c h a n a b u r a n o n (1979}. P. m o d i c a l a r v a e h a v e b e e n r e p o r t e d from the Irish Sea from July to O c t o b e r (Williamson & R o c h a n a b u r a n o n , 1979}, a n d Lindley (1987)
104
Ingo S. W e h r t m a n n
o b t a i n e d the l a r v a e in different a r e a s of the North Sea in July, A u g u s t a n d N o v e m b e r , in g o o d a g r e e m e n t with the p r e s e n t study. Processa nouveli holthuisi A I - A d h u b & Wilh'amson, 1975 On two occasions (October 9 a n d 28), P. n o u v e l i holthuisi larvae w e r e t a k e n from the p l a n k t o n n e a r Helgoland. T h e a v e r a g e t e m p e r a t u r e in O c t o b e r was 14.0 ~ Overall, two l a r v a e in s t a g e V a n d two l a r v a e in s t a g e VII w e r e found. Little information concerning s e a s o n a l a n d g e o g r a p h i c a l distribution of P. nouvefi holthuisi l a r v a e exists. In the Irish Sea, R o c h a n a b u r a n o n & Williamson (1976) collected ovigerous females from F e b r u a r y to S e p t e m b e r . Larvae h a v e b e e n h a t c h e d in the laboratory in M a r c h a n d l a t e r months a n d w e r e p r e s e n t in the p l a n k t o n until late S e p t e m b e r . Lindley (1987) found P. nouveli holthuisi larvae in the North S e a , b u t not in the G e r m a n Bight. Seasonal o c c u r r e n c e e x t e n d e d from J u n e to S e p t e m b e r . Larvae of P. nouvefi holthuisi can b e r e a r e d successfully from h a t c h i n g to m e t a m o r phosis at 15 ~ a n d 20 ~ ( R o c h a n a b u r a n o n & Williamson, 1976). The t i m e to m e t a m o r phosis a v e r a g e s a b o u t 49 d a y s at 15~ (Williamson & R o c h a n a b u r a n o n , 1979). In the p r e s e n t work, a d v a n c e d l a r v a e w e r e o b t a i n e d in October, indicating that l a r v a l d e v e l o p m e n t took p l a c e in A u g u s t a n d S e p t e m b e r . T h e s e months, including July, w e r e characterized b y the h i g h e s t m e a n t e m p e r a t u r e s during the s a m p l e p e r i o d (Fig. 2). R o c h a n a b u r a n o n & Williamson (1976) c o n c l u d e d from their laboratory e x p e r i m e n t s that m a n y P. nouveli holthuisi l a r v a e m u s t hatch in the Irish Sea at t e m p e r a t u r e s in which their chances of survival are e x t r e m e l y low, a l t h o u g h the l a r v a e p r o b a b l y d e v e l o p as well b e l o w o p t i m u m t e m p e r a t u r e conditions. T h e c o m p a r a b l y low t e m p e r a t u r e s d u r i n g s e a s o n a l occurrence of P. nouveli holthuisi at H e l g o l a n d m a y explain the l o w n u m b e r s of collected larvae. FIippolyte varians Leach,. 1814 Larval occurrence of H. varians was restricted during the study p e r i o d from the e n d of O c t o b e r to early N o v e m b e r . The s p e c i m e n s (n = 11) w e r e collected at t e m p e r a t u r e s r a n g i n g from 9.7 ~ to 13.5 ~ T h e s a m p l e s n e v e r c o n t a i n e d more t h a n 0.05 l a r v a e p e r m s. Only l a r v a e in stages III a n d IV w e r e found. Previous studies r e p o r t e d H. varians l a r v a e from the North Sea t h r o u g h o u t the year, a n d in a d v a n c e d d e v e l o p m e n t a l s t a g e s b e t w e e n A u g u s t a n d J a n u a r y (Baan et al., 1972). A l t h o u g h the results p r o v i d e d b y Rees (1952) are only b a s e d u p o n 45 H. varians l a r v a e collected d u r i n g the s a m p l e p e r i o d from 1947-49, t h e y d o c u m e n t larval o c c u r r e n c e from July to J a n u a r y with p e a k a b u n d a n c e in October. Lindley (1987) o b t a i n e d l a r v a e in the North Sea in A u g u s t a n d N o v e m b e r . A t h a n a s n i t e s c e n s Leach, 1814 Larvae of A. nitescens w e r e rarely collected n e a r H e l g o l a n d (n = 6). T h e y occurred b e t w e e n m i d - A u g u s t a n d e a r l y S e p t e m b e r within a t e m p e r a t u r e r a n g e of 14.7 ~ to 17.0 ~ M a x i m u m concentration of 0.05 l a r v a e p e r m 3 (all in s t a g e V) was o b s e r v e d at t h e e n d of August. Larvae in s t a g e II, IV, a n d VIII as well as juveniles w e r e r e c o r d e d . In good a g r e e m e n t with the p r e s e n t study, Paula (1987) o b t a i n e d m a x i m u m concent.ration of A. n i t e s c e n s l a r v a e in A u g u s t a n d S e p t e m b e r on the Portuguese A t l a n t i c coast. However, no r e c e n t studies on larval o c c u r r e n c e of A. nitescens in the N o r t h Sea are
Caridean shrimp larvae at Helgoland
105
available. Lebour (1947) noted them in the inshore plankton of Plymouth b e t w e e n June and October, coincident with findings concerning larval occurrence of A. n i t e s c e n s near the Danish coast (Thorson, 1946) and in the Baltic Sea (K~indler, 1961). Tambs-Lyche (1962) explained the distribution of adult A. n i t e s c e n s in Scandinavian waters as a possible transportation from the Enghsh Channel along the continental coast by the general current patterns; this may also be true for their larvae. However, Schellenberg (1928) and more recently Janke (1986), reported adult A. nitescens from Helgoland. Candion steveni Lebour, 1930 On August 16, 1985 one single larva in stage IX was collected. The temperature was 16.6 ~ Information on geographical distribution of C. steveni was given by O'Ceidigh & McGarth (1981). Based on one larva obtained at Helgoland by Hagmeier (unpublished), it was suggested that C. s t e v e n i must occur around this island (Lebour, 1930). This assumption can now be confirmed by the present larval record as well as by the observation of two C. steveni larvae in the last larval stage collected by the author on August 1, 1983 at Helgoland. In the Adriatic Sea, C. s t e v e n i larvae occur from May to November, but only in low numbers (Kurian, 1965) which corresponds with the results from the Mediterranean Sea (Bourdillion-Casanova, 1960; Vives, 1966). Lebour (1947) reported the larvae from the Enghsh Channel appearing in the plankton from April to June and in October, but never in numbers. Recently, Lindley (1987) collected C. s t e v e n i larvae in June in the western entrance of the English Channel, and Paula (1987) found them in May at water temperatures between 14 ~ and 15 ~ at the south-western coast of Portugal.
General s p e c i e s c o m p o s i t i o n Planktonic stages representing 11 species of caridean shrimps were identified in the present study. The absence of any species does not necessarily imply that it does not occur in the plankton near Helgoland. It must be stressed that the results of the present paper are restricted to a one-year samphng period. Further studies in successive years may show a different species composition. However, Crangon larvae are assumed to be the most abundant shrimp species in the plankton community at Helgoland. Crangon larvae were by far the most abundant specimens, comprising more than 90 % of the total numbers of the collected larvae during the sample period (Fig. 18). Their predominance was expected due to the proximity of the sample station to W a d d e n Sea areas, the preferred habitat for the common shrimp, C. crangon. However, C. aHmanni larvae were also remarkably abundant especially in June. In this month, approximately 53 % of all Crangon larvae belonged to C. allmanni. Furthermore, the highest density of any species during the entire sample period (approximately 8 individuals per m 3) was of C. allmanni larvae in mid-June. These findings can be explained by the proximity of the C. aflmanni population near Helgoland. The number of larval shrimp species near Helgoland can be compared with previous investigations conducted in the North Sea. During a sample period of 6 years near the Dutch coast, larvae of only 8 shrimp species were obtained (Baan et al., 1972). Recently, Lindley (1987) reported 14 species of caridean shrimp larvae collected by the Continuous
106
Ingo S. W e h r t m a n n
HELGOLAND ~ ~ /////// Crangon crangon
othesrpece is .,so,nosu oinosus
%
Crangon allmanni
Fig. 18. Percentage of the predominant shrimp larvae obtained during the sample period (January 1985 until January 1986) at Helgoland (n = 7697) Plankton Recorder from 5 s t a n d a r d a r e a s r e p r e s e n t i n g the m i d d l e a n d s o u t h e r n p a r t of the North Sea. The h i g h e r n u m b e r of species found b y Lindley (1987) m a y b e d u e to a l o n g e r s a m p h n g p e r i o d (3 y e a r s c o m p a r e d with one y e a r at H e l g o l a n d ) a n d a w i d e r g e o g r a p h i c a l s a m p l i n g area, including the Enghsh Ch'annel w h i c h r e p r e s e n t s a zoogeographical connection to the Atlantic fauna. Lebour (1947) also found m o r e s p e c i e s in the p l a n k t o n n e a r Plymouth during the y e a r s 1940-45. Due to the inshore s a m p l e station, she collected species typical for rivers a n d estuaries, while at H e l g o l a n d no s t r o n g influence of b r a c k i s h w a t e r m a s s e s can b e observed. Larvae of two more s p e c i e s w e r e e x p e c t e d to b e found n e a r H e l g o l a n d : both Pandalus montagui Leach a n d Pandalina brevirostn's (Rathke) h a v e b e e n r e p o r t e d for H e l g o l a n d (Schellenberg, 1928; Caspers, 1939; Holthuis, 1950). The a b s e n c e of P. montagui l a r v a e m a y b e d u e to s e a s o n a l migrations (Mistakidis, 1957; S i m p s o n et al., 1970; S t e v e n s o n & Pierce, 1985) a n d / o r to a n n u a l fluctuations in larval o c c u r r e n c e as o b s e r v e d in different shrimps (Baan et al., 1972). However, in F e b r u a r y 1986 females with e g g s w e r e collected n e a r H e l g o l a n d ("Tiefe Rinne") a n d the h a t c h i n g l a r v a e w e r e r e a r e d in the laboratory. Furthermore, on M a r c h 21, 1986 one single P. montagui larva w a s o b t a i n e d from the plankton. T h e s e observations s u g g e s t that P. montagui l a r v a e should b e a d d e d to the list of species occurring n e a r Helgoland. More t h a n 50 adult s p e c i m e n s of P. brevirostris were collected b e t w e e n O c t o b e r 1985 a n d M a r c h 1986 n e a r H e l g o l a n d ("Tiefe Rinne"). However, the s a m p l e s n e v e r c o n t a i n e d females with eggs. Allen (1965) found some e v i d e n c e of migration to a n d from d e e p e r w a t e r at t h e b e g i n n i n g a n d at the e n d of the b r e e d i n g season. Further s t u d i e s a r e n e e d e d to d e t e r m i n e w h e t h e r H e l g o l a n d r e p r e s e n t s a hatching a r e a for P. brevirostris.
C a r i d e a n shrimp larvae at H e l g o l a n d
107
The c o m p a r a t i v e l y h i g h n u m b e r of species of shrimp l a r v a e at H e l g o l a n d is b a s e d on the special biotope a r o u n d this island: H e l g o l a n d is s u r r o u n d e d b y the only rocky intertidal zone in the G e r m a n Bight with its typical flora a n d fauna (Liining, 1970; Janke, 1986). Pucus a n d Laminaria species r e p r e s e n t the p r e f e r r e d h a b i t a t for m a n y different shrimps, e . g . E , pusiolus, E. occultus, H. varians a n d A. nitescens (Smaldon, 1979), which could e x p l a i n the larval occurrence of t h e s e four species in the studied area. General relative abundance
and seasonal occurrence
A total of 7697 shrimp larvae w e r e collected during the study p e r i o d at Helgoland. Most l a r v a e (2960) w e r e o b t a i n e d in August. However, m e a n concentration of larvae, b a s e d on the s a m p l e s w h i c h c o n t a i n e d specimens, was h i g h e s t in J u n e 1985 with a p p r o x i m a t e l y 5 l a r v a e p e r m 3 (Table 2). H i g h e s t relative a b u n d a n c e w a s o b s e r v e d on J u n e 21, w h e n ca 70 % of the collected s p e c i m e n s b e l o n g e d to C. aflmanni, the majority Table 2. Mean larval concentration with standard deviation (larvae per m 3) between May 1985 and January 1986 at Helgoland, excluding samples without shrimp larvae
1985-86 May Jun Jul Aug Sap Oct Nov Dec Jan
Larval concentration (larvae per m 3) ~ 4- SD Minimum 0.20 5.46 1.49 3.50 2.10 0.30 0.17 0.03 0.01
0.20 4.54 1.24 2.11 2.33 0.37 0.23 0.02 0.01
0.06 0.49 0.22 0.64 0.03 0.02 0.01 0:01 0.01
Maximum
0.55 11.24 3.48 8.33 7.62 1.38 0.67 0.04 0.02
to s t a g e I. Due to the low n u m b e r of s a m p l e s in this month (5 c o m p a r e d with 13 in July a n d 12 in A u g u s t a n d October, respectively}, the n u m b e r of the collected shrimp l a r v a e w e r e lower than in the following 3 months. No c o m p a r a b l e d a t a for the G e r m a n Bight or Southern North Sea are available. However, Rees (1955} found m a x i m u m n u m b e r s of d e c a p o d larvae in the S o u t h e r n North Sea during the years 1949-51 b e t w e e n J u n e a n d S e p t e m b e r ; 1950 was c h a r a c t e r i z e d b y d e c r e a s e d n u m b e r s of l a r v a e in July, w h i l e p e a k a b u n d a n c e was o b t a i n e d in J u n e a n d August, w h i c h is in a g r e e m e n t with the results of the p r e s e n t study (Table 2). Furthermore, the majority of d e c a p o d crustaceans in the North Sea reaches p e a k larval a b u n d a n c e in June, August, a n d S e p t e m b e r ; only two species h a d highest concentration in July (Lindley, 1987). However, S a n k a r a n k u t t y (1975} o b t a i n e d p e a k a b u n d a n c e of d e c a p o d larvae in two w e s t - n o r w e g i a n fjords in July/August. T e m p e r a t u r e is p r o b a b l y one of the most important factors in affecting the hfe a n d survival of m e r o p l a n k t o n i c organisms. T h e relationship b e t w e e n t e m p e r a t u r e a n d incubation p e r i o d in d e c a p o d crustaceans has b e e n s t u d i e d b y W e a r (1974}. Rees (1952} a n d Lindley (1987) discussed the influence of t e m p e r a t u r e on distribution a n d s e a s o n a l
108
Ingo S. Wehrtmann
occurrence of decapod larvae. The effects of food and salinity on development of decapod larvae have been we]] documented (e.g. Broad, 1957; Rochanaburanon & Wilhamson, 1976; Sulkin & Norman, 1976; Criales & Anger, 1986). Table 3. Seasonal peak abundance of the shrimp larvae occurring near Helgoland, based on the present data Species Jan-Jul C. aflmanni
E. pusiolus E. occultus P. rnodica C. crangon A. nitescens C. steveni P. bispinosus P. trispinosus H. vaxians P. nouveli holthuisi
Peak Abundance Jul-Sept
Oct-Dec
X X X X X X X
X X X X
Concerning their peak of abundance during the sample period, shrimp species collected near Helgoland can be placed into three different groups (Table 3). As expected, peak abundance of most of the shrimp larvae occurred between July and September, which is in accordance with various field studies on seasonal occurrence of decapod Iarvae (Lebour, 1947; Rees, 1952, 1955; Lindley, 1987; Paula, 1987). Due to the relatively high water temperatures during this period; larvae have a reduced development time and a rapid growth. Experimental studies conducted with various decapod larvae showed decreased larval development time with increasing temperatures (e.g. Costlow & Bookhout, 1969; Sandifer, 1973; Dawirs, 1979, 1985; Anger, 1983; Criales & Anger, 1986). However, the chance for larvae to survive pelagic predation is lower than in early spring or at the end of the year (Creutzberg & Leeuwen, 1980). Due to rapid development, the main settlement of juvenile shrimps is hkely to take place during the time of the year which represents the most advantageous period for the remainder of their hfe span, so that the survival rate will probably be enhanced during winter. The main hatching activities of C. a l l m a n n i and E. p u s i o l u s occurred in spring, indicating a preference for lower temperatures. Laboratory experiments with C. a l l m a n n i larvae (Criales & Anger, 1986) support these findings; however, corresponding data for E. p u s i o l u s larvae are not available. The results of the present study showed a well separated period of larval abundance in the two E u a l u s species found at Helgoland. The end of the seasonal occurrence of E. p u s i o l u s coincided with the beginning of the occurrence of E. o c c u l t u s larvae. The difference may suggest different reproductive strategies and/or different temperature preferences of these two closely-related species. But again, it must be considered that the results are only based on a one-year study. The advantage of an early hatching period may be explained b y diminishing numbers of pelagic predators within this season (Creutzberg & Leeuwen, 1980; Boddeke,
Caridean shrimp larvae at H e l g o l a n d
109
1982) due to the low temperatures. W h e n a d e q u a t e provision of suitable food organisms is available, larvae can m e t a m o r p h o s e in s u m m e r an d can grow rapidly. This e n h a n c e s the survival rate in winter and provides t h e m a g o o d start in the following spring. Th e third group r e a c h e d their p e a k a b u n d a n c e b e t w e e n October and D e c e m b e r , a period characterized by decreasing t e m p e r a t u r e s n e a r H e l g o l a n d (Fig. 2). Th e larval occurrence of the four species g i v e n in T a b l e 3 indicates late h a t c h i n g activities an d a tolerance of low t e m p e r a t u r e s during larval d e v e l o p m e n t . Th e findings of seasonal o c c u r r e n c e r e g a r d i n g P. bispinosus, P. trispinosus an d H. varians coincide with observations from several authors (Lebour, 1947; Rees, 1952; Lindley, 1987; Paula, 1987} who g e n e r a l l y obtained these larvae rather late in the year. So far, laboratory studies describing the p r e f e r r e d t e m p e r a t u r e r a n g e for t h ese three species of caridean shrimp larvae h a v e not b e e n conducted. It is assumed, that P. nouve11 holthuisi does not fall into this group, although larvae occurred in October, b u t t h e y w e r e in a d v a n c e d d e v e l o p m e n tal stages. Species in this group benefit also from the d i m i n i s h e d n u m b e r of p el ag i c predators. On the other hand, low t e m p e r a t u r e s will prolong the d e v e l o p m e n t a l duration a n d / o r will p r e v e n t further larval d e v e l o p m e n t [e.g. n e i t h er C. crangon nor C. aflmanni can be r e a r e d successfully from hatching to m e t a m o r p h o s i s at 6~ (Criales & Anger, 1986}]. It m a y b e that in the winter the mortahty rate within t h e third group is h i g h e r than in the others. Furthermore, p r e d o m i n a n t s e t t l e m e n t of j u v e n i l e shrimps falls into a period of low t e m p e r a t u r e s w h ic h represents a physiological u n f a v o r a b l e t e m p e r a t u r e regime.
Acknowledgements. This paper is based on a thesis submitted in partial fulfillment of the requirements for the Diploma at the University of Hamburg. I am very grateful for the advice and support from my advisor, Prof. Dr. G. Hartmann, University of Hamburg. I wish to thank the Biologische Anstalt Helgoland, especially Prof. Dr. H.-P. Bulnheim, Dr. G. Uhlig, and Dr. K. Anger, for laboratory space and working facilities. K. Treutner and P. Mangelsdorf of the Biologische Anstalt Helgoland allowed me to use their unpublished oceanographic data. Thanks are also due to Dr. K. D. Hammer {University of Hamburg) and Dr. G. Kattner {Alfred-Wegener-Institut ffir Polar- und Meeresforschung} for their assistance with computer work. Dr. T. Bianchi (Institute of Ecosystem Studies) as well as Prof, A. Dittel (Universidad de Costa Rica) and lE. Rutherford (University of Maryland) gave valuable comments on the manuscript. Helpful suggestions were also given by anonymous referees.
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