Hyas araneus - Helgoland Marine Research

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This would be supported by similar observations by Pandian & Schumann ... linear regression can be calculated to express the relationship between D and t ( ...
HELGOL~NDER MEERESUNTERSUCHUNGEN Helgol~inder M e e r e s u n t e r s u c h u n g e n 34, 287-311 (1981)

Influence of starvation on the larval d e v e l o p m e n t of H y a s a r a n e u s (Decapoda, Majidae)* K. A n g e r I & R. R. D a w i r s 2 I Biologische A n s t a l t H e l g o l a n d (Meeresstation); D-2192 Helgoland, Federal R e p u b l i c o f G e r m a n y 2 Zoologisches Institut der Universit~t Kiel; Olshausenstral]e 40-60, D-2300 K i e l 1, Federal R e p u b l i c of G e r m a n y

ABSTRACT: The influence of starvation on larval d e v e l o p m e n t of the spider crab Hyas araneus (L.) was studied in laboratory experiments. No larval stage suffering from continual lack of food had sufficient energy reserves to reach the next instar. Maximal survival times were observed at four different constant temperatures (2°, 6 °, 12° and 18 °C). In general, starvation resistance d e c r e a s e d as temperatures increased: from 72 to 12days in the zoea-1, from 48 to 18 days in the zoea-2, and from 48 to 15 days in the m e g a l o p a stage. The length of maximal survival is of the same order of magnitude as the duration of each instar at a given temperature. "Sublethal limits" of early starvation periods were investigated at 12 °C: Zoea larvae must feed right from the b e g i n n i n g of their stage (at high food concentration) and for more than one fifth, approximately, of that stage to have at least some chance of surviving to the next instar, i n d e p e n d e n t of further prey availability. The minimum time in which e n o u g h reserves are accumulated for successfully completing the instar without food is called "point-of-reserve-saturation" (PRS). If only this m i n i m u m period of essential initial feeding precedes starvation, d e v e l o p m e n t in both zoeal stages is delayed and mortality is greater, w h e n compared to the fed control. Starvation periods b e g i n n i n g right after hatching of the first zoea cause a prolongation of this instar and, surprisingly, a slight shortening of the second stage. The delay in the zoea-1 increases proportionally to the length of the initial fasting period. If more than approximately 70 % of the maximum possible survival time has e l a p s e d without food supply, the larvae become unable to recover and to moult to the second stage even w h e n re-fed ("point-of-no-return", PNR). The conclusion, b a s e d on own observations and on literature data, is that initial feeding is of paramount importance in the early d e v e l o p m e n t of planktotrophic decapod larvae. Taking into account hormonal and other d e v e l o p m e n t a l processes during the first moult cycle, a general hypothesis is proposed to explain the key role of first food uptake as well as the response pattern of the zoea-1 stage to differential starvation periods.

INTRODUCTION M e r o p l a n k t o n i c l a r v a e h a v e p a r t i c u l a r s i g n i f i c a n c e as a link b e t w e e n p e l a g i c a n d b e n t h i c c o m m u n i t i e s ( C o s t l o w & B o o k h o u t , 1970). T h e i r s u r v i v a l , m a i n l y c o n t r o l l e d b y f o o d l i m i t a t i o n s , t e m p e r a t u r e , a n d p r e d a t i o n , is t h e p r i n c i p a l k e y for u n d e r s t a n d i n g v a r i a t i o n s i n r e c r u i t m e n t a n d e s t a b l i s h m e n t of b e n t h i c m a r i n e c o m m u n i t i e s ( T h o r s o n , 1946, 1966). * Contribution to research project "Experimentelle Marine Okosystemanalyse" sponsored by Bundesministerium f/.ir Forschung und TechnoIogie, Bonn (Grant No. MPU-0328/1). © Biologische Anstalt Helgoland

0174-3597/81/0034/0287/$ 02.00

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T h e r e is s o m e e v i d e n c e that t h e a m o u n t of s u i t a b l e p l a n k t o n i c food organisms, a v a i l a b l e d u r i n g this critical period, c a n limit t h e size of y e a r classes in fish a n d d e c a p o d p o p u l a t i o n s (for r e c e n t d i s c u s s i o n see Paul et al., 1979). This is not u n l i k e l y , since the authors o b s e r v e d a l o w e r t h r e s h o l d for successful d a i l y f e e d i n g r e s p o n s e in l a r v a e of t h r e e different d e c a p o d species. This t h r e s h o l d w a s m u c h h i g h e r t h a n a v e r a g e z o o p l a n k ton c o n c e n t r a t i o n s in t h e s e a (cf. also Omori, 1979). A n u m b e r of other authors also r e p o r t e d u n n a t u r a l l y h i g h food d e n s i t i e s as o p t i m a l for l a b o r a t o r y r e a r i n g of several d e c a p o d s p e c i e s (e.g. T e m p l e m a n , 1936; S a n d o z & Rogers, 1944; Reeve, 1969; Brick, 1974; Knowlton, 1974; Mootz & Epifanio, 1974; Roberts, 1974; W e l c h & Sulkin, 1974; P r o v e n z a n o et al., 1976; Bigford, 1978; J o h n s & P e c h e n i k , 1980). It m a y b e a r g u e d that the m o s t c o m m o n l y ' u s e d diet, Artemia salina, w h i c h is not a n a t u r a l p r e y organism, m i g h t b e q u a l i t a t i v e l y inferior to n a t u r a l p r e y items. H o w e v e r , it is w e l l s u i t e d to support p l a n k t o t r o p h i c d e v e l o p m e n t in m a n y d e c a p o d s p e c i e s in the laboratory, w h e r e a s n a t u r a l z o o p l a n k t o n is g e n e r a l l y at l e a s t two o r d e r s of m a g n i t u d e less c o n c e n t r a t e d in the sea, a n d m u c h of its b i o m a s s is not a v a i l a b l e to c r u s t a c e a n larvae, b e c a u s e p o t e n t i a l p r e y o r g a n i s m s m a y h a v e a n u n s u i t a b l e size, quality, s w i m m i n g s p e e d , d e f e n s e m e c h a n i s m or other c h a r a c t e r i s t i c s p r e v e n t i n g p r e d a t i o n (cf. H e r r n k i n d , 1968; Roberts, 1974; S u l k i n & H e u k e l e m , 1980). A l t h o u g h T h o r s o n (1950) " e x p e c t e d t h a t most p e l a g i c l a r v a e l i v i n g u n d e r n a t u r a l c o n d i t i o n s w o u l d starve", t h e e c o l o g i c a l factor " s t a r v a t i o n " has not r e c e i v e d m u c h a t t e n t i o n as o p p o s e d to a b i o t i c v a r i a b l e s such as t e m p e r a t u r e , salinity, o x y g e n etc. The fact that r e c r u i t m e n t in b e n t h i c c o m m u n i t i e s d o e s t a k e p l a c e d e s p i t e a p r e s u m a b l e chronic l a c k of food, c a n b e e x p l a i n e d b y t h e c o m b i n a t i o n of two p h e n o m e n a : the e x i s t e n c e of c o n s i d e r a b l e p a t c h i n e s s in p l a n k t o n (for r e v i e w s e e e. g. Parsons et al., 1977) a n d a d a p t a t i o n m e c h a n i s m s for s u r v i v a l u n d e r h i g h l y f l u c t u a t i n g resources. I k e d a (1974, 1977 a n d e a r l i e r papers), M a y z a u d (1973, 1976), a n d H o l l a n d (1978) r e p o r t e d on physi o l o g i c a l a n d b i o c h e m i c a l c h a n g e s d u r i n g s t a r v a t i o n conditions. H o w e v e r , not m u c h i n f o r m a t i o n exists a b o u t u l t i m a t e limits of s t a r v a t i o n r e s i s t a n c e in c a r n i v o r o u s z o o p l a n k ton, a n d e v e n less a b o u t a d a p t i o n to t e m p o r a r y l a c k of s u i t a b l e prey. S t a r v a t i o n w a s r e c o g n i z e d v e r y e a r l y as a factor s e v e r e l y i n f l u e n c i n g d e v e l o p m e n t of fish l a r v a e (for r e v i e w s e e May, 1974; Ehrlich et al., 1976), b u t h a r d l y a n y t h i n g is k n o w n a b o u t its s i g n i f i c a n c e for o t h e r m e r o p l a n k t o n o r g a n i s m s . In s e v e r a l c u l t i v a t i o n e x p e r i m e n t s w i t h d e c a p o d larvae, starvation w a s u s e d to test t h e sufficiency of y o l k r e s e r v e s for l a r v a l d e v e l o p m e n t . T h e s e e x p e r i m e n t s r e v e a l e d a c o n s i d e r a b l e specific v a r i a t i o n in the d e g r e e of d e p e n d e n c e on prey, e s p e c i a l l y a m o n g N a t a n t i a larvae. B e s i d e s a n u m b e r of s p e c i e s w h i c h p o s i t i v e l y n e e d food d u r i n g their w h o l e l a r v a l d e v e l o p m e n t , t h e r e a r e others w h i c h are a b l e to c o m p l e t e at l e a s t parts of t h e i r p e l a g i c p h a s e i n d e p e n d e n t of food (Broad, 1957; Dobkin, 1971 a n d a n u m b e r of e a r l i e r p a p e r s ; Regnault, 1969; F i e d l e r , 1970; Foxton & Herring, 1970; C h o u d h u r y , 1971; Omori, 1971, 1979; G r e e n w o o d et al., 1976). S i m i l a r i n s t a n c e s h a v e b e e n r e p o r t e d in A n o m u r a , e s p e c i a l l y in l a t e l a r v a l s t a g e s (Coffin, 1958; Bookhout, 1964, 1972; Rice & Provenzano, 1965; Provenzano, 1968a; S c h a t z l e i n & Costlow, 1978; Dawirs, 1980). In B r a c h y u r a larvae, r e s e r v e s a r e u s u a l l y not sufficient to a l l o w d e v e l o p m e n t u n d e r s t a r v a t i o n conditions. O n e e x c e p t i o n w a s r e p o r t e d b y P r o v e n z a n o & Brownell (1977) a n d b y B r o w n e l l et al. (1977) for t h e t r o p i c a l s p i d e r c r a b Mithrax spinosissimus, but not e n o u g h d e t a i l s on the m e t h o d s w e r e g i v e n to e v a l u a t e its significance. W e a r (1967)

Starvation i n H y a s a r a n e u s larvae

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described a n d r e v i e w e d cases of aberrant, more or less direct d e v e l o p m e n t i n some Brachyura from N e w Z e a l a n d a n d Australia. Those larvae mostly subsist o n yolk reserves. The p o t e n t i a l to resist starvation not o n l y d e p e n d s o n the species a n d o n the particular larval stage considered, b u t also o n e n v i r o n m e n t a l variables. T h e most important factor controlling m e t a b o l i s m a n d thus, the rate of reserve utilization, is temperature. However, its effect is b y no m e a n s clear. In the few e x p e r i m e n t s w h i c h have b e e n carried out, results are equivocal: In some cases, survival time u n d e r starvation increases with d e c r e a s i n g t e m p e r a t u r e (Rice & Provenzano, 1966; Gore, 1968; Regnault, 1969), i n other i n s t a n c e s there is the opposite t r e n d (Rice & Provenzano, 1965; Provenzano, 1967; Gore, 1970} or survival time is i n d e p e n d e n t of t e m p e r a t u r e over a wide r a n g e (Gore, 1972} or shows a m a x i m u m at a n i n t e r m e d i a t e t e m p e r a t u r e (Provenzano, 1968b). In the literature r e v i e w e d above, only survival u n d e r l o n g - t e r m starvation was considered. Those i n v e s t i g a t i o n s as well as r e a r i n g e x p e r i m e n t s u n d e r more or less optimal food conditions provide the extreme e n d s of the scale, in w h i c h n a t u r a l developm e n t of decapod larvae must be expected. The next step toward u n d e r s t a n d i n g merop l a n k t o n survival a n d d e v e l o p m e n t d u r a t i o n in a v a r i a b l e e n v i r o n m e n t is the search for " s u b l e t h a l limits" a n d " s u b l e t h a l effects" of starvation. T h e e x i s t e n c e of i n t e r n a l d e v e l o p m e n t a l processes d u r i n g each stage (see e.g. Costlow & Sastry, 1966; F r e e m a n a n d Costlow, 1980} a n d the h i g h p r o b a b i l i t y of o n l y short-term a b s e n c e of s u i t a b l e prey, together s u g g e s t that such s u b l e t h a l effects must occur i n n a t u r e a n d that their k i n d a n d extent d e p e n d o n the time w h e n starvation takes p l a c e a n d h o w 1 o n g it lasts. There are a few references to such effects: Kurata (1959), Y a t s u z u k a (1962), M o d i n & Cox (1967), a n d Kon {1979} o b s e r v e d a p a r t i c u l a r l y critical period i n the very b e g i n n i n g of larval life i n decapods: if first f e e d i n g was delayed, growth a n d survival of the larvae were lowered. Paul & Paul (1980) o b s e r v e d i n k i n g crab zoeae a s i g n i f i c a n t l y d e c r e a s i n g ability to catch prey after early starvation. S u b l e t h a l effects of fasting periods on b e h a v i o u r patterns were also reported (Burton, 1979; C r o n i n & Forward, 1980}. The p r e s e n t work is the first a t t e m p t to a n a l y z e systematically not only the u l t i m a t e limits of starvation resistance, b u t also the s u b l e t h a l effects of early lack of food on later viability a n d d e v e l o p m e n t d u r a t i o n i n a m a r i n e i n v e r t e b r a t e : i n larvae of the spider crab H y a s a r a n e u s . These larvae are c o m m o n i n the p l a n k t o n of the G e r m a n Bight from midw i n t e r . u n t i l early summer. T h e i r d e v e l o p m e n t in this area p r e s u m a b l y lasts ca. 12 to 16 w e e k s (Anger & Nair, 1979); the w i d e g e o g r a p h i c d i s t r i b u t i o n of H . a r a n e u s (cf. Christiansen0 1971) is p r o b a b l y r e l a t e d to this long p e l a g i c p h a s e (Thorson, 1961: " l o n g d i s t a n c e larvae"). Since H . a r a n e u s b e l o n g s to the most c o m m o n species in the waters a r o u n d the Island of H e l g o l a n d (North Sea), it is one of the subjects i n v e s t i g a t e d w i t h i n a joint research project (Anger & Nair, 1979). The questions on w h i c h this study c o n c e n t r a t e d were: (1) Does a n y larval stage of H. a r a n e u s u n d e r starvation possess sufficient e n e r g y reserves to survive a n d to m o u l t successfully to the next stage at a n y ecologically r e l e v a n t t e m p e r a t u r e ? If not: (2) W h a t is the order of m a g n i t u d e i n the m a x i m a l survival time, a n d h o w strong is the i n f l u e n c e of e n v i r o n m e n t a l t e m p e r a t u r e on starvation resistance? (3) How long, at least, m u s t a n early larva feed well, u n t i l it has a c c u m u l a t e d e n o u g h reserves to m o u l t successfully to the next stage (in w h i c h it m i g h t get the c h a n c e to switch to some n e w k i n d of prey)? How is survival a n d d e v e l o p m e n t time affected i n this case?

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(4) Is t h e r e a " p o i n t - o f - n o - r e t u r n " (sensu Blaxter & H e m p e l , 1963) after w h i c h s t a r v e d l a r v a e c a n n o t recover, w h e n re-fed? If so: H o w close is this point to m a x i m a l s u r v i v a l t i m e u n d e r starvation? (5) W h i c h effects do e a r l y starvation p e r i o d s exert on l a t e r d e v e l o p m e n t d u r a t i o n a n d on viability, w h e n a p p l i e d at different t i m e s w i t h i n the first z o e a l stage? A r e t h e r e p a r t i c u l a r l y s e n s i t i v e p e r i o d s w i t h i n this stage? T h e t e r m i n o l o g y u s e d in this p a p e r follows that of W i l l i a m s o n (1969). T h e m i s l e a d i n g t e r m " p o s t l a r v a " , w h i c h mostly refers to the m e g a l o p a (clearly a larval stage), but s o m e t i m e s to j u v e n i l e stage, is not used; it should be g e n e r a l l y a v o i d e d (see also Wear, 1967). T h e t e r m " s t a g e " a l w a y s refers to an instar (zoea 1, z o e a 2, m e g a l o p a , first crab), not to a unit of t h e m o u l t cycle.

MATERIAL AND METHODS Obtaining

the larvae

In J a n u a r y 1979 a n d 1980, o v i g e r o u s f e m a l e s w e r e d r e d g e d from a d e p t h of ca. 30 to 50 m off t h e i s l a n d of H e l g o l a n d (North Sea) a n d t h e r e a f t e r m a i n t a i n e d in a laboratory r e c i r c u l a t i n g system. T h e s e a w a t e r h a d a t e m p e r a t u r e of 2 °C a n d a salinity of ca. 33 Too. W h e n t h e first h a t c h i n g p r e z o e a e w e r e o b s e r v e d , the f e m a l e r e l e a s i n g l a r v a e w a s p l a c e d in a f l o w - t h r o u g h a q u a r i u m (ca. 5 1, w a t e r t e m p e r a t u r e ca. 6 °C). T h e l a r v a e w e r e c o l l e c t e d in a s i e v e s t a n d i n g in a s e c o n d a q u a r i u m a n d r e c e i v i n g the w a t e r from the o v e r f l o w of the first one. In this w a y it w a s a s s u r e d that all z o e a e u s e d in an e x p e r i m e n t o r i g i n a t e d from t h e s a m e m o t h e r a n i m a l a n d h a t c h e d the s a m e d a y (within m a x i m a l l y 6 h). Experiments

on maximal starvation resistance

For all e x p e r i m e n t s , freshly h a t c h e d zoea-1 s t a g e l a r v a e (Z-l) w e r e p i p e t t e d indiv i d u a l l y into n u m b e r e d vials c o n t a i n i n g ca. 15 to 20 ml of filtered s e a w a t e r (Millipore m e m b r a n e filter, 0.4 #m pore size) w i t h a salinity of ca. 33 Too. I n d i v i d u a l c o n f i n e m e n t w a s necessary, since A n g e r & Nair (1979) h a v e s h o w n that o t h e r w i s e c a n n i b a l i s m or n e c r o p h a g y s e v e r e l y falsify s u r v i v a l t i m e s u n d e r starvation. Sets of 50 or 100 larvae e a c h (100 only at 12°C) w e r e p l a c e d into t e m p e r a t u r e - c o n t r o l l e d rooms, w h e r e they a c c l i m a t i z e d w i t h i n a f e w hours to t h e e x p e r i m e n t t e m p e r a t u r e s : 2 °, 6 °, 12 ° a n d 18 °C. T h e e x p e r i m e n t s w e r e c h e c k e d daily at the s a m e time; w a t e r w a s c h a n g e d r e g u l a r l y e v e r y o t h e r day. S e v e r a l h u n d r e d z o e a e w e r e r e a r e d at 12 °C to l a t e r s t a g e s u s i n g the s a m e t e c h n i q u e of i n d i v i d u a l m a i n t e n a n c e as d e s c r i b e d above, b u t f e e d i n g a m i x t u r e of Brachiomls plicatilis a n d freshly h a t c h e d Artemia salina n a u p l i i ad l i b i t u m (ratio ca. 10 : 1, ca. 50 to 100 food o r g a n i s m s p e r ml). This r e a r i n g m e t h o d w a s found to be superior to the mass r e a r i n g t e c h n i q u e s p r e v i o u s l y u s e d by A n g e r & N a i r (1979) b e c a u s e both mortality a n d d e v e l o p m e n t d u r a t i o n c o u l d be s u b s t a n t i a l l y r e d u c e d . T h e b r i n e shrimp e g g s c a m e from Kew, M e l b o u r n e , Australia; the rotifers w e r e c u l t i v a t e d a n d p r e p a r e d in the s a m e w a y as d e s c r i b e d by A n g e r & Nair (1979). No a n t i b i o t i c s or a l g a e w e r e a d d e d to the c u l t u r e m e d i u m . W a t e r a n d food w e r e c h a n g e d e v e r y s e c o n d day. T h e vials w e r e c h e c k e d e v e r y 24 h for e x u v i a e or d e a d larvae. An artifical d a y - n i g h t r h y t h m L : D 12:12 w a s p r o v i d e d .

S t a r v a t i o n in F I y a s

araneus

larvae

291

As soon as possible after the l a r v a e h a d m o u l t e d to the s t a g e desired, t h e y w e r e transferred to filtered s e a w a t e r a n d t r e a t e d as d e s c r i b e d a b o v e for the Z-1 stage. In this way, the i n d i v i d u a l s u r v i v a l t i m e of 50 to 75 (75 only at 12 °C) z o e a - 2 l a r v a e (Z-2} a n d of 25 m e g a l o p a e w a s also o b s e r v e d at e a c h e x p e r i m e n t a l t e m p e r a t u r e , i.e. a total of 250 Z1,225 Z-2, a n d 100 m e g a l o p a e . Larvae w e r e c o n s i d e r e d d e a d w h e n o p a q u e or w h e n no m o v e m e n t of any a p p e n d a g e or i n t e r n a l structure c o u l d be s e e n u n d e r m o d e r a t e magnification, E x p e r i m e n t s o n t h e e f f e c t s of e a r l y s t a r v a t i o n o n l a t e r d e v e l o p m e n t

and survival

Basically the s a m e e x p e r i m e n t t e c h n i q u e s as d e s c r i b e d a b o v e w e r e u s e d to e v a l u a t e " s u b l e t h a l effects" of early starvation. T h e e x p e r i m e n t a l d e s i g n is s h o w n in F i g u r e 1. Each e x p e r i m e n t c o n s i s t e d of two to s e v e n sets ( s u b e x p e r i m e n t s ) with 25 (in o n e case 50) i n d i v i d u a l l y m a i n t a i n e d larvae. Thus, o n e e x p e r i m e n t c o m p r i s e d 50 to 175 larvae, e a c h in its o w n n u m b e r e d vial. This t e c h n i q u e l a t e r a l l o w e d a d e t a i l e d statistical analysis. S p e c i a l care w a s t a k e n to follow e x a c t l y the r e s p e c t i v e t i m e s c h e d u l e for controls and m a n i p u l a t i o n s in a 24 h rhythm. Larvae w h i c h w e r e to be s w i t c h e d from f e e d i n g to s t a r v i n g c o n d i t i o n s w e r e t r a n s f e r r e d to c l e a n vials, only after b e i n g w a s h e d in baths of filtered s e a w a t e r , in o r d e r to a v o i d a c c i d e n t a l transfer of food organisms. All e x p e r i m e n t s r e f e r r e d to in F i g u r e 1 w e r e c a r r i e d out w i t h Z-1 larvae. As soon as they m o u l t e d to the s e c o n d instar, t h e y fed regularly, a n d their later d e v e l o p m e n t w a s r e c o r d e d daily (same culture m e t h o d s as d e s c r i b e d above), u n t i l t h e y d i e d or

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Fig. 3. H y a s a r a n e u s : Experiment 1. Larval development (mean values +_ 95% confidence limits and range of single observations) and mortality in relation to differential starvation. Cross: no survival to following stage. Further explanations see Figure 1 and text of starvation (Figs 1 a n d 3): O n e set of Z-1 l a r v a e (in this e x c e p t i o n a l case, 50 i n s t e a d of 25 i n d i v i d u a l s ) w a s s t a r v e d for 12 days. This is only slightly b e l o w t h e lethal t h r e s h o l d at 12 °C, but 26 z o e a e s u r v i v e d to the first d a y of f e e d i n g . A n o t h e r set fasted for only six days b e f o r e b e i n g fed; all 25 l a r v a e s u r v i v e d to this day, as in the control (C in Fig. 3; no starvation). N o n e of the l a r v a e w h i c h h a d b e e n s t a r v e d for 12 days r e c o v e r e d a n d r e a c h e d the s e c o n d stage. S o m e of t h e m l i v e d for up to 29 days b e f o r e t h e y died. This i n d i c a t e s that t h e y h a d not c o m p l e t e l y lost their a b i l i t y to t a k e u p a n d to c o n v e r t food, but they did lose t h e i r ability to moult. Six days of initial starvation also c a u s e d s i g n i f i c a n t l y h i g h e r mortality, after comm e n c e m e n t of f e e d i n g , t h a n in the fed control g r o u p (P < 10-3). T h e survivors n e e d e d s e v e n days l o n g e r t h a n the control l a r v a e to r e a c h the Z-2 stage. If it is a s s u m e d that d u r i n g starvation no d e v e l o p m e n t a l p r o c e s s e s take p l a c e and therefore, six days are s u b t r a c t e d from the i n t e r m o u l t d u r a t i o n (dotted range, mean, a n d c o n f i d e n c e limits in Fig. 3), t h e n t h e r e still r e m a i n s a s i g n i f i c a n t d i f f e r e n c e in d e v e l o p m e n t rate, w h e n c o m p a r e d w i t h the control (P = 0.02). Slight d i f f e r e n c e s in d e v e l o p m e n t rate a n d mortality, o b s e r v e d in later stages, w e r e not statistically significant. E x p e r i m e n t 2 w a s an a t t e m p t to e s t i m a t e the time n e c e s s a r y to a c c u m u l a t e sufficient e n e r g y r e s e r v e s for m o u l t i n g successfully to the s e c o n d z o e a l stage w i t h o u t further food supply. As s h o w n in F i g u r e s 1 a n d 4, f e e d i n g c e a s e d after differential p e r i o d s in five s u b e x p e r i m e n t s , w h i c h can be c o m p a r e d w i t h a s t a r v e d (0) a n d a fed control g r o u p (C). T h e s t a r v e d z o e a e a g a i n d i e d after 12 to 14 days w i t h o u t r e a c h i n g the second stage (Fig. 4). In t h e g r o u p fed for only t w o days after h a t c h i n g , t w o i n d i v i d u a l s successfully m o u l t e d to t h e Z-2 after 14 days (i.e. after s t a r v i n g for 12 days). Both larvae, however, d i e d later w i t h o u t r e a c h i n g the m e g a l o p a stage.

S t a r v a t i o n in H y a s a r a n e u s l a r v a e

of feeding (day in Z| stage)

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After four days or m o r e of f e e d i n g , s t a r v a t i o n d i d not i n f l u e n c e survival to t h e s e c o n d stage: T h e r e w a s p r a c t i c a l l y no m o r t a l i t y in the Z-1. Unfortunately, the fed control g r o u p h a d u n u s u a l l y poor s u r v i v a l in the Z-2 a n d in the m e g a l o p a stages a n d thus, i n t e r p r e t a tion of the mortality f i g u r e s is difficult in this e x p e r i m e n t . A l t h o u g h t h e r e w a s an u n u s u a l l y h i g h v a r i a t i o n in t h e d u r a t i o n of s t a g e 1 in t h e fed control too, the v a l u e s for d e v e l o p m e n t rate in F i g u r e 4 s h o w c l e a r trends: T h e e a r l i e r t h e first z o e a l s t a g e was starved, the l o n g e r its d e v e l o p m e n t lasted. This effect b e c a m e e v e n more e v i d e n t in the Z-2, in w h i c h no l a c k of food o c c u r e d d u r i n g this e x p e r i m e n t . T h e s e trends are r e f l e c t e d in statistically s i g n i f i c a n t r e g r e s s i o n s (solid l i n e s in Fig. 4): Z - l : In D = 2 . 5 8 - 0 . 1 0 - l n t (r = - 0 . 9 9 9 8 ; P = 0.01); Z-2: D = 1 8 . 1 8 - 0 . 7 8 t (r = - 0 . 9 9 9 8 ; P = 0.01) w h e r e D = d e v e l o p m e n t duration, t = t i m e (day) d u r i n g Z-1 s t a g e at w h i c h starvation b e g a n . T h e m e a n v a l u e s of s t a g e d u r a t i o n in s i n g l e s u b e x p e r i m e n t s w e r e not s i g n i f i c a n t l y different from the control g r o u p u n l e s s f e e d i n g c e a s e d r a t h e r soon (4 days after h a t c h i n g

296

K. A n g e r & R. R. D a w i r s

for t h e Z - l , 6 days or s o o n e r for t h e Z-2 duration). A s t o n i s h i n g l y , t h e control g r o u p d e v e l o p e d e v e n s l o w e r in b o t h z o e a l s t a g e s t h a n t h e g r o u p s s t a r v e d d u r i n g the last 2 to 4 days b e f o r e m o u l t i n g to the Z-2. T h e d u r a t i o n of the m e g a l o p a s t a g e w a s v i r t u a l l y u n a f f e c t e d by e a r l y starvation. It f l u c t u a t e d b e t w e e n 23.5 + 1.5 a n d 24.7 _ 0.9 days in t h e r e m a i n i n g five groups. Since the a b o v e effects in the z o e a l s t a g e s a d d to e a c h o t h e r a n d the m e g a l o p a had a rather c o n s t a n t duration, total d e v e l o p m e n t {D) to t h e first crab s t a g e w a s also significantly d e l a y e d d u e to e a r l y starvation (t) (values rising from 45.5 + 1.6 to 49.0 +_ 1.4 days): D = 51.55 - 0.58 t (r = - 0.9770; P = 0.02). For c o m p a r a t i v e e c o l o g i c a l c o n s i d e r a t i o n s the m i n i m u m time n e c e s s a r y to a c c u m u late e n o u g h r e s e r v e s for r e a c h i n g the n e x t instar i n d e p e n d e n t of further food supply m i g h t b e of interest. W e call this v a l u e h e r e " p o i n t of r e s e r v e s a t u r a t i o n " (PRS). Since t h e r e is no c o n d i t i o n g u a r a n t e e i n g a 100 % s u r v i v a l to any l a t e r stage, t h e 50 % point in the m o r t a l i t y c u r v e will be c o n s i d e r e d a m e a s u r e for the d e g r e e of d e p e n d e n c e on e x t e r n a l e n e r g y s u p p l y in a g i v e n s t a g e u n d e r d e f i n e d conditions. This PRS50 v a l u e is, a c c o r d i n g to the a b o v e e x p e r i m e n t , ca. 3 days or ca. 30 % of d e v e l o p m e n t time for the Z1 s t a g e at 12 °C a n d f e e d i n g c o n d i t i o n s as d e s c r i b e d above. E x p e r i m e n t 3 : T h e last e x p e r i m e n t r e v e a l e d that six days of f e e d i n g in the b e g i n n i n g of the Z-1 s t a g e a l l o w almost a n o r m a l d e v e l o p m e n t to t h e Z-2 and later instars. E x p e r i m e n t 3 w a s d e s i g n e d as a test of w h e t h e r this p e r i o d is sufficient in any case or only if a p p l i e d soon after h a t c h i n g (Fig. 1). As in e x p e r i m e n t 1, o n e set of 25 z o e a e w a s s t a r v e d for six days a n d t h e n fed until the l a r v a e r e a c h e d t h e s e c o n d s t a g e or died. T h e results w e r e similar, but mortality was h i g h e r (88 % to the first crab stage, in contrast to 68 % in exp. 1), a n d t h e duration of the Z-1 s t a g e w a s s o m e w h a t m o r e d e l a y e d {19.6 vs. 17.9 days). T h e differences can be e x p l a i n e d b y t h e fact that e x p e r i m e n t 3 w a s c a r r i e d out at the e n d of the artificially p r o l o n g e d h a t c h i n g s e a s o n (May, 1979), a n d the last h a t c h i n g l a r v a e w e r e a p p a r e n t l y less v i a b l e t h a n e a r l i e r ones. A p a r a l l e l set of l a r v a e w a s t r e a t e d in t h e s a m e w a y until d a y 12: After fasting six days a n d t h e n f e e d i n g six days, t h e y w e r e s t a r v e d again. N o n e of t h e s e l a r v a e r e a c h e d the Z-2 stage; the last z o e a d i e d after 32 days w i t h o u t moulting. This lack of flexibility i n d i c a t e d the e x i s t e n c e of p a r t i c u l a r l y s e n s i t i v e p e r i o d s a n d thus of i n t e r f e r e n c e with an i n t e r n a l p r o g r a m m e r u n n i n g d u r i n g t h e first z o e a l instar. T h e r e f o r e , o n e y e a r later, n e w e x p e r i m e n t s w e r e started to e l u c i d a t e t h e s i g n i f i c a n c e of this d e v e l o p m e n t a l p r o g r a m m e for the r e s i s t a n c e a g a i n s t s t a r v a t i o n periods. E x p e r i m e n t 4 (Figs 1 a n d 5) w a s an e x t e n s i o n of e x p e r i m e n t 1 a n d the reversal of e x p e r i m e n t 2. T h e q u e s t i o n to be a n s w e r e d was: H o w l o n g c a n an early larva resist s t a r v a t i o n w i t h o u t l o s i n g its a b i l i t y to r e c o v e r a n d to m o u l t successfully to the next stage? F r o m F i g u r e 5 it b e c o m e s e v i d e n t that a n y l a c k of food in t h e b e g i n n i n g of larval life c a u s e s a d e l a y in d e v e l o p m e n t : T h e d u r a t i o n of t h e Z-1 s t a g e (D) s h o w e d a strong c o r r e l a t i o n w i t h the t i m e of starvation {t) in its b e g i n n i n g . D = 10.31 + 1.44 t (r = 0.9985; P < 10 -4) T h e s l o p e of this r e g r e s s i o n (solid line in Fig. 5, l o w e r part) is not only significantly d i f f e r e n t from zero (P< 10-4), b u t also (P = 0.002) from t h e t h e o r e t i c a l r e l a t i o n s h i p (dotted line in.Fig. 5, l o w e r part), w h i c h c a n b e e x p r e s s e d as: D = D¢ + t, w h e r e D¢ = d u r a t i o n of Z-1 d e v e l o p m e n t in t h e control (C)

Starvation in H y a s araneus l a r v a e End

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This m e a n s that a s i g n i f i c a n t l y i n c r e a s i n g t i m e (t') in a d d i t i o n to D c + t is n e c e s s a r y to c o m p e n s a t e for the p e r i o d of starvation (t). Mortality did not follow the s a m e l i n e a r pattern, but r a t h e r a s i g m o i d a l r e l a t i o n s h i p (Fig. 5). N e i g h b o u r i n g v a l u e s w e r e not s i g n i f i c a n t l y different from e a c h o t h e r e x c e p t in the r a n g e 6 to 10 days of starvation (P = 0.02 to 0.002). S u r v i v a l w a s g e n e r a l l y h i g h e r t h a n in the c o m p a r a b l e 1979 e x p e r i m e n t s 1 a n d 3, b u t it s h o w e d a s i m i l a r u p p e r l i m i t of resistance: After 10 days of starvation, only o n e s u r v i v o r r e c o v e r e d a n d r e a c h e d t h e next m o u l t (and e v e n m e t a m o r p h o s i s ) . After 12 days fasting, no m o r e l a r v a r e c o v e r e d a n d m o u l t e d to the Z-2 stage; the last o n e d i e d after 34 days. Such limit for e a r l y starvation r e s i s t a n c e w a s also f o u n d in fish l a r v a e ; in a c c o r d a n c e with Blaxter & H e m p e l (1963) w e a p p l y t h e t e r m " p o i n t - o f - n o - r e t u r n " (PNR) to this limit. For 50 % of the p o p u l a t i o n c o n s i d e r e d , this v a l u e (PNRs0) w a s f o u n d after s o m e w h a t less than 8 days or slightly m o r e t h a n 50 % of the m a x i m u m p o s s i b l e s u r v i v a l t i m e u n d e r starvation. O n c e the first z o e a l m o u t t is successfully p a s s e d , l a t e r s u r v i v a l is o b v i o u s l y not i n f l u e n c e d by e a r l y starvation periods: In all s u b e x p e r i m e n t s p r a c t i c a l l y no m o r e mortality occurred in the later stages (three i n d i v i d u a l s out of 103 w h i c h h a d r e a c h e d t h e Z-2). A surprising p h e n o m e n o n , h o w e v e r , w a s n o t e d in the Z-2 stage: T h e r e is a statisti-

298

K. A n g e r & R. R. D a w i r s

cally s i g n i f i c a n t d e c l i n e in t h e d u r a t i o n of this instar (D) w i t h i n c r e a s i n g starvation time at t h e b e g i n n i n g of t h e Z-1 s t a g e (t): D = 13.58 - 0.16 t (r = 0.9822; P < 10 -3) This t r e n d (solid l i n e in Fig. 5, u p p e r part) is s i g n i f i c a n t l y different from the control (dotted h o r i z o n t a l l i n e in Fig. 5, u p p e r part), but it is m u c h w e a k e r t h a n the i n c r e a s e in Z1 d u r a t i o n a n d thus, c a n c o m p e n s a t e for o n l y little part of this delay. In the m e g a l o p a s t a g e t h e r e is a slight (statistically insignificant) i n c r e a s e from 26.3 _+ 2.0 to 28,6 ___ 1.9 days. Total d e v e l o p m e n t (D) to the first crab s t a g e clearly i n c r e a s e s w i t h e a r l y starvation t i m e (t) from 51,7 + 2.0 to 64 days. T h e r e g r e s s i o n e q u a t i o n d e s c r i b i n g this trend is: D = 50.79 + 1.33 t (r = 0.9894; P < 10 -3) In e x p e r i m e n t 4, as in all l a t e r 1980 e x p e r i m e n t s , the d e v e l o p m e n t rate in the two z o e a l s t a g e s w a s s i g n i f i c a n t l y s l o w e r t h a n o n e y e a r before, w h e r e a s the m e g a l o p a stage h a d not c h a n g e d . This o b s e r v a t i o n w i l l be d i s c u s s e d below. E x p e r i m e n t 5 (Figs 1 a n d 6): It b e c a m e e v i d e n t that starvation p e r i o d s in the b e g i n n i n g a n d at the e n d of the first z o e a l s t a g e e a c h h a d different effects on later d e v e l o p m e n t a n d s u r v i v a l (cf. exp. 2 a n d 4). Therefore. a m o r e d e t a i l e d analysis of the Starvation

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S t a r v a t i o n in H y a s a r a n e u s l a r v a e

299

interaction between the internal development programme and starvation effects was needed. In e x p e r i m e n t 5 a c o n s t a n t 4 - d a y f a s t i n g p e r i o d w a s s h i f t e d f r o m t h e b e g i n n i n g to t h e m i d d l e a n d to t h e e n d of t h e Z - l s t a g e . T h e l a t e r t h i s p e r i o d of s t a r v a t i o n o c c u r r e d , t h e less it d e l a y e d t h e d u r a t i o n of t h e Z - l , b u t t h e m o r e it i n f l u e n c e d t h e Z-2. T h e r e g r e s s i o n s of t h e m e a n d a y s of t h e 4 - d a y p e r i o d s (t) o n t h e d u r a t i o n s of t h e z o e a l s t a g e s (D) are: Z - l : l n D ---- 2 . 9 0 - 0 . 1 8 . l n t (r ---- - - 0 . 9 9 7 2 ; P ---- 0.048) Z-2: D ---- 12,76 + 0.15 t (r = 0.9988; P = 0.03) As in e x p e r i m e n t 4, t h e r e w a s a w e a k t r e n d in m e g a l o p a d e v e l o p m e n t o p p o s e d to t h a t of t h e Z-2 s t a g e . It w a s a g a i n s t a t i s t i c a l l y i n s i g n i f i c a n t . O n l y s t a r v a t i o n in t h e v e r y b e g i n n i n g of t h e Z-1 s t a g e h a d a s i g n i f i c a n t ; d e l a y i n g i n f l u e n c e o n t o t a l d e v e l o p m e n t t i m e to t h e fist crab: 55.3 + 1.5 v e r s u s 51.3 _+ 1.6 to 51,7 _- 2.0 d a y s . M o r t a l i t y w a s n o t i n f l u e n c e d b y t h e s e short s t a r v a t i o n t i m e s : D u r i n g t o t a l l a r v a l d e v e l o p m e n t it a m o u n t e d to 10 % i n t h e w h o l e e x p e r i m e n t . Starvation period (days in

Z ]

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0-2 I 2~4 I ~6 I B-818-1ollo-j2 19,

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o-2 I 2:4 I ~,:s J 6:a I a..~o 110-:'J2 Fig. 7. Hyas araneus: Experiment ft. Explanations see Figures 1 an 3

300

K. A n g e r & R. R. Dawirs

Experiment 6 was carried out i n the same w a y as the last one, only the starvation periods were s h o r t e n e d from 4 to 2 days (Figs 1 a n d 7). As m i g h t be expected, no statistically significant differences b e t w e e n single m e a n v a l u e s could be found, since o n l y two days of starvation h a r d l y i n f l u e n c e d d e v e l o p m e n t a n d survival. However, there was a n u n e x p e c t e d f i n d i n g : Short starvation i m m e d i a t e l y after h a t c h i n g h a d a p p a r e n t l y less d e l a y i n g i n f l u e n c e o n the Z-1 stage t h a n the same short period a p p l i e d a little later (Fig. 7). A l t h o u g h the difference b e t w e e n these two m e a n values was not statistically significant, it m i g h t h a v e a m e a n i n g w h i c h will b e discussed later. This first v a l u e was the only one not fitting the t r e n d s h o w n b y all the other figures. They r e v e a l e d a similar d e c l i n e (only weaker) to that o b s e r v e d i n e x p e r i m e n t 5 for Z-1 d u r a t i o n (D) in relation to starvation time ( m e a n of the period, t): D = 13.34 - 0 . 0 9 t (r = - 0 . 9 8 8 4 ; P = 10 -3) Short starvation occurring b e y o n d the first four days of Z-1 d e v e l o p m e n t caused a slight ~telay i n the Z-2. In contrast to e x p e r i m e n t 5 there was no further difference in the extent of this delay. Mortality was h i g h e r t h a n i n the other e x p e r i m e n t s (12 to 28 % died before metamorphosis), b u t did not show a n y trend. Experiment 7 was a n e x t e n s i o n of exp. 3 a n d the reversal of 5 a n d 6 (Fig. 1): I n s t e a d of a starvation period a p p e a r i n g at different times in early d e v e l o p m e n t , a rather short f e e d i n g period (4 days) shifted w i t h i n a long starvation period. T h e results c o m p l e m e n t a n d confirm all a b o v e o b s e r v a t i o n s (Fig. 8): Four days of f e e d i n g i m m e d i a t e l y after h a t c h i n g were sufficient for most of the larvae to reach the next stage w i t h o u t a n y further food s u p p l y (cf. PRSs0 i n e x p e r i m e n t 2). W h e n this 4-day f e e d i n g period followed a n e q u a l l y long starvation period, mortality i n c r e a s e d s i g n i f i c a n t l y (P = 0.04), a n d the i n t e r m o u l t d u r a t i o n of Z-1 stage was Feeding period (days in ZI staged O-l. 100"

~-8

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8-12

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Fig. 8. Hyas araneus: Experiment 7. Explanations see Figures 1 and 3

Starvation in H y a s a r a n e u s l a r v a e

301

c o n s i d e r a b l y p r o l o n g e d ; still 48 % of t h e l a r v a e r e a c h e d t h e Z-2 a n d 32 % the first crab stage. In both s u b e x p e r i m e n t s also, the Z-2 d e v e l o p m e n t w a s strongly d e l a y e d . After e i g h t days of starvation, a 4 - d a y f e e d i n g p e r i o d w a s insufficient to support d e v e l o p m e n t to the s e c o n d stage. T h e latest l a r v a d i e d after 40 days (28 days of starvation f o l l o w i n g only 4 days of feedingT). Survival in the s e c o n d z o e a l s t a g e w a s s i g n i f i c a n t l y r e d u c e d in the g r o u p fed from day 4 to 8 as o p p o s e d to the control (P ---- 0.02). In the m e g a l o p a s t a g e t h e r e w a s no mortality in a n y group. E x p e r i m e n t 8 f o l l o w e d e x a c t l y t h e s a m e d e s i g n as e x p e r i m e n t 2 (Fig. t), e x c e p t t h e r e w e r e no control g r o u p s ( c o r r e s p o n d i n g to 0 a n d C in Fig. 1), a n d the s e c o n d z o e a w a s c o n s i d e r e d i n s t e a d of t h e first s t a g e (Fig. 9). This e x p e r i m e n t w a s p l a n n e d as an a t t e m p t to p r o v i d e a p r e l i m i n a r y i d e a a b o u t t h e g e n e r a l b e h a v i o u r of t h e Z-2 to b e e x p e c t e d in future i n v e s t i g a t i o n s . T h e PRS50 v a l u e w a s f o u n d to b e ca. 5 days. This w a s (absolutely) later t h a n in the Z1, but a b o u t the s a m e in r e l a t i o n to its d u r a t i o n (ca. one third). D e v e l o p m e n t d u r a t i o n in the Z - 2 w a s only p r o l o n g e d w h e n f e e d i n g c e a s e d a l r e a d y after four days; in this i n s t a n c e

End of feeding (day in Z I | stage) 2

,

6

8

10

o '°1 38" 363/.. 3230-

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28.

g E

26-

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22"

2"

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megalopa

20-

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15 14

13

zoea II

Fig. 9. Hyas araneus: Experiment 8. Explanations see Figure 3

302

K. A n g e r & R, R. Dawirs

mortality was s i g n i f i c a n t l y h i g h e r (P < 10 -4) t h a n i n the group fed two days longer. If starvation c o m m e n c e d e v e n sooner, no larva r e a c h e d the m e g a l o p a stage. T h e d u r a t i o n of the m e g a l o p a stage was s u r p r i s i n g l y unaffected b y starvation d u r i n g the Z-2 i n s t a l Also In the total d e v e l o p m e n t time to the first crab only i n s i g n i f i c a n t differences w e r e o b s e r v e d (52.5 _ 1.4 to 53.7 _ 1.6 days).

DISCUSSION The first question in the section "Introduction" can be answered as follows: All larval stages of Hyas araneus depend on the availabilityof food organisms for further development, regardless of temperature. However, they are apparently well adapted to temporary lack of food, as maximal survival times under starvation conditions are considerably longer than shown by other figures hitherto reported for crustacean larvae (only exception: Kon, 1979). The limits for starvation resistance vary in relation to temperature and stage. In all stages, there is a more or less clearly developed inverse relationship between survival time and temperature. This finding might be explained simply by the well-known temperature dependence of metabolic processes; however, this explanation would be too simple. As shown by Rice & Provenzano (1965), Provenzano (1967, 1968b), and Gore (1970), not necessarily the lowest, but often the o p t i m a I temperature allows longest survival in starved decapod larvae. Some tropical species, for example, are killed by temperatures of I0° to 15° C, long before their reserves have been used up (Provenzano, pets. comm.). There are obviously two mechanisms superimposed on each other: (1). generally decreasing metabolism with decreasing temperature, and (2). a temperature range in which enzymatic and other biochemical processes function optimally due to genetic or non-genetic adaptation (cf. Kinne, 1964, Rosenberg & Costlow, 1979). Since H. araneus is a cold-water species, these two phenomena act principally together and cannot be clearly distinguished. On the other hand, modifications of this general trend should be expected concerning the different larval stages. Hatching takes place during the season with coldest water temperature, larval development during rising temperatures in spring. This means that the Z-1 stage should be adapted to the lowest (ca. 3o-7° C), the Z-2 to intermediate (ca. 5°-10° C), and the megalopa to the highest temperatures (ca. 8°-15° C) (see the graphical model proposed by Anger &Nail 1979). The survival pattern in Figure 2 corresponds rather well to these assumptions. Differential starvation resistance in the larval stages appears to be related to the temperature optima estimated above. If the values from Figure 2 are plotted against the mean stage durations summarized b y A n g e r & Nair (1979), plus some r e c e n t l y o b t a i n e d figures (Anger & Dawirs, u n p u b lished) for 18° C (8 days for Z - l , 10 days for Z-2), t h e n the following regression is o b t a i n e d : S = 5.2 + 0.9 D (r =- 0.9387; P < 10 -3) This gives a n a n s w e r to the second q u e s t i o n i n the "Introduction". M a x i m a l survival time (S) u n d e r starvation is i n the same order of m a g n i t u d e as the " n o r m a l " d u r a t i o n (D) of e a c h stage at a g i v e n t e m p e r a t u r e , mostly S is u s u a l l y slightly h i g h e r t h a n D. Similar r e l a t i o n s h i p s (S -- D) w e r e also o b s e r v e d b y K n o w l t o n (1974), Roberts (1974), Yaqoob (1977}, a n d P r o v e n z a n o (1978). D e v i a t i o n s from this rule were o b s e r v e d at t e m p e r a t u r e s b e l o w the optimal r a n g e (Gore, 1968, 1970; Provenzano, 1967, 1968b). In these cases,

Starvation i n H y a s araneus larvae

303

survival was c o n s i d e r a b l y shorter t h a n d e v e l o p m e n t (if this was, at all, possible}; i n the optimal range, S a n d D w e r e a g a i n similar. If the g e n e r a l v a l i d i t y of this r e l a t i o n s h i p c a n b e confirmed, it should b e p o s s i b l e to e s t i m a t e the a p p r o x i m a t e m a x i m a l s u r v i v a l times of b r a c h y u r a n larvae from their stage durations. E x p e r i m e n t s carried out i n 1979 a n d 1980 i n d i c a t e d some systematic differences i n d e v e l o p m e n t d u r a t i o n w h i c h c a n n o t yet be e x p l a i n e d definitely. T h e latter e x p e r i m e n t s started about one m o n t h earlier i n the year t h a n the former series. Since the b e r r i e d females were always kept i n cold w a t e r (2 °C), a n irreversible n o n - g e n e t i c a d a p t a t i o n (Rosenberg & Costlow, 1979} m i g h t have c a u s e d a decrease in i n t e r m o u l t d u r a t i o n with i n c r e a s i n g time of adaptation. A n o t h e r possible e x p l a n a t i o n m i g h t c o n c e r n the a m o u n t of yolk reserves i n larvae, h a t c h e d at different times, as c a r b o n m e a s u r e m e n t s a n d starvation resistence w e r e h i g h e r i n larvae o b s e r v e d i n F e b r u a r y 1980 t h a n i n M a y 1979. It is still a n o p e n question, w h e t h e r these differences r e s u l t e d from different females, periods w i t h i n the s p a w n i n g s e a s o n or from different years. If there w a s n o t e m p e r a t u r e adaptation, a decrease i n yolk reserves d u r i n g o n e s e a s o n m i g h t b e the most p r o b a b l e explanation! This w o u l d b e s u p p o r t e d b y s i m i l a r o b s e r v a t i o n s b y P a n d i a n & S c h u m a n n (1967) a n d R e g n a u l t (1969). T h e s i g n i f i c a n c e of those p h e n o m e n a will b e i n v e s t i g a t e d before further e x p e r i m e n t s on starvation resistance a n d " s u b l e t h a l effects" of starvation are started. Q u e s t i o n n u m b e r 3 i n the " I n t r o d u c t i o n " is a n s w e r e d i n Figures 4 a n d 9: Both zoeal stages n e e d at least one third approximately, of their d e v e l o p m e n t d u r a t i o n to a c c u m u late e n o u g h reserves for a b o u t 50 % of the larvae to m o u l t successfully to the next stage, i n d e p e n d e n t of food a v a i l a b i l i t y (PRSs0 }. If starvation lasts from the PRSs0 to the moult, survival is r e d u c e d a n d d e v e l o p m e n t is delayed. T h e time at w h i c h n o larva has yet a c c u m u l a t e d sufficient reserves to survive starvation to the next m o u l t (PRS0) is o n l y little earlier. In both zoeal stages it a p p e a r s to b e a b o u t 20 % of stage duration. In other words: Zoea larvae m u s t feed right after h a t c h i n g (or moulting} for more t h a n o n e fifth of their n o r m a l d u r a t i o n i n order to have at least some c h a n c e of s u r v i v i n g later starvation; if more t h a n o n e third of the stage d u r a t i o n has e l a p s e d u n d e r good f e e d i n g conditions, every second larva p r o b a b l y survives starvation to the next moult. In e x p e r i m e n t 2 (Fig. 4) starvation d u r i n g the last 2 to 4, days of the first zoeal stage resulted i n s o m e w h a t faster d e v e l o p m e n t as c o m p a r e d to the control (C). This m i g h t suggest that food o r g a n i s m s in some w a y disturb rather t h a n support m o u l t i n g zoeae. The differences were statistically not significant, a n d they w e r e not f o u n d a g a i n i n e x p e r i m e n t 5 {Fig. 6); therefore this p o s s i b l e effect m u s t r e m a i n i n question. The fourth q u e s t i o n i n the " I n t r o d u c t i o n " deserves a clear "yes": T h e point-of-noreturn for 50 % of the Z-1 larvae (PNRs0 } is r e a c h e d after p a s s i n g more t h a n half of the m a x i m a l l y possible survival time u n d e r starvation (Fig. 5). If more t h a n 70 % of this m a x i m u m time has e l a p s e d w i t h o u t food supply, a p p a r e n t l y no larva has a c h a n c e to recover w h e n re-fed (PNRa00). These figures i n d i c a t e a n u n u s u a l l y good a d a p t a t i o n to fluctuating prey a v a i l a b i l i t y as c o m p a r e d to fish larvae (see Ehrlich et al., 1976}. T h e y correspond closely to the only c o m p a r a b l e data for zoeae of a m a j i d crab p r o v i d e d by Kon (1979). The regression l i n e for Z-1 d u r a t i o n (D} a g a i n s t starvation (t) i n F i g u r e 5 s u g g e s t s a basic i n t e r n a l m e c h a n i s m i n early d e v e l o p m e n t : T h e p r o g r a m m e w h i c h has to b e completed to permit m o u l t i n g to the second stage, does not start as long as the l a r v a has

304

K. A n g e r & R. R. Dawirs

not fed for the first time. N o r m a l d e v e l o p m e n t d u r a t i o n (Dc) is p r o l o n g e d by the s t a r v a t i o n t i m e (t) plus a n a d d i t i o n a l a m o u n t of t i m e (t') w h i c h is p r o b a b l y n e c e s s a r y to c o m p e n s a t e for e n e r g y losses d u r i n g starvation. S i n c e t' is p r o p o r t i o n a l to t, a n o t h e r l i n e a r r e g r e s s i o n c a n be c a l c u l a t e d to e x p r e s s the r e l a t i o n s h i p b e t w e e n D and t (solid line in Fig. 5, l o w e r part). In this n e w r e g r e s s i o n the slope is s i g n i f i c a n t l y s t e e p e r than in the t h e o r e t i c a l D -- D c + 1 t (dotted in Fig. 5, l o w e r part). Kon (1979) found such a d d i t i o n a l p r o l o n g a t i o n (t') only after m o r e t h a n o n e w e e k of initial starvation. T h e g e n e r a l r e s p o n s e of M a j i d z o e a e to early starvation as d e s c r i b e d in that p a p e r is b a s i c a l l y t h e s a m e as found in our e x p e r i m e n t s : D e v e l o p m e n t starts only after first f e e d i n g . A similar o b s e r v a t i o n w a s also m a d e in k i n g - c r a b z o e a e (Kurata, 1959). T h e n e w l i n e a r r e l a t i o n s h i p i n d i c a t e s a constant e n e r g y loss p e r unit of starvation t i m e for a c e r t a i n range. T h e r e is, h o w e v e r , a restriction. T h e m e c h a n i s m a s s u m e d a b o v e is not fully v a l i d for v e r y short starvation p e r i o d s d i r e c t l y after t h e p r e z o e a l moult. For starvation p e r i o d s shorter t h a n a b o u t t h r e e days, t' a p p e a r s to e q u a l zero or it b e c o m e s e v e n n e g a t i v e ! T h e s a m e effect w a s also o b s e r v e d in e x p e r i m e n t 6 (Fig. 7). This m e a n s that a s m a l l part (about o n e day) of t h e d e v e l o p m e n t a l p r o g r a m m e m e n t i o n e d a b o v e m u s t run, i n d e p e n d e n t of e x t e r n a l e n e r g y supply, in the v e r y b e g i n n i n g of the stage. S i n c e freshly h a t c h e d l a r v a e possess e n o u g h r e s e r v e s to run a g r e a t e r part of their d e v e l o p m e n t a l p r o g r a m m e w i t h o u t food (Anger & Nair, 1979), the a b o v e m e c h a n i s m c a n n o t be e x p l a i n e d e x c l u s i v e l y with e n e r g e t i c s . A p o s s i b l e e x p l a n a t i o n for the k e y role of first f e e d i n g in e a r l y l a r v a l d e v e l o p m e n t of d e c a p o d s w i l l be g i v e n below. T h e e x i s t e n c e of a critical p e r i o d at the b e g i n n i n g of larval d e v e l o p m e n t was

2.S.j E

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Commencement of starvation (day in Z ! )

Fig. 10. H y a s araneus: Response pattern in the zoea-1 stage(Zl) to differential starvation. Delay expressed as multiple of development duration in fed controls. Further explanations see text

Starvation i n H y a s a r a n e u s larvae

305

already suggested b y o b s e r v a t i o n s reported by Y a t s u z u k a (1962), M o d i n & Cox (1967), a n d Kon (1979). These authors d e s c r i b e d l o w e r e d survival i n d e c a p o d larvae, w h e n f e e d i n g c o m m e n c e d too late following hatching. A n a n a l o g y exists i n larval fishes (Ehrlich et al., 1976). Also C h a m b e r l a i n ' s (1957) o b s e r v a t i o n s most p r o b a b l y b a s e d o n the same m e c h a n i s m : X a n t h i d larvae fed e x c l u s i v e l y on diatoms d u r i n g the first days (later they received a n i m a l food) s h o w e d c o n s i d e r a b l y d e l a y e d d e v e l o p m e n t as o p p o s e d to s i b l i n g larvae fed with z o o p l a n k t o n from the b e g i n n i n g . It is n o w g e n e r a l l y a c c e p t e d that b r a c h y u r a n larvae are strictly carnivorous a n d c a n n o t subsist on a l g a l food. This m e a n s that C h a m b e r l a i n starved the zoeae i n v o l u n t a r i l y i n a similar w a y as i n our e x p e r i m e n t 1 (Fig. 3), a n d he o b t a i n e d similar results. Figure 10 s u m m a r i z e s the response p a t t e r n s of the first zoeal stage of Ft. a r a n e u s to starvation: The d e l a y i n Z-1 d e v e l o p m e n t , e x p r e s s e d as p r o l o n g a t i o n factor u s i n g the control as unit (C = 1), shows differential effects of starvation. The delay increases with d u r a t i o n of the starvation period, b u t e v e n more drastically with its a d v a n c i n g c o m m e n c e m e n t w i t h i n the stage. This p a t t e r n confirms the criticalpoint concept (see above) a n d it a n s w e r s the last q u e s t i o n i n the section "Introduction". If starvation starts before the PRSs0 is r e a c h e d or if it e n d s later t h a n the PNR50 (shaded area, b in Fig. 10), t h e n less t h a n half of all larvae have a c h a n c e to reach the s e c o n d stage. The PNR100 a n d the PRS 0 define the u l t i m a t e limit for a n y further d e v e l o p m e n t (hatched area, a). A similar r e s p o n s e p a t t e r n as s h o w n i n Figure 10 is obtained, if mortality i n s t e a d of d e v e l o p m e n t a l delay is t a k e n as a m e a s u r e for starvation effects. However, zoeal mortality is a less accurate, sensitive, a n d r e l i a b l e i n d e x (cf. Costlow & Bookhout, 1970) a n d therefore was only t a k e n as a d d i t i o n a l i n f o r m a t i o n i n this study. Also the observation reported by Wickins (1972), who p r o v i d e d food of different q u a l i t y d u r i n g differential periods in larval d e v e l o p m e n t of p e n a e i d shrimps, correspond very well to our findings. With the exception of e x p e r i m e n t 8, there was n e v e r a n y starvation a p p l i e d to the second zoea, b u t effects of early starvation o n later stages did occur. Lack of food i n the final phase of the Z-1 stage did not s i g n i f i c a n t l y affect the d u r a t i o n of this stage (Figs 4, 6, 7, 10), but that of the next instar. The effects (delayed d e v e l o p m e n t a n d i n c r e a s i n g mortality) d e p e n d a g a i n on the d u r a t i o n of the fasting period. A s u r p r i s i n g p h e n o m e n o n is observed w h e n lack of food occurs in the b e g i n n i n g of the Z - l : the d u r a t i o n of the s e c o n d stage is s h o r t e n e d (Figs 5 a n d 6). We c a n n o t find sensible e n e r g e t i c e x p l a n a t i o n s for this p a r t i a l c o m p e n s a t i o n i n d e v e l o p m e n t rate. From our e x p e r i m e n t a l o b s e r v a t i o n s a n d from literature data the following hypothesis is d e r i v e d a n d proposed as a possible e x p l a n a t i o n : The first day of the moult cycle in the Z-1 stage is p r e s u m a b l y characterized b y the postmoult periods A a n d B. According to the only c o m p a r a b l e figures for crab larvae (Freeman & Costlow, 1980) we a s s u m e t h e m to last, t a k e n together, ca. 10 % of the stage duration. D u r i n g this time, w a t e r a n d m i n e r a l s are t a k e n up, a n d the e n d o c u t i c l e is secreted. The latter step i n v o l v e s chitin synthesis, w h i c h is i n d e p e n d e n t of food u p t a k e (Anger & Nair, 1979). Starvation, therefore, p r e s u m a b l y does not affect further development, if suffered only d u r i n g postmoult. Moult i n h i b i t i n g h o r m o n e (MIH) is p r o b a b l y secreted into the h a e m o l y m p h d u r i n g this phase, i n d e p e n d e n t l y of nutrition. As the larva approaches i n t e r m o u l t (C), food u p t a k e is n e c e s s a r y to initiate further

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d e v e l o p m e n t . A l l r e c o n s t r u c t i o n p r o c e s s e s cease, if this initial cue is m i s s i n g (see above), a n d p r o t e i n r e s e r v e s a r e u t l i z e d as m a i n e n e r g y s o u r c e d u r i n g this t i m e ( A n g e r & Nair, 1979). T h e l e n g t h of s t a r v a t i o n t i m e (t, m e a s u r e d from the b e g i n n i n g of p h a s e Co) c o r r e s p o n d s to the m i n i m u m p r o l o n g a t i o n of i n t e r m o u l t d u r a t i o n ( e x p e r i m e n t 4, cf. Kurata, 1959; Kon, 1979). T h e l o n g e r initial s t a r v a t i o n lasts d u r i n g p h a s e C, the more a d d i t i o n a l t i m e (t') is a d d e d for c o m p e n s a t i o n of p r o t e i n loss. T h e r e is a n u p p e r limit (ca. 70 % of m a x i m a l l y p o s s i b l e s u r v i v a l time) w h i c h c a n n o t b e e x c e e d e d w i t h o u t l o s i n g the a b i l i t y to r e c o v e r a n d to moult. T h e a c t u a l c a u s e of this p o i n t - o f - n o - r e t u r n can only b e s p e c u l a t e d : T h e a b i l i t y to c a t c h p r e y is c e r t a i n l y w e a k e n e d (Paul & Paul, 1980), but insufficient food u p t a k e a l o n e c a n h a r d l y e x p l a i n t h e PNR. Survival after initial starvation a n d r e c o m m e n c e m e n t of f e e d i n g is m o s t l y m u c h l o n g e r t h a n m a x i m u m survival u n d e r c o m p l e t e l a c k of food (exp. 1, 3, 4, 7; s e e also Kon, 1979). T h e r e f o r e some i r r e v e r s i b l e b i o c h e m i c a l or h i s t o l o g i c a l d a m a g e m u s t b e suffered w h i c h p r e v e n t s recovery and moulting. W h e n p r e y is a v a i l a b l e d u r i n g intermoult, tissue g r o w t h a n d a c c u m u l a t i o n of o r g a n i c r e s e r v e s t a k e p l a c e ( Y a m a o k a & Scheer, 1970). This p e r i o d is a s s u m e d to last ca. one t h i r d of Z-1 d u r a t i o n ( e s t i m a t i o n b a s e d on figures g i v e n b y F r e e m a n & Costlow, 1980), i. e. s o m e w h a t less t h a n four days. If s t a r v a t i o n (in t h e w i d e s t sense) p r e c e d e s or i n t e r r u p t s p h a s e C, it will last l o n g e r (of. F i g s 5-8), b e c a u s e p r o t e i n losses h a v e to b e c o m p e n s a t e d for. T h e r e a r e s e v e r a l s u b s t a n c e s e s s e n t i a l for g r o w t h in C r u s t a c e a (Provasoli, 1976). The fact t h a t t h e i n t e r m o u l t p h a s e (C) n e e d s a s t a r t i n g m e c h a n i s m s u g g e s t s that there m i g h t b e a s i n g l e k e y s u b s t a n c e . W e a s s u m e that sterols t a k e n from the first d i e t m a y p l a y a c r u c i a l role. T h e y c a n n o t b e s y n t h e s i z e d b y t h e l a r v a e (Whitney, 1969; G i l b e r t & O ' C o n n o r , 1970; Provasoli, 1976), b u t t h e y are n e e d e d as p r e c u r s o r s of steroid hormones. It is p o s s i b l e t h a t [~-ecdysone ( = ~ - e c d y s t e r o n e , c r u s t e c d y s o n e ) s y n t h e s i s is the a c t u a l s t a r t i n g p o i n t of further d e v e l o p m e n t . If s t a r v a t i o n sets in after the start of p h a s e C, d e v e l o p m e n t d o e s not i m m e d i a t e l y c e a s e ; if at this t i m e the p o o l of n e c e s s a r y r e s e r v e s is a l r e a d y " s a t u r a t e d " ( " p o i n t - o f - r e s e r v e - s a t u r a t i o n " , PRS, see above), i. e. p o s s i b l y a sterol p o o l sufficient for Z-1 d e v e l o p m e n t h a s b e e n a c c u m u l a t e d , t h e n the ~ - e c d y s o n e will suffice to i n i t i a t e p r e m o u l t a n d ecdysis, i n d e p e n d e n t of further p r e y a v a i l a b i l i t y . If s t a r v a t i o n b e g i n s too soon d u r i n g p h a s e C to a l l o w successful c o m p l e t i o n of the moult cycle, t h e n s o m e d e v e l o p m e n t still t a k e s p l a c e a u t o m a t i c a l l y . It will c e a s e later at some p o i n t until f e e d i n g r e c o m m e n c e s . In this c a s e the d e l a y in d e v e l o p m e n t is shorter t h a n the a c t u a l s t a r v a t i o n p e r i o d (Figs 4 a n d 6). I n t e r m o u l t (C) is c o m p l e t e d w h e n the ~ - e c d y s o n e has e x c e e d e d that l e v e l of activity w h i c h is n e c e s s a r y to e l i m i n a t e t h e i n f l u e n c e of MIH a n d to start the first p r e m o u l t p h a s e {Do}. B e y o n d this point, further d e v e l o p m e n t is p r o g r a m m e d b y t h e m o u l t i n g hormone; its a u t o m a t i c course is not s i g n i f i c a n t l y a f f e c t e d a n y m o r e b y p r e y a b s e n c e or p r e s e n c e . If p o s t m o u l t a n d intermoult, c o m b i n e d , a m o u n t to ca. 40 % of the s t a g e d u r a t i o n (cf. F r e e m a n & Costlow, 1980), t h e n D O s h o u l d c o m m e n c e after a b o u t five days. This a s s u m p t i o n c o r r e s p o n d s to t h e o b s e r v a t i o n s in e x p e r i m e n t s 2 a n d 5. It w o u l d m e a n that t h e Z-1 of H . a r a n e u s u n d e r g o e s a d i e c d y s i c t y p e of m o u l t (Knowles & Carlisle, 1956}. E x p e r i m e n t s 2 a n d 5 also s u g g e s t that d u r i n g p r e m o u l t some s u b s t a n c e s t a k e n from t h e d i e t a r e a c c u m u l a t e d w h i c h a r e i m p o r t a n t for t h e s e c o n d z o e a l stage. If starvation lasts for t h e w h o l e p r e m o u l t period, the d u r a t i o n of the Z-2 s t a g e is significantly

S t a r v a t i o n in H y a s a r a n e u s l a r v a e

307

prolonged. T h e k e y s u b s t a n c e m i g h t be a g a i n ~ - e c d y s o n e or s o m e p r e c u r s o r y sterol stored d u r i n g this period. A n o t h e r p o s s i b i l i t y m i g h t b e lipid, w h i c h is n e e d e d as a pool of precursors for c h i t i n s y n t h e s i s in t h e Z-2 (Holland, 1978). It s h o u l d b e r e c a l l e d that this effect w a s not o b s e r v e d d u r i n g t h e transition from t h e Z-2 to t h e m e g a l o p a (Fig. 9), s u g g e s t i n g that the l o n g - l a s t i n g m e g a l o p a s t a g e is m u c h less d e p e n d e n t on such reserves. Since the MIH is most p r o b a b l y s e c r e t e d d u r i n g the p o s t m o u l t ( F r e e m a n n & Costlow, 1980), the s t r a n g e s h o r t e n i n g effect in t h e Z-2 d e v e l o p m e n t ( e x p e r i m e n t 4; Fig. 5, u p p e r part) m i g h t be e x p l a i n e d in the f o l l o w i n g way: T h e M I H is, a c c o r d i n g to R a n g a r o (1965), a p e p t i d e . It is also k n o w n that u n d e r starvation, a m i n o a c i d s c a n b e c o m e an important source of e n e r g y , i. e. t h e y a r e c a t a b o l i z e d ( M u n d a y & Poat, 1971). Thus, it is p o s s i b l e that part of n e u r o s e c r e t o r y M I H is u s e d u p d u r i n g e a r l y starvation. This w o u l d , later c h a n g e t h e ratio b e t w e e n t h e M I H a n d the [3-ecdysone s y n t h e s i z e d d u r i n g intermoult (after r e c o m m e n c e m e n t of feeding). This d i s t u r b a n c e in t h e h o r m o n e s y s t e m should i n c r e a s e with the d u r a t i o n of t h e starvation period. S i n c e t h e effects of d e l a y e d i n t e r m o u l t initiation a n d that of c o m p e n s a t i o n for e n e r g y loss in the Z-1 (see above) are far stronger t h a n that of a r e d u c e d M I H pool, the latter m a y b e c o m e v i s i b l e only in the Z2 stage. So far, our e x p e r i m e n t s h a v e s h o w n that e a r l y l a r v a e of H. a r a n e u s h a v e a c o n s i d e r a b l e c a p a c i t y to s u r v i v e in an e n v i r o n m e n t w i t h h i g h l y v a r i a b l e z o o p l a n k t o n c o n c e n t r a tion. T h e t e c h n i q u e u s e d to e v a l u a t e limits a n d c h a n g e s of this p o t e n t i a l (Fig. 1} is also a suitable c o m p l e m e n t a r y m e a n s for a n a l y z i n g d e v e l o p m e n t a l p r o c e s s e s in c r u s t a c e a n larvae. Future i n v e s t i g a t i o n s will h a v e to s c r u t i n i z e this h y p o t h e t i c a l course of e v e n t s u s i n g b i o c h e m i c a l as w e l l as h i s t o l o g i c a l m e t h o d s . S u c h a n a l y s e s m a y also p e r m i t an e x p l a n a t i o n for the point-of-no return: W h y does a s t a r v e d l a r v a b e c o m e u n a b l e to moult? W h i c h i r r e v e r s i b l e d a m a g e is r e s p o n s i b l e for this effect? F u r t h e r m o r e , s i m i l a r studies on different s p e c i e s s h o u l d h e l p to d i s t i n g u i s h b e t w e e n s p e c i e s - s p e c i f i c effects a n d g e n e r a l rules. Finally, l a t e r larval s t a g e s m u s t also b e i n v e s t i g a t e d , s i n c e t h e y m a y r e v e a l r e s p o n s e p a t t e r n s different from t h o s e in t h e first z o e a (cf. Figs 4 a n d 9), a n d t h e y l e a d to the most i m p o r t a n t transition in d e c a p o d d e v e l o p m e n t : to m e t a m o r p h o s i s . A c k n o w l e d g e m e n t s . This research was supported by Bundesministerium ffir Forschung und Technologie (Grant no. MFU-0328/1). We are grateful to the following colleagues for providing food organisms: Dr. W. Greve, Mr. M. Janke, Ms. F. Schorn, and Dr. E. Wahl. Ms. B. L~mmel made the drawings. Our sincere thanks are also due to Dr. J. Markham for correcting the manuscript. The second author is indebted to Studienstiftung des deutschen Volkes, Bonn-Bad Godesberg, for financial support.

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