and Salvagens from Levring (1974}; for Libya from Nizamuddin et al. (1979}. See text to .... Nizamuddin, M., West, J. A. & Mefiez, E. G., 1979. A list of algae from ...
HELGO~DER MEERESUNTERSUCHUNGEN I-Ielgol~inder Meeresunters. 38, 349-363 (1984)
Temperature r e s p o n s e s of s o m e North Atlantic Cladophora species ( C h l o r o p h y c e a e ) in relation to their g e o g r a p h i c distribution* M. Cambridge, A. M. Breeman, R. van Oosterwijk & C. v a n d e n H o e k Department of Marine Biology, Biological Centre, University of Groningen; P.O. Box 14, NL-9750 A A Haren (Gn], The Netherlands
ABSTRACT: The temperature responses for growth and survival have b e e n experimentally tested for 6 species of the g r e e n algal g e n u s Cladophora (Chlorophyceae; Cladophorales) (all isolated from Roscoff, Brittany, France, one also from Connecticut, USA), selected from 4 distribution groups, in order to determine which p h a s e in the annual temperature regime might prevent the spread of a species beyond its present latitudinal range on the N. Atlantic coasts. For five species geographic limits could be specifically defined as due to a growth limit in the growing season or to a lethal limit in the a d v e r s e s e a s o n . These species were: (1) C. coelothrix (Amphiatlantic tropical to w a r m temperate), with a northern boundary on the European coasts formed by a summer growth limit near the 12 °C August isotherm. On the American coasts sea temperatures should allow its occurrence further north. (2) C. vagabunda (Amphiatlantic tropical to temperate), with a northern boundary formed by a summer growth limit near the 15 °C August isotherm on both sides of the Atlantic. (3) C. dalmatica, as for C. vagabunda, (4) C. hutchinsiae (Mediterranean-Atlantic warm temperate), with a northern boundary formed by a summer growth limit near the 12 °C August isotherm, a n d possibIy also a winter lethal limit near the 6°C February isotherm; and a southern boundary formed by a southern lethal limit near the 26 °C August isotherm. It is absent from the warm temperate American coast because its lethal limits, 5 ° and 30 °C, are regularly r e a c h e d there. (5) Preliminary data for C. rupestris {Amphiatlantic temperate}, suggest the southeastern boundary on the African coast to be a summer lethal limit near the 26 °C August isotherm; the southwestern boundary on the A m e r i c a n coast lies on the 20 °C August isotherm. For one species, C. albida, the experimental growth and survival range was wider than expected from its geographic distribution, and reasons to account for this are suggested. INTRODUCTION V a n d e n H o e k (1982a) p r o p o s e d t h a t t h e g e o g r a p h i c d i s t r i b u t i o n b o u n d a r i e s of b e n t h i c a l g a l s p e c i e s c o u l d b e d e f i n e d a c c o r d i n g to l i m i t i n g t e m p e r a t u r e s , e i t h e r for g r o w t h a n d r e p r o d u c t i o n i n t h e f a v o u r a b l e g r o w i n g s e a s o n or s u r v i v a l i n t h e a d v e r s e s e a s o n . T h i s d e v e l o p e d f r o m t h e p r o p o s i t i o n of H u t c h i n s (1947) r e g a r d i n g m a r i n e z o o g e o g r a p h i c l i m i t s . T h e r a n g e of t e m p e r a t u r e at t h e b o u n d a r i e s of a s p e c i e s ' g e o -
* Paper p r e s e n t e d at the S e a w e e d Biogeography Workshop of the International Working Group on S e a w e e d Biogeography, held from 3-7 April, 1984 at the Department of Marine Biology, University of Groningen (The Netherlands). Convenor: C. van den Hoek. © Biologische Anstalt Helgoland, Hamburg
350
M. C a m b r i d g e , A. M. Breeman, R. v a n Oosterwijk & C. v a n d e n Hoek
g r a p h i c d i s t r i b u t i o n w o u l d a p p e a r to be the best i n d i c a t i o n of its t e m p e r a t u r e limits in the n a t u r a l e n v i r o n m e n t . Thus, b y e x a m i n i n g s u m m e r a n d w i n t e r isotherms at b o u n d aries, a r a n g e of t e m p e r a t u r e s c a n b e inferred w h i c h the species must tolerate for it to occur at that b o u n d a r y . T h e s e i n f e r r e d t e m p e r a t u r e s m a y t h e n b e c o m p a r e d to experim e n t a l l y d e t e r m i n e d limits to growth, r e p r o d u c t i o n a n d survival i n order to suggest w h i c h part of the a n n u a l t e m p e r a t u r e r e g i m e is l i m i t i n g the s p r e a d of a species b e y o n d its b o u n d a r i e s . The b o u n d a r y m a y b e t h e n d e f i n e d specifically as d u e to a growth (or reproduction) limit i n the g r o w i n g s e a s o n a n d / o r a lethal limit i n the adverse season. Species of the g e n u s Cladophora (Chlorophyceae, Cladophorales) have b e e n selected for this study because, following t a x o n o m i c revisions of the g e n u s (van d e n Hoek, 1963, 1979, 1982b; v a n d e n Hoek & Womersley, 1984), they form a group of species whose systematics a n d g e o g r a p h i c distributions are n o w r e a s o n a b l y well d o c u m e n t e d for large parts of the world's sea coasts. This p a p e r reports the results of e x p e r i m e n t a l testing of six species of Cladophora b e l o n g i n g to four d i s t r i b u t i o n groups, n a m e l y C. coelothrix b e l o n g i n g to the Amphiatlantic, tropical to w a r m t e m p e r a t e group; C. v a g a b u n d a a n d C. dalmatica to the A m p h i a t l a n t i c , tropical to t e m p e r a t e group; C. rupestris a n d C. albida to the Amphiatlantic t e m p e r a t e group; a n d C, h u t c h i n M a e to the M e d i t e r r a n e a n - A t l a n t i c warm t e m p e r a t e group. MATERIAL AND M E T H O D S Isolates of 6 Cladophora species collected at Roscoff, France, a n d one isolate from Connecticut, USA (Table 1), were c u l t u r e d in tubes with 10 mls of Provasoli enriched s e a w a t e r m e d i u m . Growth responses u n d e r c o n s t a n t t e m p e r a t u r e conditions r a n g i n g from 5 °-30 °C were m e a s u r e d on 5 or 10 replicates at short (8:16 h; light:dark) a n d long (16:8 h) day conditions, p h o t o n flux d e n s i t y 40 ~t E m -2 s -1, u s i n g c l o n e d material from tip cuttings, except for C. hutchinMae for w h i c h sporelings were used. For g e n e r a l m e t h o d s a n d e q u i p m e n t for cultivation, see Yarish et al. (1984). Growth was m e a s u r e d as relative growth rate (RGR); after c u t t i n g from actively g r o w i n g tips, f r a g m e n t s of a p p r o x i m a t e l y e q u a l l e n g t h were p l a c e d singly i n tubes, a n d after a s e t t l i n g p e r i o d of 3 days, d r a w n with a camera lucida a n d m e a s u r e d for length, or i n the case of C. coelothrix, area, u s i n g a H e w l e t t P a c k a r d digitiser (Model 9835A). They Table 1. Cladophora spp. isolates from Roscoff, France (May 1983), tested for temperature responses Cladophora spp. C. albida C. C. C. C. C.
coe]othn'x dalmatica hutchinsiae rupestris vagabunda
Isolate code A 83.4 A 83.C * C 83.14 D 83.13 H 83.8 R 83.9 V 83.17
Collection site
Midlittoral tide pool Lagoon, shallow sublittoral Muddy harbour, shaded low littoral rocks Artificial pool, filling each day with tide Exposed coast, shaded low littoral pool Exposed coast, deep shaded low littoral pool Artificial pond, estuary, permanently filled with water, eutrophic
* Collected from Connecticut, U.S.A., January 1983
T e m p e r a t u r e responses of Cladophora species
351
were t h e n r e d r a w n 3, 7 a n d / o r 10 days later for the s u b s e q u e n t l e n g t h / a r e a m e a s u r e ment{s}, d e p e n d i n g on the size of plants. Relative growth rate was c a l c u l a t e d as RGR = ln(12 - ll)100/T = % i n c r e m e n t p e r d a y where 11 = initial length, 12 = final l e n g t h after T days. Survival was tested at 0 °C a n d 35 °C a n d for some species - 5 °C. For 0 °C, 5 t u b e s each c o n t a i n i n g a s i n g l e p l a n t w e r e p l a c e d at light i n t e n s i t i e s of 10 a n d 20 ~t E m -2 s - 1 at short day (8:16 h) conditions. Plants were e x a m i n e d 2 m o n t h s later for v i a b i l i t y or s i g n s of d a m a g e such as cell necrosis, In species w h e r e there was d e a t h a n d / o r necrosis in some of the replicates, the p l a n t s were c h e c k e d for their ability to recover by setting them at 20 °C after i n c r e a s i n g the t e m p e r a t u r e b y 5 °C intervals, each lasting 4 days. For 5 °C, tubes with s p o r e l i n g s were set at progressively lower t e m p e r a t u r e s , b e i n g h e l d at 5 °C a n d t h e n 0 °C for 2 w e e k s each. T h e m e d i u m w a s t h e n d r a i n e d from the tubes, a n d they were w r a p p e d in a l u m i n i u m foil to e x c l u d e light a n d set i n a freezer at -- 5 °C. After 2 months, the p l a n t s were t h a w e d for 24 h at 5 °C, still with light excluded. The t u b e s were t h e n refilled with m e d i u m a n d after 2 w e e k s at 5 °C p l a c e d at 15 °C to test for active growth. At 35 °C, 5 replicates of 1 p l a n t per t u b e of 10 mls PES w e r e set at 35 °C (16:8 h) after progressively i n c r e a s i n g the t e m p e r a t u r e b y 5 °C intervals, each lasting 4 days. S i g n s of d a m a g e were n o t e d a n d mortality scored after 1-2 weeks, b u t the trial was c o n t i n u e d for 2 months for those species tolerant of these h i g h temperatures. -
RESULTS G e n e r a l i s e d growth a n d survival characteristics of the s e v e n species i n v e s t i g a t e d are g i v e n in Figure 1. Species have b e e n a r r a n g e d according to the d i s t r i b u t i o n groups d i s t i n g u i s h e d by v a n d e n Hoek (1979, 1982a, b). Figure 2 gives the t e m p e r a t u r e - g r o w t h curves for 6 strains ( r e p r e s e n t i n g 5 species) for w h i c h growth rates are a v a i l a b l e over the t e m p e r a t u r e r a n g e of 5 °-30 °C (or 35 °C). In Figures 1 a n d 2, Cladophora coelothrix as a r e p r e s e n t a t i v e of the a m p h i a t l a n t i c tropical to w a r m t e m p e r a t e group, grew best at h i g h t e m p e r a t u r e s (25 °-35 °C) b u t could not tolerate low (0 °-5 °C) temperatures, the actual lethal t e m p e r a t u r e d e p e n d i n g on light period a n d light intensity, with i n c r e a s e d t o l e r a n c e to low t e m p e r a t u r e s i n dim light a n d short days. Species i n the a m p h i a t l a n t i c tropical to t e m p e r a t e group (C. vagabunda, C. dalmatica) were also able to grow best at h i g h t e m p e r a t u r e s b u t survived low t e m p e r a tures, at least lower t h a n 0 °C. The a m p h i a t l a n t i c t e m p e r a t e species s h o w e d two forms of temperature response. The first, r e p r e s e n t e d by C. rupestris s h o w e d growth at lower t e m p e r a t u r e s b u t no survival at h i g h t e m p e r a t u r e s with the lethal t e m p e r a t u r e n e a r 30 °C. The second form of response was e x h i b i t e d by C. albida with good growth from m e d i u m (15°C) to high (30°C) t e m p e r a t u r e s a n d a very wide survival r a n g e b e y o n d - 5 °C a n d 35 °C. This response is similar to those of species with a tropical to t e m p e r a t e distribution. The species r e p r e s e n t i n g the w a r m t e m p e r a t e M e d i t e r r a n e a n - A t l a n t i c group (C. hutchinsiae) h a d a relatively n a r r o w o p t i m a l growth (15 °-25 °C) a n d survival (5~-30°C) r a n g e and, as i n the tropical to w a r m t e m p e r a t e species, the lower lethal t e m p e r a t u r e could be modified by light period a n d intensity.
352
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DISCUSSION G e o g r a p h i c p a t t e r n s of d i s t r i b u t i o n of six Cladophora s p e c i e s (Figs 3 - 8 ) a n d o c e a n i s o t h e r m s at t h e n o r t h e r n a n d s o u t h e r n b o u n d a r i e s of d i s t r i b u t i o n a r e c o m p a r e d h e r e in o r d e r to t e s t t h e v a l i d i t y of i n t e r p r e t i n g s u c h p a t t e r n s in t e r m s of t h e t e m p e r a t u r e r e q u i r e m e n t s for g r o w t h or s u r v i v a l .
Cladophora coelothrix T h i s s p e c i e s " o p t i m u m t e m p e r a t u r e s for g r o w t h (25 ° - 3 5 °C) s h o w n in F i g u r e 2 a g r e e w i t h its o c c u r r e n c e i n t h e tropics. T h e h i g h g r o w t h r a t e of C. coelothrix at 35 °C p r o b a b l y r e f l e c t s its o c c u r r e n c e in p r o t e c t e d t r o p i c a l l a g o o n s w h e r e t e m p e r a t u r e s m a y rise c o n s i d e r a b l y a b o v e 3 0 ° C , as g r o w t h of e v e n strictly t r o p i c a l s p e c i e s t e n d s to b e dep r e s s e d at 35 °C (see M c L a c h l a n & Bird, 1984). Its g r o w t h p o t e n t i a l at 15 ° - 2 0 °C (Fig. 2) p e r m i t s its o c c u r r e n c e in t h e w a r m t e m p e r a t e M e d i t e r r a n e a n A t l a n t i c R e g i o n w h e r e t h e s e t e m p e r a t u r e s do o c c u r in s u m m e r . A t t h e N.E. b o u n d a r y (Europe) in E i r e (Fig. 3), s i t u a t e d at t h e 8 °C F e b r u a r y i s o t h e r m a n d at t h e 14 °C A u g u s t i s o t h e r m , t h e s p e c i e s n e e d s to s u r v i v e w i n t e r t e m p e r a t u r e s of a b o u t 7 °C, w h i c h is a b o v e t h e e x p e r i m e n t a l l y d e t e r m i n e d l e t h a l l i m i t ( b e t w e e n 0 ° and 5 °C) i n d i c a t i n g t h a t this n o r t h e r n b o u n d a r y is n o t a l e t h a l o n e . In s u m m e r "sufficient" g r o w t h m u s t o c c u r at a b o u t 12 °C (Fig. 3) a n d t h e e x p e r i m e n t a l l y d e t e r m i n e d limit for
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Fig. 3. Cladophora coelothrix ( A m p h i a t l a n t i c tropical to w a r m t e m p e r a t e distribution}. M a p s h o w s g e o g r a p h i c d i s t r i b u t i o n o n N. A t l a n t i c coasts, after v a n d e n H o e k (1963, 1982b). C o n t i n u o u s d i s t r i b u t i o n s h o w n as e - o , i n d i v i d u a l r e c o r d s as (e), h e r e for N o r t h u m b e r l a n d . F e b r u a r y (F} a n d A u g u s t (A) i s o t h e r m s at b o u n d a r i e s a n d in tropics b a s e d o n S v e r d r u p et al. (1942) a n d a d d i t i o n a l d a t a s u m m a r i s e d in v a n d e n H o e k (1982a). Bar d i a g r a m s c o m p a r e t h e r m a l t o l e r a n c e inferred (I) f r o m d i s t r i b u t i o n a l r a n g e w i t h e x p e r i m e n t a l l y d e t e r m i n e d t h e r m a l limits (E, for e x p l a n a t i o n of s y m b o l s s e e Fig. 1). U p p e r d i a g r a m (I) s h o w s t e m p e r a t u r e r a n g e s o v e r w h i c h " s u f f i c i e n t " growth ( o p e n bar} a n d / o r s u r v i v a l {single line} m u s t o c c u r to e n a b l e p e r s i s t e n c e t h r o u g h o u t t h e distribution r a n g e , b a s e d o n A u g u s t (A) a n d F e b r u a r y (F} i s o t h e r m s .at v a r i o u s n o r t h e r n b o u n d a r i e s a n d in tropics. I n f e r r e d t h e r m a l r a n g e s d e t e r m i n e d a s follows: l o w e s t t e m p e r a t u r e at w h i c h s p e c i e s m u s t b e a b l e to s u r v i v e d e r i v e d f r o m l o w e s t F i s o t h e r m at a n y of t h e N b o u n d a r i e s m o d i f i e d , as in v a n d e n H o e k (1982a, p. 37), to a c c o u n t for s u r v i v a l in w i n t e r s c o l d e r t h a n a v e r a g e (thus N o r t h u m b e r l a n d : 5 °C Feb. -- 1 °C = 4 °C); l o w e s t t e m p e r a t u r e w h i c h m u s t s u p p o r t " s u f f i c i e n t " g r o w t h d e r i v e d from l o w e s t A i s o t h e r m at a n y of t h e N b o u n d a r i e s m o d i f i e d , as in v a n d e n H o e k (1982a, p. 37}, to account for " s u f f i c i e n t " g r o w t h in s u m m e r s c o l d e r t h a n a v e r a g e ( t h u s Eire: 14 °C A u g . - 2 ° C = 12°C). H i g h e s t t e m p e r a t u r e s w h i c h m u s t b e s u r v i v e d in s u m m e r a n d m u s t a l l o w " s u f f i c i e n t " growth in w i n t e r d e r i v e d f r o m tropical A a n d F i s o t h e r m s , r e s p e c t i v e l y , m o d i f i e d , as in v a n d e n H o e k (1982a, p. 37}, to a c c o u n t for y e a r s w a r m e r t h a n a v e r a g e (thus: 2 9 ° C A u g . + 3 ° C = 3 2 ° C in A u g u s t , 27°C Feb. + 2 °C = 2 9 ° C in F e b r u a r y )
T e m p e r a t u r e responses of Cladophora species
355
"sufficient growth" (here arbitrarily d e f i n e d as 20 % of the m a x i m a l growth rate) lies b e t w e e n 10 ° a n d 15 °C (Fig. 3). Therefore this b o u n d a r y is best e x p l a i n e d as a n o r t h e r n growth b o u n d a r y (and not as a lethal b o u n d a r y n e a r the 8°C w i n t e r isotherm as s u g g e s t e d by v a n d e n Hoek, 1979, 1982a). The o u t l y i n g record from N o r t h u m b e r l a n d , b a s e d on a collection from 1902, is on the 14 °C A u g u s t isotherm as i n Eire (Fig. 3) b u t also on the 5 °C F e b r u a r y isotherm. Here p l a n t s w o u l d h a v e to survive 4 °C i n w i n t e r a n d since the e x p e r i m e n t a l l y d e t e r m i n e d lethal limit lies b e t w e e n 0 ° a n d 5 °C a w i n t e r lethal b o u n d a r y m a y operate here i n c o m b i n a t i o n with a s u m m e r growth b o u n d a r y . The n o r t h w e s t e r n b o u n d a r y (America) occurs i n the Gulf of Mexico (15 °C February, 29 °C August; Fig. 3) w h e r e C, coelothrix must survive at least 13 °C i n winter. This is far above the e x p e r i m e n t a l lethal limit ( b e t w e e n 0 ° a n d 5 °C). It must also b e able to grow "sufficiently" at least at 27 °C in s u m m e r a n d a g a i n "sufficient" growth occurred at m u c h lower t e m p e r a t u r e s (Fig. 3). Thus n e i t h e r w i n t e r nor s u m m e r t e m p e r a t u r e s a p p e a r to b e l i m i t i n g the n o r t h w a r d spread of C. coelothrix either further into the Gulf of Mexico or northward along the Florida coast. The a n s w e r m a y be i n the u n u s u a l t e m p e r a t u r e regime of the e a s t e r n coast of North America. Inshore l a g o o n a l waters reach w i n t e r t e m p e r a t u r e s as low as 0 °C or less far to the south, a n d e v e n in the S o u n d s of N. C a r o l i n a ( - 35 °N) water t e m p e r a t u r e s drop to 0 °C i n w i n t e r (Searles, 1984). It is therefore likely that i n t e r m i t t e n t low lethal t e m p e r a t u r e s (~ 0 °C) p r e v e n t C. coelothrix from occurring far to the north a l o n g the w a r m t e m p e r a t e coasts of N.E. A m e r i c a in the l a g o o n a l habitats where this species u s u a l l y occurs. However, one w o u l d expect C. coelothrix to occur more to the north t h a n its p r e s e n t N.E. A m e r i c a n n o r t h e r n m o s t record i n s o u t h e r n Florida (van d e n Hoek, 1982b). We t h i n k that the scanty p h y c o l o g i c a l e x p l o r a t i o n of the coasts b e t w e e n N. Carolina a n d S. Florida, c o m b i n e d with the notorious taxonomic difficulties in the g e n u s Cladophora, are r e s p o n s i b l e for the lack of records, at least i n the s o u t h e r n m o s t parts of these coasts. Thus, the n o r t h e r n b o u n d a r y of C. coelothrix i n the W. Atlantic O c e a n is p r o b a b l y a lethal b o u n d a r y . In that case, C. coelothrix has a n o r t h e r n composite b o u n d a r y i n the N. Atlantic Ocean: a lethal b o u n d a r y i n the W. Atlantic, a n d a growth b o u n d a r y i n the E. Atlantic. E x p e r i m e n t a l e v i d e n c e points to the existence of c o m p a r a b l e composite n o r t h e r n b o u n d a r i e s for other species in the tropical to w a r m t e m p e r a t e d i s t r i b u t i o n - g r o u p : Dictyota dichotoma, Polysiphonia ferulacea (van d e n Hoek, 1982c), a n d Centroceras d a v u l a t u m (van d e n Hoek, 1982a).
Cladophora vagabunda This species' optimal t e m p e r a t u r e s for growth (15 °-30 °C) (Figs 2, 4) a n d its survival r a n g e b e y o n d 0 °C a n d 35 °C are in a c c o r d a n c e with its w i d e d i s t r i b u t i o n from t e m p e r a t e to tropical regions. O n its n o r t h e a s t e r n b o u n d a r y (Fig. 4) i n the Baltic Sea (2 °C February, 15 °C August), C. vagabunda must survive at least 1 °C i n w i n t e r b u t t e m p e r a t u r e s d o w n to 0 °C could b e survived, t h e r e b y i n d i c a t i n g that low w i n t e r t e m p e r a t u r e s do not set the n o r t h e r n boundary. However s u m m e r t e m p e r a t u r e s (13°C) are w i t h i n the interval w h e r e the growth rate falls b e l o w 20 % of the m a x i m u m ( b e t w e e n 10 °-15 °C) a n d so a s u m m e r growth limit is i n d i c a t e d o n the I5 °C A u g u s t isotherm. O n the n o r t h w e s t e r n b o u n d a r y i n the Gulf of St L a w r e n c e {Fig. 4, -- 1 °C February, 15 °C August), C. vagabunda w o u l d have to survive at least - 2 °C i n w i n t e r on the o p e n
356
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Cladophora dalmatica As for C. vagabunda, this species' w i d e t e m p e r a t u r e r a n g e s for growth a n d survival (Figs 2, 5) are reflected i n its wide g e o g r a p h i c r a n g e from tropical to t e m p e r a t e regions, a l t h o u g h its n o r t h e r n e x t e n s i o n is slightly more restricted. G r o w t h at h i g h t e m p e r a t u r e s (25 °-30 °C) is consistent with d i s t r i b u t i o n t h r o u g h the tropics, a l t h o u g h the m a x i m u m was m e a s u r e d at 25 °C, a little lower t h a n that of C, vagabunda at 30 °C. The n o r t h e a s t e r n b o u n d a r y in the Baltic Sea on the 2 °C F e b r u a r y a n d 15 °C A u g u s t isotherms (Fig. 5) a g a i n a p p e a r s to b e a s u m m e r growth b o u n d a r y , as for C. vagabunda, since t e m p e r a t u r e s lower t h a n the w i n t e r t e m p e r a t u r e s at the b o u n d a r y were still survived (i.e. 0 °C) (Fig. 4). O n the n o r t h w e s t e r n b o u n d a r y n e a r Boston, the 15 °C A u g u s t isotherm passes d o w n the coast from N e w f o u n d l a n d to C a p e Cod, so that the b o u n d a r y isotherm for C. dalmatica is the same as for the more northerly occurring C. vagabunda. As for the E u r o p e a n coast a s u m m e r growth limit n e a r the 15 °C A u g u s t isotherm w o u l d a p p l y for the A m e r i c a n coast•
358
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Cladophora rupestris T h i s s p e c i e s ' u p p e r l e t h a l t e m p e r a t u r e b e t w e e n 25 ° a n d 30 °C a n d s u r v i v a l b e y o n d - 5 °C is c o n s i s t e n t w i t h its a b s e n c e f r o m t h e t r o p i c s a n d e x t e n s i o n i n t o c o l d t e m p e r a t e regions• A t its n o r t h e r n b o u n d a r i e s o n b o t h s i d e s of t h e A t l a n t i c (Fig. 6), w i n t e r t e m p e r a t u r e s a r e a b o v e - 5 °C, w h i c h is t h e l o w e s t t e m p e r a t u r e so f a r t e s t e d w h i c h w a s still s u r v i v e d . W
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