A. M. Breeman

RELATIVE IMPORTANCE OF TEMPERATURE AND OTHER FACTORS IN DETERMINING GEOGRAPHIC BOUNDARIES OF SEAWEEDS - EXPERIMENTAL AND PHENOLOGICAL EVIDENCE

Experimentally determined ranges of thermal tolerance and requirements for completion of the life history of some 60 seaweed species from the North Atlantic Ocean were compared with annual temperature regimes at their geographic boundaries. In all but a few species, thermal responses accounted for the location of boundaries. Distribution was restricted by: (a) lethal effects of high or low temperatures preventing survival of the hardiest life history stage (often microthalli), (b) temperature requirements for completion of the life history operating on any one process (i.e. [sexual] reproduction, formation of macrothalli or blades), (c) temperature requirements for the increase of population size (through growth or the formation of asexual propagules). Optimum growth/reproduction temperatures or lethal limits of the non-hardiest stage (often macrothalli) were irrelevant in explaining distribution. In some species, ecotypic differentiation in thermal responses over the distribution range influenced the location of geographic boundaries, but in many other species no such ecotypic differences were evident. Specific daylength requirements affected the location of boundaries only when interacting with temperature. The following types of thermal responses could be recognised, resulting in characteristic distribution patterns: (A) Species endemic to the (warm) temperate eastern Atlantic had narrow survival ranges (between ca 5 and ca 25°C) preventing occurrence in NE America. In species with isomorphic life histories without very specific temperature requirements for reproduction, northern and southern boundaries in Eur/Africa are set by lethal limits. Species with heteromorphic life histories often required high and/or low temperatures to induce reproduction in one or both life history phases which further restricted distribution. (B) Species endemic to the tropical western Atlantic also had narrow survival ranges (between ca 10 and ca 35°C). Northern boundaries are set by low, lethal winter temperatures. Thermal properties would potentially allow occurrence in the (sub) tropical eastern Atlantic, but the ocean must have formed a barrier to dispersal. No experimental evidence is so far available for tropical species with an amphi-Atlantic distribution

The distribution of algae, corals and gorgonians in relation to depth, light attenuation, water movement and grazing pressure in the fringing coral reef of Curaçao, Netherlands Antilles

Abstract The south-west coast of Curacao (Netherlands Antilles) is lined by a rich fringing coral reef, the surface of which forms a submarine plateau mostly 30–100 m broad with a steep slope in front of it. Both plateau and slope are covered by rich living coral and algal communities. The zonation of coral, gorgonian, and algal species in two 5 m broad transects perpendicular to the coast line was investigated down to about 40 m depth (with a few observations down to 65 m), using a phytosociological method. Transect I (Figs. 1 and 2) was situated in a relatively sheltered bight, and transect II in front of a relatively exposed cape (Figs. 1 and 3). In transect II, water movement [as measured by Dotys (1971) diffusion factor] was appreciably higher than in transect I, at least down to a depth of about 20 m (Fig. 12). The following seven zonal communities were distinguished along both transects on the basis of cluster analysis and reef physiognomy: (1) the eulittoral Cyanophycean community; (2) the lower eulittoral community (characterized by algae such as Laurencia papillosa and Sargassum polyceratium ); (3) the shallow reef community (depth c. 1–4 m, characterized by the corals Acropora palmata and Diploria clivosa ); (4) the gorgonian community (depth c. 4–6 m, characterized by the gorgonians Pseudopterogorgia acerosa and P. americana ); (5) the drop off community (depth c. 6–12 m, characterized by the coral Madracis mirabilis , the dominance of Montastrea annularis and the extremely sparse algal growth); (6) the roof shingle community on the upper part of the steep slope (depth c. 12–27 m, characterized by roof shingle-like corals such as Agaricia agaricites and the roof shingle-like forms of species such as Porites astreoides ); (7) the deep algal community on the lower part of the steep slope (depth c. 27–c. 50 m, characterized by a conspicuous algal turf, possibly reflecting low grazing pressure at this depth, and by a more scattered growth of corals such as Agaricia lamarckii, A. grahamae and Madracis formosa ). In the shallow reef, the crustose corallines Porolithon pachydermum, Lithophyllum daedaleum and L. intermedium were abundant. In the roof shingle community and the deep algal community, Hydrolithon boergesenii and Archaeolithothamnion dimotum abounded. An increasingly sparse algal turf occurred between 50 and 65 m, where it seemed to reach its lower limit. Light intensity amounted here to about 1% of the surface radiation. The lower limit of hermatypic coral and crustose coralline growth lies at c. 80–90 m, where light intensity is estimated to be c. 0.2% of the surface radiation, but this is also the lower limit of solid substrate which dips here into a sediment plain. Despite differences in water movement and the form of the profiles, the zonation patterns in both transects resembled each other to a high degree. The two transects differed mainly by differences in the quantitative development of structurally important corals in the upper 20 m of water which are more turbulent in transect II than in transect I. Thus, in transect II, the corals of the drop off community and the roof shingle community have developed impressive buttresses which are lacking in transect I. Such buttresses often occur in more exposed areas along the southwest coast of Curacao.

TEMPERATURE, LIGHT, AND PHOTOPERIOD RESPONSES OF SOME NORTHEAST AMERICAN AND WEST EUROPEAN ENDEMIC RHODOPHYTES IN RELATION TO THEIR GEOGRAPHIC-DISTRIBUTION

The relationship between distributional boundaries and temperature responses of some Northeast American and West European endemic and amphiatlantic rhodophytes was experimentally determined under varying regimes of temperature, light, and daylength. Potentially critical temperatures, derived from open ocean surface summer and winter isotherms, were inferred from distributional data for each of these algae. On the basis of the distributional data the algae fall within the limits of three phytogeographic groups: (1) the Northeast American tropical-to-temperate group; (2) the warm-temperate Mediterranean Atlantic group; and (3) the amphiatlantic tropical-to-warm temperate group. Experimental evidence suggests that the species belonging to the northeast American tropical-to-temperate group(Grinnellia americana, Lomentaria baileyana, andAgardhiella subulata) have their northern boundaries determined by a minimum summer temperature high enough for sufficient growth and/or reproduction. The possible restriction of 2 species (G. americana andL. baileyana) to the tropical margins may be caused by summer lethal temperatures (between 30 and 35 °C) or because the gradual disintegration of the upright thalli at high temperatures (>30 °C) promotes an ephemeral existence of these algae towards their southern boundaries. Each of the species have a rapid growth and reproductive potential between 15–30 °C with a broad optimum between 20–30 °C. The lower limit of survival of each species was at least 0 °C (tested in short days only). Growth and reproduction data imply that the restrictive distribution of these algae to the Americas may be due to the fact that for adequate growth and/or reproduction water temperatures must exceed 20 °C. At temperatures ≦15 °C reproduction and growth are limited, and the amphiatlantic distribution through Iceland would not be permitted. On the basis of experimental evidence, the species belonging to the warm-temperate Mediterranean Atlantic group(Halurus equisetifolius), Callophyllis laciniata, andHypoglossum woodwardii), have their northern boundaries determined by winter lethal temperatures. Growth ofH. equisetifolius proceeded from 10–25 °C, that ofC. laciniata andH. woodwardii from 5–25 °C, in each case with a narrow range for optimal growth at ca. 15 °C. Tetrasporelings ofH. woodwardii showed limited survival at 0 °C for up to 4 d. For all members of the group tetrasporangia occurred from 10–20 °C. The southern boundary ofH. equisetifolius andC. laciniata is a summer lethal temperature whereas that ofH. woodwardii possibly is a winter growth and reproduction limit. Since each member of this group has a rather narrow growth and survival potential at temperatures <5 °C and >20 °C, their occurrence in northeast America is unlikely. The (irregular) distribution ofSolieria tenera (amphiatlantic tropical-to-warm temperate) cannot be entirely explained by the experimental data (possibly as a result of taxonomic uncertainties).

Survival Strategies and Temperature Responses of Seaweeds Belonging to Different Biogeographic Distribution Groups

The relationship between distributional boundaries and temperature responses of six western European endemic and amphiatlantic rhodophytes were experimentally determined under varying regimes of temperature, light and daylength. The algae fall within two phytogeographic groups: the warm-temperate Mediterranean Atlantic group (Calliblepharis ciliata, Polyneura hilliae, Lomentaria articulata and Cryptopleura ramosa) and the amphiatlantic-temperate group (Callithamnion tetragonum and Lomentaria orcadensis). In the former group, four species appear to have their northern and southern boundaries delimited by winter and summer lethal temperatures, respectively. Growth and reproduction proceeded from 10—20 °C and survival potential at temperatures 20 °C was limited, making their occurrence in northeast America unlikely. The gametophytes of P. hilliae have a narrower survival range at low temperatures than the tetrasporophytes thereby restricting its distribution. For the two representatives of the amphiatlantic-temperate group evidence points to the occurrence of ecotypic differentiation with regard to temperature tolerance for populations from the same and from either side of the Atlantic. As yet, the available evidence is insufficient to explain the nature of their geographic boundaries completely. Partly, this may be due to the taxonomic uncertainties that exist in these species.

GROWTH-INHIBITION OF LOBOPHORA-VARIEGATA (LAMOUROUX) WOMERSLEY BY SCLERACTINIAN CORALS

Growth rate, blade size, cover, and longevity of the foliose brown macroalga Lobophora variegata (Lamouroux) Womersley were recorded at various distances from the periphery of living coral colonies at ≈ 30 m depth on the coral reef of Curacao, Netherlands Antilles. Five coral species were studied: Agaricia agaricites (Linnaeus), Agaricia lamarcki Milne Edwards et Haime, Meandrina meandrites (Linnaeus), Mycetophyllia aliciae Wells, and Stephanocoenia michelinii Milne Edwards et Haime. Growth rates of Lobophora variegata blades close to corals (< 1 cm distance) were significantly lower than at a greater distance, which was accompanied by a higher proportion of blades having damaged margins. These effects were not due to differences in longevity of the blades, as half-lives were not significantly different at various distances from corals (≈15 days). Reduced growth rates resulted in smaller blade size and lower cover close to corals. All coral species reduced the growth rates of L. variegata blades by ≈ 35 % when in contact with the alga. In addition, Agaricia lamarcki and Meandrina meandrites reduced growth rates of Lobophora variegata at distances up to 1 cm. For Meandrina meandrites and Mycetophyllia aliciae, the reduction in growth rate was not accompanied by an increased proportion of damaged blades close to the colonies. These interspecific differences among corals suggest that there are various defence mechanisms against being overgrown by Lobophora variegata. Although L. variegata was observed to overgrow living coral tissues, it is concluded that high turnover rates of L. variegata blades (a result of intense herbivory), together with defence mechanisms of the corals themselves, generally prevent L. variegata from overgrowing coral colonies.

TEMPERATURE RESPONSES OF TROPICAL TO WARM TEMPERATE CLADOPHORA SPECIES IN RELATION TO THEIR DISTRIBUTION IN THE NORTH-ATLANTIC OCEAN

The relationship between distribution boundaries and temperature responses of some North AtlanticCladophora species (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 sites inside and outside distribution boundaries. The species tested belonged to two phytogeographic groups: (1) the tropical West Atlantic group (C. submarina: isolate from Curaçao) and (2) the amphiatlantic tropical to warm temperate group (C. prolifera: isolate from Corsica;C. coelothrix: isolates from Brittany and Curaçao; andC. laetevirens: isolates from deep and shallow water in Corsica and from Brittany). In accordance with distribution from tropical to warm temperate regions, each of the species grew well between 20–30°C and reproduction and growth were limited at and below 15°C. The upper survival limit in long days was <35°C in all species but high or maximum growth rates occurred at 30°C.C. prolifera, restricted to the tropical margins, had the most limited survival at 35°C. Experimental evidence suggests thatC. 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, when cold northerly weather penetrates far south every few years. Experimental evidence suggests thatC. prolifera, C. coelothrix andC. laetevirens are restricted to their northern European boundaries by summer temperatures too low for sufficient growth and/or reproduction. Their progressively more northerly located boundaries were accounted for by differences in growth rates over the critical 10–15°C interval.C. prolifera andC. coelothrix are excluded or restricted in distribution on North Sea coasts by lethal winter temperatures, again differences in cold tolerance accounting for differences in their distribution patterns. On 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. Isolates from two points along the European coast (Brittany, Corsica) ofC. laetevirens showed no marked differences in their temperature tolerance but the Caribbean and European isolates ofC. coelothrix differed markedly in their tolerance to low temperatures, the lethal limit of the Caribbean isolate lying more than 5°C higher (at ca 5°C).

TEMPERATURE RESPONSES OF SOME NORTH-ATLANTIC CLADOPHORA SPECIES (CHLOROPHYCEAE) IN RELATION TO THEIR GEOGRAPHIC-DISTRIBUTION

The temperature responses for growth and survival have been experimentally tested for 6 species of the green algal genusCladophora (Chlorophyceae; Cladophorales) (all isolated from Roscoff, Brittany, France, one also from Connecticut, USA), selected from 4 distribution groups, in order to determine which phase 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 adverse season. These species were: (1)C. coelothrix (Amphiatlantic tropical to warm 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 forC. vagabunda. (4)C. hutchinsiae (Mediterranean-Atlantic warm temperate), with a northern boundary formed by a summer growth limit near the 12°C August isotherm, and possibly 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 reached there. (5) Preliminary data forC. 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 American 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.

The Geographic Distribution of Seaweed Species in Relation to Temperature: Present and Past

Dumontia contorta exemplifies a number of temperate species occurring in the N Pacific Ocean and the N Atlantic Ocean and which were probably exchanged after the opening of the Bering Seaway (3.5 MA ago); their temperature responses indicate that their passage required a 6–8°C higher summer temperature than the present one in the Arctic Ocean. Some species in the above group, for instance Desmarestia viridis, have also an amphipolar distribution. Their passage across the tropics would have required a ca 5°C lowering of the equatorial sea surface temperature. This same temperature lowering can explain the extinction, along the east coasts of the Atlantic and Pacific Oceans, of tropical seaweeds such as Dictyosphaeria cavernosa with a W Atlantic-Indo W Pacific distribution. This lowering probably did not occur (sub)recently (for instance during Pleistocene glaciations), but earlier in the Cenozoic. We approached the question of the timing of the above temperature lowerings by estimating genetic divergence of disjunct populations of the same species or species complexes using the DNA-DNA hybridization method. Disjunct Atlantic and Pacific populations of several tropical and warm temperate species appeared to have genetically diverged in a high degree thus indicating a highly conservative morphology; this accords with their hypothetical divergence by the mid-Miocene (or earlier) closure of the Tethys Ocean. The divergence of amphipolar populations of the same species was probably more recent. Temperature changes of the sea surface predicted for the next century have a similar extent as those which have caused, in a more or less distant geologic past, profound alterations in the composition of the world’s seaweed floras.

Seaweed Biogeography of the North Atlantic: Where are we now?

Reconstructions of the glacial distribution areas of individual species belonging to the various seaweed regions, lead to the conclusion that species belonging to the Arctic-cold temperate N Atlantic flora could have been faced with such an extreme reduction of their distribution area (especially in the NW Atlantic) that they were threatened with extinction. Such severely adverse conditions did not exist in the N Pacific, and this may explain the much greater richness of the cold-temperate N Pacific flora. Laminaria hyperborea possibly exemplifies species that became extinct in the NW Atlantic during the glaciations, but survived in the NE Atlantic. Species in other seaweed regions than those in the Arctic-cold temperate N Atlantic were probably much less affected by the Pleistocene glaciations. Species endemic to the NW Atlantic coast, such as Grinnellia americana, are eurythermous and could potentially inhabit a broad area along NW African coasts and in the Mediterranean. Its absence there indicates that the central Atlantic Ocean can function as a barrier to long distance dispersal.

LIFE-HISTORY REGULATION AND PHENOLOGY OF THE RED ALGA BONNEMAISONIA-HAMIFERA

Bonnemaisonia hamifera Hariot (Rhodophyceae, Bonnemaisoniales) from Galway Bay, Ireland has been studied in the field and in laboratory culture. The reproductive behaviour of tetrasporophytes and gametophytes in the field appeared to be strictly regulated by their temperature/daylength responses as observed in culture. Tetrasporangia were abundant in early autumn when short days (<12 h of light per day) coincided with seawater temperatures over about 11°C, the lower limit for sporangium formation. Spermatangia were observed in very young gametophytes between mid-December and February, and in adult plants from late March until the end of May. They were absent in mid-winter when low temperatures of about 2°C inhibited their formation. Carpogonia were first observed at the end of April as seawater temperatures had by then risen to the required value of around 10°C. Carpogonia were fertilised and plants with mature cystocarps were present until early July. The onset of reproduction was accompanied by a cessation of growth and led to senescence within 2–3 months. Thus, gametophytes were absent in summer in spite of persistently favourable seawater temperatures. In various parts of the North Atlantic Ocean, annual temperature regimes are such as to cause a certain lack of synchronisation in the occurrence of reproductive male and female plants. This may account for the many anomalous reports of reproductive plants in the wild.