studies on the effects of temperature on the life history and the tolerance of species .... 3). In short days, it could survive for 2 but not 6 weeks at 10 ~ whereas at. 5 .... interval of limited survival for 4 months in cold years and this may account for ...
HELGOLANDER MEERESUNTERSUCHUNGEN Helgol/inder Meeresunters. 41,329-354 (1987)
Temperature responses of tropical to w a r m temperate Cladophora species in relation to their distribution in the North Atlantic Ocean M. L. Cambridge, A. M. Breeman, S. K_raak & C. van den H o e k Department of Marine Biology, University of Groningen; P.O. Box 14, NL-9750 A A Haren (Gn), The Netherlands
A B S T R A C T : The relationshipbetween distributionboundaries and temperature responses of some North Atlantic Cladophora spedes (Chlorophyta) was experimentally examined under various regimes of temperature, light and daylength. Experimentally determined critical temperature intervals, in which survival, growth or reproduction was limited, were compared with annual temperature regimes (monthly means and extremes) at sitesinside and outside distributionboundaries. The species tested belonged to two phytogeographic groups: (1) the tropicalWest Atlantic group (C. subrnarina: isolate from Curacao) and (2) the amphiatlantic tropicalto w a r m temperate group (C. prolifera: isolatefrom Corsica; C. coelothrix: isolatesfrom Brittany and Curacao; and C. laetevirens: isolatesfrom deep and shallow water in Corsica and from Brittany).In accordance with distribution from tropical to w a r m temperate regions, each of the species grew well between 20-30 ~ and reproduction and growth were limited at and below 15 ~ The upper survival limitin long days was < 35 ~ in all species but high or m a x i m u m growth rates occurred at 30 ~ C. prolifera, restrictedto the tropical margins, had the most limited survival at 35 ~ Experimental evidence suggests that C. submarina is restricted to the Caribbean and excluded from the more northerly American mainland and Gulf of Mexico coasts by sporadic low winter temperatures in the nearshore waters, w h e n cold northerly weather penetrates far south every few years. Experimental evidence suggests that C. prolifera, C. coelothrix and C. laetevirens are restrictedto their northern European boundaries by summer temperatures too low for sufficientgrowth and/or reproduction. Their progressively more northerly located boundaries were accounted for by differences in growth rates over the critical10-15 ~ interval. C. prolifera and C. coelothrix are excluded or restrictedin distributionon North Sea coasts by lethal winter temperatures, again differences in cold tolerance accounting for differences in their distribution patterns. O n the American coast, species were probably restricted by lethal winter temperatures in the nearshore and, in some cases, by the absence of suitable hard substrates in the more equable offshore waters. Isolatesfrom two points along the European coast (Brittany,Corsica) of C. laetevirens showed no marked differences in their temperature tolerance but the Caribbean and European isolatesof C. coelothrix differedmarkedly in their tolerance to low temperatures, the lethal limit of the Caribbean isolatelying more than 5 ~ higher (at ca 5 ~
INTRODUCTION The genus Cladophora consists at least of 42 species and is widely distributed over all oceans from the near polar regions to the tropics. Following taxonomic revisions (van den Hoek, 1963, 1982 b; van den Hoek & Womersley, 1984; Sakai, 1964), they form a group whose systematics and geographic distributions are relatively weU known, although some problems with identifications, and thus misrepresentations of the geo9 Biologische Anstalt Helgoland, Hamburg
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M. L. C a m b r i d g e , A. M. Breeman, S. K r a a k & C. v a n d e n H o e k
g r a p h i c distribution r e m a i n b e c a u s e of the morphological plasticity of s o m e species. In particular, consistent p a t t e m s of g e o g r a p h i c distribution e m e r g e d on N o r t h Atlantic coasts w h e r e e x t e n s i v e north-south coastline's e n a b l e distribution to b e c o m p a r e d with continous t h e r m a l gradients. The coincidence of a distribution b o u n d a r y w i t h t h e s a m e s e a w a t e r isotherm on b o t h t h e A m e r i c a n a n d E u r o p e a n coasts w a s n o t a b l e a n d cont r a s t e d with the vastly different latitudinal r a n g e s of the species on e a c h coast. This l e d to the s u g g e s t i o n t h a t the b i o g e o g r a p h i c distribution of the species w a s a d i r e c t result of limiting w i n t e r or s u m m e r t e m p e r a t u r e s (van d e n Hoek, 1979, 1982 b). Direct e v i d e n c e for the t e m p e r a t u r e control of distribution comes from l a b o r a t o r y studies on the effects of t e m p e r a t u r e on the life history a n d the t o l e r a n c e of s p e c i e s to h i g h or low t e m p e r a t u r e s . Studies on other s e a w e e d s h a v e s h o w n t h a t t e m p e r a t u r e r e s p o n s e s (in c o m b i n a t i o n with light a n d photoperiodic responses) d e t e r m i n e d in the l a b o r a t o r y can e x p l a i n distribution p a t t e r n s along latitudinal g r a d i e n t s (McLachlan & Bird, 1984; Yarish et al., 1984, 1986; a n d other studies r e v i e w e d in v a n d e n H o e k , 1982a, c). Hutchins (1947) p r o p o s e d that t e m p e r a t u r e could act as a limiting factor at the p o l e w a r d a n d e q u a t o r w a r d ends of the distribution r a n g e of a m a r i n e o r g a n i s m as follows: (a) A t the p o l e w a r d b o u n d a r y , t e m p e r a t u r e s m a y be.too cool in s u m m e r for a d e q u a t e g r o w t h a n d / o r reproduction, or too cold in winter to survive e v e n d u r i n g the d o r m a n t phase, or a c o m b i n a t i o n of both. (b) At the e q u a t o r w a r d b o u n d a r y , t e m p e r a t u r e s m a y b e too w a r m in w i n t e r in short days for a d e q u a t e g r o w t h a n d / o r reproduction, or too hot in s u m m e r to survive e v e n in the d o r m a n t p h a s e , or a c o m b i n a t i o n of both. In this p a p e r , the existence of t e m p e r a t u r e limits at the distribution b o u n d a r i e s is e x a m i n e d for four species of Cladolahora in the North Atlantic. O n e of t h e s e species, C. submarina C r o u a n frat. ex S c h r a m m & Maze, b e l o n g s to v a n d e n H o e k ' s (1982 a, b, c) "Tropical w e s t e r n Atlantic distribution group", w h o s e species are r e s t r i c t e d to the C a r i b b e a n . T h e o t h e r t h r e e species, C. prolifera (Roth.) Kiitz., C. coelothrix K~itz. a n d C. laetevirens (Dillw.) K~itz. b e l o n g to v a n d e n H o e k ' s (1982a, b, c) " A m p h i a t l a n t i c tropicalt o - w a r m t e m p e r a t e group with a n o r t h e a s t e r n extension". Species in this g r o u p do not e x t e n d m u c h b e y o n d t h e tropics on A m e r i c a n coasts but occur far into the t e m p e r a t e zone in Europe. T e m p e r a t u r e s limiting growth, sporulation a n d l o n g - t e r m survival h a v e b e e n e x p e r i m e n t a l l y d e t e r m i n e d in u n i a l g a l cultures. T h e s e have b e e n c o m p a r e d with the a n n u a l t e m p e r a t u r e r e g i m e s inside a n d outside the distribution b o u n d a r i e s on t h e E u r o p e a n a n d A m e r i c a n coasts, to d e t e r m i n e w h e t h e r a d v e r s e s u m m e r or w i n t e r temp e r a t u r e s p r e v e n t the species e x t e n d i n g b e y o n d their p r e s e n t b o u n d a r i e s . METHODS Collections of t h e four Cladophora species (Table 1) w e r e i s o l a t e d into u n i a l g a l culture a n d m a i n t a i n e d in t u b e s with 10 ml Provasoli's e n r i c h e d s e a w a t e r .
331
T e m p e r a t u r e responses of Cladophora species Table I. Collection data for Cladophora isolates
Species
Collection
Habitat
Cladophora submarina
Curaqao
Boca Grandi; wavepounded littoral pools eroded from limestone (savahs)
C. prolifera
Calvi, Corsica
Sunlit sea wall, 1 m deep
C. coelothrix
Curacao
Spaanse Water, on mud between mangrove roots entangled with other algae Muddy harbour, low littoral
Roscoff, Brittany C. laetevirens
Calvi, Corsica Calvi, Corsica Roscoff, Brittany
Sunlit sea wall, 1 m deep Under seagrass leaves, 10 m deep lle Ledanet, deep, midlittoral pool on west shore
G r o w t h responses
Growth responses under constant temperature conditions ranging from 5-35 ~ at 5 ~ experimental intervals, were measured on 5 rephcates at short (LD 8:16 h) and long (LD 16:8 h) day conditions, photon fluence rate 40 ~mol. m -2- s-i, using tip cuttings from a single clone for each isolate.For general methods and equipment, see Yarish et al. (i984). Growth at each condition was measured as relative growth rate (RGR). Fragments of approximately equal length, cut from actively growing tips,were placed singly in tubes, and after a settling period of 3 days, were drawn with a camera lucida and measured for length using a Hewlett Packard digitiser(Model 9835A). They were then remeasured 3, 7 and/or 10 days later. Relative growth rate was calculated as RGR = (In 12 - In It) 9 I00 9 T - I = % i n c r e m e n t per day w h e r e 11 = initial length, 12 = length after T days. Upper a n d lower growth hmits were arbitrarily defined as the 5 ~ interval in which the RGR fell below 20 % of the maximum.
experimental
Long-term survival and sporulation Survival potential at extreme temperatures was d e t e r m i n e d as follows: three or six well grown large plants or b r a n c h e s were placed in Erlemeyer flasks with 200 ml of Provasoh enriched seawater a n d set at temperatures close to the lethal limit as determ i n e d from growth experiments (usually 0 or 5 ~ a n d 30 or 35 ~ Plants were gradually b r o u g h t to the e x p e r i m e n t a l temperatures in steps of 5 ~ each lasting a few days. Survival was tested at three photon fluence rates of 10, 20 a n d 40 ~tmol. m -2. s -1 at short (8:1--6h) and/or long (16:8 h) day conditions over 2, 6 a n d 12 w e e k s (see, for example, Fig. 2). Plants tested at 0 ~ were placed in a water bath (___ 0.5 ~ in short days. At all other
332
M. L. C a m b r i d g e , A. M. Breeman, S. Kraak & C. van d e n H o e k
t e m p e r a t u r e s plants w e r e k e p t in controlled e n v i r o n m e n t incubators ( + 1 ~ in l o n g a n d short days. Plants at 35 ~ w e r e t e s t e d in long d a y s only. At the e n d of e a c h test interval, the p l a n t s w e r e r e m o v e d a n d if t h e y a p p e a r e d to b e in g o o d condition, t h e n this w a s r e c o r d e d a n d t h e y w e r e g i v e n no further treatment. However, if t h e y w e r e e x t e n s i v e l y n e c r o s e d or a p p e a r e d d e a d , t h e n their ability to recover w a s tested b y p l a c i n g t h e m in n e w m e d i u m a n d b r i n g i n g t h e m to the o p t i m u m growth t e m p e r a t u r e via 5 ~ s t e p s e a c h lasting a d a y or two at r e d u c e d p h o t o n fluence rate (20 ~mol. m - t . s - l ) . If n o n e w g r o w t h was e v i d e n t after 6 - 8 w e e k s t h e n the t e m p e r a t u r e was d e f i n e d as lethal. U p p e r a n d l o w e r l e t h a l limits w e r e d e f i n e d as the 5 ~ e x p e r i m e n t a l interval w h e r e survival w a s limited (less t h a n 12 w e e k s ) in long a n d short days, respectively. F o r m a t i o n of zooids (zoospores or gametes) was d e t e r m i n e d i n l a r g e p l a n t s w h i c h w e r e k e p t at the e x p e r i m e n t a l t e m p e r a t u r e s r a n g i n g from 5-30 ~ at 5 ~ i n t e r v a l s for 3 months. Distribution and temperature
records
Distribution d a t a as s u m m a r i z e d in Figs 5, 9, 13 a n d 17 h a v e b e e n d e r i v e d from v a n d e n H o e k (1963, 1982b) with additional literature records for C. coelothrix a n d C. proli[era, w h i c h are easily recognized species. Only a few s e l e c t e d r e f e r e n c e s to C. laetevirens h a v e b e e n a d d e d , as it h a s often b e e n confused with o t h e r species, l i t e r a t u r e records b e i n g g e n e r a l l y unreliable. For C. submarine, there are no reliable r e c o r d s at p r e s e n t in other literature sources. T e m p e r a t u r e r e g i m e s h a v e b e e n c o m p i l e d from various sources. W i n t e r (February) a n d s u m m e r (August) isotherms in the North Atlantic O c e a n are s h o w n in F i g u r e I, w h i c h is d r a w n to the s a m e scale as the distribution m a p s so as to facilitate comparisons. Isotherms a r e from t h e U. S. N a v y m a r i n e climatic atlas of the world (1981). A n n u a l t e m p e r a t u r e r e g i m e s (monthly m e a n s a n d ranges) at stations within a n d o u t s i d e distribu/don b o u n d a r i e s w e r e b a s e d on d e t a i l e d local records w h e n e v e r t h e s e w e r e a v a i l a b l e (see l e g e n d to Figs 4, 8, 12 a n d 16 for sources). For other sites, m o n t h l y m e a n s w e r e b a s e d on s e a surface isotherms g i v e n in G o r s h k o v (1978). For o p e n coasts, r a n g e s a r o u n d the m e a n s w e r e e s t i m a t e d from the U. S. N a v y m a r i n e climatic atlas of t h e N o r t h Atlantic O c e a n (1974). This atlas gives m o n t h l y g r a p h s of the cumulative p e r c e n t f r e q u e n c y of s e a w a t e r t e m p e r a t u r e s for s e l e c t e d oceanic sites. T h e t e m p e r a t u r e i n t e r v a l e n c o m p a s sing 50-90 % of all records w a s u s e d to estimate the r a n g e of r e g u l a r l y occurring t e m p e r a t u r e s a b o v e the m e a n ; similarly the interval e n c o m p a s s i n g 10-50 % of all records w a s u s e d to estimate the r a n g e b e l o w the mean. L e n g t h of g r o w i n g s e a s o n T h e p r o g r e s s i v e d e c r e a s e in l e n g t h of the g r o w i n g season at n o r t h e r n b o u n d a r i e s on the E u r o p e a n coast w a s e s t i m a t e d from the p e r i o d with s e a w a t e r t e m p e r a t u r e s e q u a l to or a b o v e 10 ~ (Fig. 18). Two estimates of the l e n g t h of the g r o w i n g s e a s o n w e r e m a d e u s i n g firstly, m e a n m o n t h l y s e a surface t e m p e r a t u r e s (from Gorshkov, 1978), a n d secondly, m i n i m u m t e m p e r a t u r e s [10 % of t e m p e r a t u r e s r e c o r d e d w e r e l o w e r t h a n this v a l u e (from the U. S. N a v y m a r i n e climatic atlas of the North Atlantic O c e a n 1974)] for sites on t h e Atlantic Irish, Scottish a n d N o r w e g i a n coasts. Estimates for Roscoff a n d H e l g o l a n d w e r e b a s e d on local records (see l e g e n d to Fig. 18 for sources).
T e m p e r a t u r e r e s p o n s e s of
Cladophora s p e c i e s
333
FEBRUARY
AUGUST
40
"
20
"
0
"
20
40
Fig. 1. Winter (February) and summer (August) isotherms in the North Atlantic Ocean in comparison with geographic distribution of four Cladophora species as shown in Figs 5, 9, 13 und 17
334
M. L. Cambridge, A. M. Breeman, S. Kraak & C. v a n d e n H o e k RESULTS AND DISCUSSION
In the following section, we consider w h e t h e r temperature responses c a n explain the distribution of the 4 species on N. Atlantic coasts. Their t e m p e r a t u r e responses a n d tolerances in culture are compared with the t e m p e r a t u r e regimes within a n d b e y o n d the n o r t h e r n distribution boundaries. These species occur through the tropics, so there is no southern b o u n d a r y in the N. Atlantic b u t tolerance to tropical t e m p e r a t u r e r e g i m e s is also considered in the question of distribution.
Cladophora submarina This species' geographic r a n g e is restricted to islands of the C a r i b b e a n , a n d Berm u d a is the northernmost record (Fig. 5). There are no records for the A m e r i c a n m a i n l a n d or African coasts. Its habitat also seems to be restricted as it has b e e n f o u n d only i n pools in the u p p e r intertidal on limestone platforms of exposed tropical coasts (van d e n Hoek, 1982b). The constant wash of surf m e a n s that the w a t e r is rapidly replaced so despite the strong tropical sun, water t e m p e r a t u r e s p r o b a b l y do not rise above ambient.
Northern boundary- America A n isolate from Curacao was tested for t e m p e r a t u r e s lirniting survival (Fig. 2) a n d growth (Pig. 3). In short days, it could survive for 2 b u t not 6 weeks at 10 ~ w h e r e a s at 5 ~ death occurred in less t h a n 2 weeks. At 15 ~ plants could persist indefinitely a n d so i n Figure 4, the lower lethal hmit has b e e n s h o w n in the interval 10-15 ~ O n the same figure, temperature curves are s h o w n for B e r m u d a (the northernmost record), Key West, on the southern tip of Florida (N. B.: n e a r e s t record is from the Bahamas, Pig. 5), a n d C e d a r Keys in the Gulf of Mexico, which hes well b e y o n d the boundary. T e m p e r a t u r e s on B e r m u d a are n e v e r lethal b u t at Florida Keys, t e m p e r a t u r e s m a y fall below 15~ d u r i n g a cold w i n t e r (Earle, 1969; Walker et al., 1982), w h i c h is the t e m p e r a t u r e interval below which survival is limited. However, these cold spells last only 1-2 weeks, b e i n g c a u s e d b y intrusions of polar air masses chilIing the extensive shallow bays a n d b a n k waters of Florida. Por example, Walker et al. (1982) recorded temperatures below 15~ lasting a b o u t 10 days in Florida Bay (mean 10.6~ with the
-8 I
. 0 i,
10 short day 20 4O long day
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Fig. 2.Survival of Cladophora submarina isolates from Curaqao. Isolates were tested at 0 ~ in short (LD 8:16 h) days, at 5~ and 10~ in short days und long (LD 16:8 h) days and at 35~ in long days, at 3 photon fluence rates 10, 20 and 40 ~mol.m-2.s -1. Survival intervals were defined as follows: * ; l e s s than 2 weeks; blank bars = 2 weeks but not 6 weeks; stippled bars = 6 weeks but not 12 weeks; grey bars = more than 12 weeks; n.t. = not tested
T e m p e r a t u r e responses of Cladophora species
335
6C
~-o 40
b
,,...-
20
I
5
1"0.
15
I
20 25 temperature (~
I
30
I
35
Fig. 3. Mean relative growth rates (RGR) and standard deviations (n --- 5) of Cladophora submarina from Curaqao measured from 5-35 ~ at 5 ~ intervals. Isolates were grown in long day (o} (LD 16:8 h} and short day (e) (LD 8:1-6 h) conditions with photon fluence rate of 40 ~xnol.m-2.s-t. At some temperatures, growth was also measured at higher (zx = 72 i~mot-m-l.s-1} and lower (a = 20 ~mol- m -2. s- 1) photon fluence rates. Broken line = 20 % of maximum RGR, defining growth limits
m i n i m u m value recorded b e i n g as low as 8.7 ~ At the highest light level tested C. submarina survived for more than 2 weeks at 10 ~ in short b u t not in long days (Fig. 2), so these winter cold spells in ca 11 h daylengths are probably very close to the lethal limit. Further north in the Gulf of Mexico, there would also be a clear lethal limit b e c a u s e temperatures drop well below 10 ~ during the cold spells, a n d this w o u l d b e lethal to C. submarina (see, for example C e d a r Keys, Fig. 4). C. submarina's sensitivity to temperatures above 30~ (Figs 2, 4) m e a n s that in extreme years, m a x i m u m s u m m e r temperatures are also within the r a n g e of limited survival at Florida a n d C e d a r Keys. Thus, in extreme years, the a n n u a l temperature fluctuations could potentially exceed both the u p p e r a n d lower hmit of temperature tolerance in the Gulf of Mexico. T e m p e r a t u r e extremes may also b e a n important c o m p o n e n t of the a p p a r e n t l y specific habitat r e q u i r e m e n t s of this species for wave w a s h e d intertidal pools w h e r e temperatures are m a i n t a i n e d very close to a m b i e n t seawater. This contrasts with the calm s e d i m e n t coasts with lagoons u n d estuaries common along m u c h of the Florida coast a n d the Gulf of Mexico, w h e r e t e m p e r a t u r e s m a y reach extreme values. Low s u m m e r t e m p e r a t u r e s do not restrict the species' northward spread a l o n g the American coast. At B e r m u d a a n d Florida Keys, s u m m e r temperatures r a n g e from 25 to more than 30 ~ corresponding to the temperatures with the m a x i m u m growth rates in long days (Figs 3, 4). This is also the case m u c h further north along the A m e r i c a n coast up to about N. C a r o h n a (compare to Fig. 8}. Sporulation occurred b e t w e e n 15-30 ~ a n d so would not be h m i t i n g to northward extension either.
336
M. L. C a m b r i d g e , A. M. B r e e m a n , S. K r a a k & C. v a n d e n H o e k TEMI~RA~ORE RESPONSES
Pig. 4. Cladophora submarina. Annual temperature regimes as .monthly means and ranges (shaded) at sites within and outside the northern boundaries compared to experimentally determined temperature tolerances. (A) Within boundaries, B - - B Bermuda, means after Gorshkov, 1978, ranges based on U. S. Navy Marine climatic atlas, 1974; e - - e S. Plorida, Key West, means and ranges based on Earle, 1969~ shaded range shows 28-year mean values of monthly maxima and minima; extreme records shown for January and August (vertical lines); 10-day m e a n (| and lowest record (dashed line) during extreme cold spell in January 1981 based on Walker et al., 1982. (B) Outside hound~ies, e - - e Cedar Keys, means and ranges based on Earle (1969); shaded range shows 18-year mean values of monthly maxima and minima; extreme records shown for January and August (vertical lines). Bar diagram shows experimentally determined upper and lower lethal limits and growth limiting temperatures at 40 ~unol-m -2. s -1 for an isolate from Curaqao (from Figs 2 and 3). Upper lethal limit taken from response in long days (LD 16:8 h), lower lethal limit taken from response in short days (LD 8:16 h); * = lethal in less than 2 weeks; blank column = survived 2 weeks but not 6 weeks; stippled column = survived 6 weeks but not 12 weeks; grey column = survived more than 12 weeks; tapering column: growth hmit lies in this interval, in which RGR exceeds 20 % of the maximum; 9 = sporulation within 12 weeks
Potential vs actual distribution C. submarina is o n l y k n o w n f r o m t h e C a r i b b e a n a n d B e r m u d a a n d h a s n o t b e e n f o u n d on t h e A m e r i c a n m a i n l a n d or t h e e a s t e r n Atlantic coasts (Fig. 5). T h e s p e c i e s ' a b s e n c e f r o m t h e W. C a r i b b e a n is a n o t i c e a b l e g a p in its distribution, w h i c h is n o t a t t r i b u t a b l e to l i m i t i n g t e m p e r a t u r e s (Figs 1, 5) b u t to l i m i t e d s a m p l i n g ( v a n d e n H o e k , 1982b, m e n t i o n s 4 Cladophora r e c o r d s in total f r o m W. C a r i b b e a n shores). B e y o n d t h e C a r i b b e a n , its p o t e n t i a l d i s t r i b u t i o n w o u l d i n c l u d e the tropical coasts of W. Africa, C a n a r y Islands a n d t h e E. M e d i t e r r a n e a n w h e r e t e m p e r a t u r e s lie w i t h i n t h e t r o p i c a l r a n g e (Fig. 1).
T e m p e r a t u r e r e s p o n s e s of Cladophora s p e c i e s
337 I
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Fig. 5. Distribution of C1adophora submarina in the N. Atlantic (from v a n d e n Hoek, 1982b). Sampling site of cUltured isolate (* 1 Curaqao) and stations for which temperature regimes are s h o w n in Fig. 4 indicated (within boundaries: * 2 Bermuda, * 3 Florida Keys; outside boundaries: * 4 Cedar Keys)
C1adophora prolifera This species occurs on both sides of the Atlantic in tropical and w a r m temperate zones (Fig. 9). It has been recorded from habitats ranging from shallow waters, either sunlit or deeply shaded by overhangs, to deep reefs off the N. Carolina coast and at depths from 0-70 m. O n European Atlantic coasts, it also grows in the lower littoral,on steep north facing rocks (van den Hoek, 1963, 1982b).
Northern boundary - Europe The northernmost records of C. prolifera are from Clare Island on the west coast of Ireland and the English Channel (Fig.9). The Clare Island record is an old collectionand the sole record from Ireland, the next most northerly records being from the English Channel. Here populations have been consistently collected and thus this site might be regarded as a better indication of the northern boundary. A n isolatefrom Calvi, Corsica, was tested for temperatures limiting survival (]Fig.6) and growth (Fig. 7). In short days, the Corsican isolate could survive for 6 but not 12 weeks at 5 ~ whereas at 0 ~ death occurred in less than 2 weeks, or between 2-6 weeks at lower lightintensity.At I0 ~ plants could persistindefinitely.The lower lethal limitis -thus shown in the interval 5-10~ in Figure 8. In the same figure, it can be seen that
338
M. L. C a m b r i d g e , A. M. Breeman, S. K r a a k & C. v a n d e n H o e k
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temperature ("C) Fig. 7. Mean relative growth rates and standard deviations (n = 5} of Cladophora prolifera from Corsica. Growth conditions described in Fig. 3 m i n i m u m w i n t e r t e m p e r a t u r e s at Roscoff, n e a r the northern b o u n d a r y , c a n fall within this interval of limited survival for 4 months in cold y e a r s a n d this m a y a c c o u n t for the species' rarity at Roscoff. M e a n w i n t e r t e m p e r a t u r e s are n e a r 10~ a n d t h e s e c o u l d b e easily survived, a n d e v e n d u r i n g a cold winter, t e m p e r a t u r e s do not r e a c h 5 ~ w h i c h t e m p e r a ture could b e survived for m o r e than 6 w e e k s . However, it is e a s y to see w h y C. prolifera does not p e n e t r a t e into the North Sea from the t e m p e r a t u r e curve of H e l g o l a n d , s h o w n in Figure 8b. Here, m e a n w i n t e r t e m p e r a t u r e s drop b e l o w 5 ~ for m o r e t h a n 3 months a n d this w a s lethal to p l a n t s in culture. Winter t e m p e r a t u r e s on the w e s t e r n coasts of I r e l a n d a n d Scotland a r e w a r m e r t h a n North S e a t e m p e r a t u r e s (Fig. 1) a n d so do not constitute a lethal b o u n d a r y . H o w e v e r , s u m m e r t e m p e r a t u r e s are close to the l o w e r growth limit. No g r o w t h o c c u r r e d in cultures at 10~ a n d g r o w t h w a s still very slow at 15~ 3 % p e r d a y (Fig. 7). At this g r o w t h rate a p l a n t w o u l d t a k e m o r e t h a n one m o n t h to double in size, so that s u m m e r t e m p e r a t u r e s limiting g r o w t h a r e s u g g e s t e d as limiting n o r t h w a r d extension along Irish a n d Scottish coasts. Sporulation only occurred at 20 a n d 25 ~ in the M e d i t e r r a n e a n isolate u s e d (Fig. 8) a n d these t e m p e r a t u r e r e q u i r e m e n t s for spornlation w o u l d not b e m e t in a r e a s closer to the n o r t h e r n b o u n d a r y . Northern boundary - A m e r i c a No isolate w a s t e s t e d from the A m e r i c a n side of the Atlantic a n d t h e r e f o r e only tentative s u g g e s t i o n s are g i v e n on the n a t u r e of the n o r t h e r n b o u n d a r y on t h e A m e r i c a n coast. The n o r t h e r n m o s t r e c o r d for C. prolifera is N e w River, N o r t h Carolina, a n d it is also c o m m o n l y found on the a d j a c e n t O u t e r Shelf reefs (Schneider, 1976). In F i g u r e 8,
T e m p e r a t u r e r e s p o n s e s of C. PROLIFERA
Cladophora species
339
TEMPERATURERESFONSE$ CORSICANISOLATE
Fig. 8. Cladophora prolffera_Annual temperature regimes as monthly means and ranges {shaded) at sites within and outside the northern boundaries compared to experimentally determined temperaturn tolerances. (A) Within boundaries: 9 9 Roscoff, Brittany, means after I'I.S.T.P.M.,Roscoff (1976), ranges based on U.S. Navy Marine climatic atlas, 1974; e - - e N. Carolina inshore, Wrightsville Beach, means after Kapraun (1978), January and February means for a cold year ((D) and extreme records for January, February and August {verticallines) based on data from 1976 (Kapraun & Zechman, 1982); m - - m N. Carolina offshore,Outer Shelf reefs,means after Gorshkov
{1978), ranges based on U. S. Navy Marine climatic atlas {1974). (B) Outside boundaries: 9 Helgoland, means after We9 {1978}, ranges based on U. S. Navy Marine climatic atlas {1974}; e - - e inshore Chesapeake Bay at Gloucester Point, Virginia, means only (after Humm, 1979). Bar diagram shows experimentally determined upper and lower lethal limits and growth limiting temperatures (details as in Fig. 4) for an isolate from Corsica (from Figs 6 and 7) t e m p e r a t u r e curves are shown for Wrightsville Beach, n e a r N e w River Inlet a n d for the N. Carolina O u t e r Shelf reefs. Winter t e m p e r a t u r e s are m u c h lower at the inshore Wrightsville Beach site, a v e r a g i n g 6-7 ~ for 2 months during cold winters (Kapraun & Z e c h m a n , 1982} a n d this w o u l d b e close to the lethal limit for the Corsican isolate (Pigs 6, 8). O n the O u t e r Shelf reefs, t e m p e r a t u r e s are favourable for growth most of the y e a r (Pigs 7, 8) a l t h o u g h w i n t e r minima of 8 - 1 0 ~ h a v e b e e n r e c o r d e d (Peckol & Searles, 1984}. T h e s e reefs, providing the only h a r d substrate for a l g a e in the w a n n e r offshore w a t e r s do not e x t e n d further north. B e y o n d the n o r t h e r n boundaries, for e x a m p l e in C h e s a p e a k e Bay (Fig. 8), even a v e r a g e w i n t e r t e m p e r a t u r e s are b e l o w 5~ for a b o u t 3 months a n d this w o u l d b e lethal for the Corsican isolate (Pig. 8). In the a b s e n c e of t e m p e r a t u r e r e s p o n s e s for an A m e r i c a n isolate, w e tentatively c o n c l u d e that this northern b o u n d a r y is a w i n t e r lethal one, particularly since there is a r a p i d decline in winter t e m p e r a t u r e s within a relatively short l e n g t h of coast north of this b o u n d a r y in the C a p e Hatteras a r e a (Fig. 1). Inshore s u m m e r t e m p e r a t u r e s w o u l d be optimal for growth of the Corsican isolate m u c h further north {Figs 1, 8) a n d this is in
340
M. L. Cambridge, A. M. Breeman, S. Kraak & C. v a n d e n H o e k
contrast to the situation on the l~uropean northern boundary, which is set by a s u m m e r growth limit.
Potential vs actual disfldbution C. prolifera's distribution range, from tropical to w a r m temperate zones, has gaps for the central and western Caribbean and the Gulf of Mexico, where the species might be expected to occur in view of their tropical temperatures (Figs I, 9). However, the limited survival potential of the Corsican isolate above 30 ~ (Fig. 6) suggests that high temperatures might be responsible.
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Fig. 9. Distribution of Cladophora proliferain the North Atlantic (from van den Hoek, 1963, 1982b) (o = isolatedrecord from 1912). Additional records: tropicalWest Africa (Lawson & John, 1982)~ Cap Blanc (Lawson & John, 1977); Morocco (Gayral, 1958); Canary Islands (B6rgesen, 1925; GilRodriguez & Alfonso-Carillo, 1980); Azores (Feldmann, 1946); Madeira (Levring, 1974); Portugal (Ardr4, 1970); N W Spain (Perez-Cirera, 1975; Neill, 1978); Pelagie Islands, south of Sicily (CineUi et al.,1976); Afboran Sea (Conde, 1984); eastern Sicily(Cormaci & Furnari, 1979); Rhodos (Diannelidis et al., 1977); Israel (Lipkin & Safriel, 1971); Tunesia (Metier & Mathieson, 1981). Sampling site of cultured isolate (* 1 Corsica) and stations for which temperature regimes are shown in Fig. 8 indicated (within boundaries: * 2 Roscoff, * 3 N. Carolina; outside boundaries: * 4 Helgoland, * 5 Chesapeake Bay)
Cladophora
coelothrix
This species occurs on both sides of the Atlantic, in tropical and w a r m temperate zones (Fig. 13). It has often been recorded from m u d d y habitats; in the tropics, from mangrove roots and forming cushions on the m u d d y tidal flats between m a n g r o v e trees
T e m p e r a t u r e r e s p o n s e s of Cladophora s p e d e s
341
(van d e n Hoek, 1982b) a n d in t e m p e r a t e regions, from m u d d y estuaries a n d h a r b o u r s (van d e n Hoek, 1963}, such as La Rance, Brittany as well as bays, such as G a l w a y Bay, Ireland. Northern boundary - Europe N o r t h e r n m o s t records in Europe are from W. Ireland on the Atlantic coast a n d No rbhumberland on the North Sea coast {Pig. 13}. The N o r t h u m b e r l a n d r e c o r d is an old collection a n d the sole record for the North Sea, the next most northerly record b e i n g from the Irish S. W. coast (Guiry, 1978}. Here populations h a v e b e e n consistently collected a n d thus this site m i g h t b e r e g a r d e d as a b e t t e r indication of b o u n d a r y populations. A n isolate from Roscoff, Brittany, w a s tested for t e m p e r a t u r e s limiting survival {Fig. 10a) a n d growth (Fig. 11). In short days c o r r e s p o n d i n g to winter conditions, the Roscoff isolate survived p e r m a n e n t l y at 5~ w h e r e a s at 0~ it survived for 6 w e e k s b u t not 12 w e e k s . T h e h g h t intensity did not affect survival m u c h b u t d a y l e n g t h did.. Accordingly, the lower lethal limit for the Roscoff isolate is shown in the interval 0 - 5 ~ in F i g u r e 12. In the s a m e figure, it can b e seen that w i n t e r t e m p e r a t u r e s for the west of I r e l a n d r e m a i n a b o v e 5 ~ e v e n in a cold winter a n d a b o v e 10 ~ in a w a r m winter. Thus, e v e n cold winters could b e easily survived b y subhttoral populations of C. coelothrix a n d w e s u g g e s t that winter t e m p e r a t u r e s do not p r e v e n t the species e x t e n d i n g further north.
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