In high latitudes framework constructing carbonate production is enhanced by the growth of branching coralline algae which predominantly generate maerl-type ...
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PI. 21-23
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ERLANGEN 1993
Coralline Algal Maerl FrameworksIslands within the Phaeophytic Kelp Belt Andr~ Freiwald, Bremen KEYWORDS: CORALLINE ALGAE - MAERL - KELP FOREST - COMPETITION - DIATOM MICROFOULING - HERBIVORY - SELF-ORGAN/ZATION - SEA URCHIN OSTRACODA - POLYPLACOPHORA - GASTROPODA - RECENT
SUMMARY In the subtropical belt highly productive ecosystems are formed by coral reefs in oligotrophic seas. Towards more eutrophic conditions, coral reefs diminish and are subsequently replaced by highly productive kelp forests. In high latitudes framework constructing carbonate production is enhanced by the growth of branching coralline algae which predominantly generate maerl-type deposits. On a global view, these coralline algal ecosystems show an island-like distribution pattern within the phaeophytic kelp belt. Compared to kelp ecosystems, coralline-algaldominated ecosystems have low rates of productivity. Therefore, it is reasonable to seek the pronounced competitive value of the extremely slow-growing corallines. Due to their low annual growth increment, the coralline algae studied are very endangered by abiotic physical disturbances and by overgrowth of rapidly growing filamentous algae or sessile invertebrates. To overcome fouling pressure and storm - triggered physical disturbances, coralline algae thrive well in wave-sheltered headlands or skerry areas and generate characteristic 'denuded areas' by intense herbivory. This general distributional pattern is also true for high-boreal to subarctic coralline algal bioherms in northern Norway. Such a complex biological feedback maintains a high potential of self-regulation or self-organization in the algal reef bioherms. The different proponents involved in feedback processes include bacterial colonization, diatom microfouling and selective induction of larval metamorphosis. The negative impact of diatom microfouling and the important role of herbivores are relevant activities in the feedback system on a microscopic scale. Macroscopically, intense herbivory on coralline algae create denuded conditions, which are a widespread phenomenon in coralline algal ecosystems. I INTRODUCTION This contribution is an expanded version of a lecture given at the Hamburg colloquium 'Microbial Control of
OFG-Schwerpunkt BIOGENE SEDIMENTATION
Carbonates and Reefs' in November, 1992. Special emphasis is given to the impact of microbial activities on uncalcified parts of coralline algal frameworks and their assumed effects in shaping the distributional pattern of coralline algal communities, at least in non-tropical climates. Our own observations from modem algal reef bioherms existing on coastal platforms off Troms, northern Norway (Fig. 1; FRErWALD 1993, FREIWALD& HErCRICHsubm.), and recently published scientific results on microbial - coralline algal interactions shed light on complex biological positive feedback processes that may add to the knowledge of often mentioned extreme competitive success of slow-growing coralline algal communities (see reviews of STENECK1983, 1985, 1986). Ecosystems are maintained by a constant flow of energy to all their living members. Passing from member to member, energy is dissipated thus giving rise to definite hierachic, or thermodynamically ranked food chains, either the grazing food chain or the detritus food chain. This constant energy dissipation is characteristic for systems far from equilibrium (JArZrSCH 1992 and further references). The persistance of ecosystem s, their general 'stability', is related to efficient selforganization (see also BAK & Cm~N 1991, KAUFFMAY1991). Self-organization determines the process by which many systems evolve from a less ordered to a more ordered state (N~coLls & PRIOOOINE1977). Today, coral reefs represent the most productive type of ecosystem in the marine realm of low latitudes. Rapid nutrient recycling on comparatively small areas enables coral reefs to thrive well in oligotrophic environments (HALLOCK& SCm~ER 1986). A vast number of grazers living in the coral reef system are involved in short-term nutrient recycling. Additionally, grazers prevent development of perennial fleshy macrophytes in coral reefs (HALLOCX1988). Towards the more trophicated seas of higher latitude shelves, coral reefs are replaced by large
Address: Dr. A. Freiwald, Fachbereich Geowissenschaften, Universit~t Bremen, Klagenfurter St]. D-28359 Bremen; Fax:: Germany-0421-183116
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Fig. 1. Geographic map of northern Norway (A). The arrow indicates the position of the working area in the Troms district (B). The coralline algal reef is located near the southern tip of Rebbenes0y (1). Rhodolith pavements investigated are found within a skerry archipelago off Kvalcy (2) and in the Kvalsund (3).
phaeophytic belts on both hemispheres (Fig. 2; KRE~k 1981, Lt~n~o 1990). These phaeophyte ecosystems, dominated by kelp algae of the Laminariales group, are present along gently sloping, wave-exposed and hard substrate bearing coastal platforms. The Laminariales evolved in the northern Pacific (EsTES& S~n~ERC 1988), probably in Late Miocene (STAMet al. 1988, LONIN~& a'OMDmCK 1990). In contrast to coral reefs, kelp forests turn over about 90% of their algal biomass in the detritus food chain and only 10% is converted by the grazing food chain (BARNES & MANN 1980, KOOVet al. 1982). Focussing on the boreal northwest European shelf, another type of macrophytic ecosystem is developed. This macrophyte system forms islands of intense framework carbonate production within the phaeophytic belt, namely coralline algal ecosystems (Figs. 2-3). Coralline algae are slow-growing, but long-living plants with low productivity and low caloric value (Lirn.~R & LIttLER 1980, 1984). This life history is typical for K-strategists (sensu PtAYr~ 1970), meaning that long-lived slow growers tend to
build up their biomass to the maximum that the environment will support. Coralline algal dominated ecosystems which generate maerl-type deposits in boreal to subarctic regions are brought into focus by LEMOe,~ (1910), H~star~ (1942), C~IocH (1969),LzEs etal. (1969), BOSENCE (1980), SCOFFIN (1988) and F~Iwat~ et al. (1991), who depict corallines as valuable tools for interpreting past environmental conditions. The key to understanding the coexistence of low-productive coralline algal ecosystems and their close neighbourship to highproductive kelp forests is a good knowledge of biological feedback mechanisms that interfere with the frequency and intensity of storm-triggered physical disturbances. The success of coralline algae is viewed as the result of microbial positive feedback which ends up in the shaping and distributional patterns of corallines, thus providing a peculiar example for self-regulation in complex biological systems. 2 T H E A L G A L R E E F IN N O R T H E R N N O R W A Y A 'SEA DESERT'?
Along the northwestern European platform, coralline algal frameworks thrive well in wave- and swell-protected rocky habitats (STEr~CK1986). If attached to hard substrates, the algal framework constructions can form reefs even beyond the Arctic Circle, on coastal platforms off Troms, northern Norway (Fig. 1; F~iwat~ 1993, F~iwatD & I-tEbrmCH subm.). The algal bioherms and rhodolith pavements are almost free of macroscopic sessile epiphytes (PI. 21/1-3). The term 'Isoyake condition' (NoRo et al. 1983) or 'sea desert' are coined to describe this globally distributed phenomenon in coral line algal systems. The reef framework is constructed by composite growth of encrusting Phymatolithon sp. and branching Lithothamnion cf. glaciale (Fig.
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Fig. 2. The global distribution of the cold-water phaeophyte kelp belt (black stripes) and the warm-water coral reef belt (R signature). The 20~ isotherm roughly marks the boundaries between the two different types of highly productive benthic ecosystems. Data adopted from KREMER(1981) and L(mlNO(1990). The arrow point to maerl-type carbonate deposits on the northwestern European shelf (1 = Brittany, 2 = western Ireland, 3 = western Scotland and Orkney Islands, 4 = Swedish Bohusliincoast, 5 = Troms district, northernNorway).
4, P1.21/1). No secondary fusion of branch tips occurs after branching. However, due to distally enlarged apices (P1.21/ 4), this species forms dense carpets of high architectural strength. On dead corallines and in reef cavities, however, a dense colonization of a diverse fouling community is developed. Grazers efficiently removed rapidly growing invertebrates at their postlarval stage and plant spores and thus keep the living surface of coralline algae clean.
2.1 The macroscopic approach Underwater TV-surveys from the densely branched reef framework in northern Norway show large accumulations of juvenile Strongylocentrotus droebachiensis. Adult specimens of this sea-urchin have been predominantly observed outside of the coralline algal systems. Grab-sampled reef slabs host limpets and chitons, as well as numerous 'small' gastropods and ostracods (PI. 21/5-10). Fixed bryozoan colonies, dominated by flexible bushes of Dendrobeania murrayana (see FREIWALDet al. 1991: P1. 83/1), hydrozoans and annual filamentous algal turf, are developed on mobile rhodolith pavements but rarely on the algal reef framework. Their holdfasts are nearly always fixed in hollows between adjacent coralline algal branches. Some rhodoliths as well as some large bivalves are colonized by single kelp. However, when the hydrodynamic drag of kelp is large enough to overcome the friction of colonized objects (KL~RASS 1974), rafting after stonns or strong tides occurs, keeping the kelp out of this coralline algal ecosystem.
2.1.1
Sea urchins
The most conspicious mobile faunal element on the algal reef are large numbers of juvenile sea urchins, Strongylocentrotus droebachiensis. The sea urchins are found in high densities of 30 to 60 specimens per square meter on the algal reef and on adjacent rhodolith pavements. The strong biting apparatus (Aristotele's lantern) generates characteristic pentaradiate grazing marks of 30 ~tm to 50 lain depth on the distally enlarged branch tips ofLithothamnion cf. glaciale (Fig. 4). These observations correspond well with Saxr~cx' s (1990) studies on the density patterns of Strongylocentrotus droebachiensis on several species of coralline algae. Highest densities were recorded on branching Lithothamnion cf. glaciale with up to 55 specimens per square meter. 2.1.2 Limpets and chitons The encrusting Phymatolithon sp. is the preferred grazing habitat of the limpet Tectura testudinalis and for the chiton Lepidopleurus asellus. Both herbivore molluscs create characteristic grazing tracks on the algae. Tectura bitings resemble rake tracks made by the docoglossan radula (PI. 22/ 5). The short and stout teeth are hardened by iron and silica minerals (STE~CX & WATLIYO1982), thus providing a great excavating capability on tough substrata. Lepidopleurus asellus is much less abundant on the algal reef, compared to Tectura testudinalis. Lepidopleurus asellus generates surficially sharp and straight grooves that are arranged in two parallel traces (FARROW& CLogaE 1979). The grazing intensity, which means the amount of biomass that is re-
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Fig. 3. Maps showing characteristic distribution of framework coralline algae (C) and kelp forests (K) in northern Norway (FR~w~a.o 1993) and in western Scottish island archipelagos (modified from Sco~eq 1988). Both examples have in common, that the kelp forests and related carbonate deposits are located on the wave-exposed coastal platforms. Coralline algal rhodolith pavements are concentrated within the island archipelagos. moved with a single bite (S~rcECX 1990), varies between 10 lxm and 20 gm in both limpets and chitons respectively.
2.2 The microscopic approach The microscopic approach demonstrates heterotypic interactions that take place on the living coralline algal surface. Special emphasis is given to the anatomy of the thick cuticle and its reaction against fouling by diatom films. The diatoms themselves, are a major food resource for a number of 'small' gastropods and ostracods living on and between the branches of the algal framework. In contrast to sea urchins, limpets, and chitons, the impact of these microherbivores to the algal framework is not witnessed by grazing marks. However, the grazing activities of the microherbvores are considered to play a prominent part in a feedback affecting the entire reef development. Finally, the distinct distribution pattern of rod-shaped bacteria which are attached to the living algal surface cells is described. 2.2.1 The coralline algal - water interface: epithallial cells and cuticle The epithallus of corallines serve as an interface for the algae with their ambient environment. The epithallial and cuticle structure of corallines has long been considered
merely protective in function, but SEM and TEM studies havealso revealed secretory attributes (BAILEY& BIsA~tna~ 1970, BOROVaTZXA& VESK 1978, GmAt.rD& CABIOCrt1976, 1979, CABIOC, & G l ~ t m 1986).
2.2.1.1 The epithallial cells Epithallial cells form unistratose or multistratose layers that terminate each algal filament distally (Fig. 5). The surface cells originate from cell division of vegetative initials or meristematic cells. In most corallines, such asLithothamnion, the outward walls of epithallial cells are uncalcified. Initial stages of calcification start at the base of the cells. Therefore, dried specimens reveal collapsed vacuolate epithallial cells, so that the algal surface is structured by a characteristic polygonal cup-like depression pattern (P1. 22/1-3, 6-8). Epithallial cells and underlying vegetative initials bear plastids for photosynthesis. The epithallial cells are sloughed off in many coralline algae (JomqsoN & MANN 1986). However, in Lithothamnion cf. glaciale of the reef framework studied, epithallial shedding of surface cells seems to be an uncommon feature. The process of sloughing off epithallial cells, thus creating an unstable substrate for epiphytic communities to attach to (MILtSON & MOSS 1985, CaBIOCH& GmAtrO 1986, JOHNSON & M a ~ 1986) is more conspicuous to coralline algae
Fig. 4. A sketch from a grab-sampled coraUinealgal framework from the algal reef (see Fig. 1 for location). The framework is constructed by a binding algae (Phymatolithon sp.) and by baffling algae (Lithothamnion cf. glaciale and Lithothamnion sp.).
137 votes. Both groups are involved in permanent, non-excavating grazing and thus forming a 'grazing shield'. 2.2.3 Foraminifera
Fig. 5. A schematic cross-section of surface cell and cuticle arrangement in Lithothamnion cf. glaciale (not to scale). The active growth zone is located in the vegetative initial cells (Vi). The vegetative initials are coyered by flat epithallial cells (E). The basal parts of epithallial cells are calcified only. Firstly, tangential calcitic crystallites (t) were precipitated along the polysaccharide rich middle lamella. The radially fibrous calcites (r) were formed later. Translocation of metabolites is made possible by pit-connections (p), The surface cells are partly covered by the thick cuticle (C). The cuticle is formed by a series of laminae. The cuticle is often fouled by a dense diatom film (d). Incorporation of diatoms between the laminae of the cuticle is possible.
obtaining a multistratose epithallus. However, it remains unclear whether epithallial shedding is an actively triggered antifouling process by the algae itself, or if epithallial shedding is enhanced by organic material decomposing bacteria during cell aging (LEWIS et al. 1985, Ivl~t.tsoN & Moss 1985, Jor~soN & Ma~,cN 1986). 2.2.1.2 The cuticle The granular, m ultilaminated cuticle merges proximately with distal walls of epithallial cells (G1Rat~ & CA~JOCH 1976, GARBARY& VELaXAra_O1980, Fig. 5). This sandwichlike construction of the cuticle is evidenced by shrinking cracks in dried Lithothamnion (PI. 22/7-8). The cuticle is composed of up to 6 laminae, each with a thickness of approximately 0.25 Bm. Shrinked pieces of single laminae strip off from the surface (PI. 22/7-8). The cuticle is distributed heterogenously on the Lithothamnion surface. It is concentrated around branch tips and crust margins, but it occurs on lateral branch sections as well. Towards the margins of cuticle coverages, the number of laminae decreases. 2.2.2 'Small' gastropods and ostracods The functional form group of 'small' gastropods is comprised of a number of non-excavating grazers not larger than 2mm (Tab. 1 and P1. 21/5-10). They occur in large numbers on the living relief-rich surface of the algal reef and are thought to feed predominantly on diatoms and other microalgae. Sediment samples taken from reef-cavities contain a number of ostracods that are known to feed on diatoms and fragmented algal detritus (Tab. 1). Since these herbivores are commonly found among algae between Lithothamnion branches, they are assumed to be non-excavating herbi-
The largest members of sessile invertebrates attached to the living corallines are foraminifers, Cibicides lobatulus (PI. 23/1), and his assumed planorbulid schizont (sensu NYHOLM1961; P1.23/2). The feeding adaptations of Cibicides lobatulus include grazing diatoms and bacteria with pseudopodial protrusions and, probably, suspension feeding (see also ALEXANDER& DELACA1987 for Cibicidesrefulgens). Rarely, Polymorphina ovata (P1.23/3), fixed by its spiny calcareous protrusions between branches of Lithothamnion thalli, as well as beneath Phymatolithon crusts have been observed (compare GIESE 1991). 2.2.4 Diatoms Benthic diatoms include taxa that attach to other objects such as rocks and plants, thus forming epilithon or epiphyton communities (RouND 1971 and MCI~mRE & MOORE1977 for review). The diatom associations consist of one dominante species and three to five other less abundant species, most belonging to Cocconeis (1'1.23/4-5). The distribution of the epiphyton community is extremely heterogenous and varies on a very small scale. Generally, diatoms form singlelayered or double-layered films on the surface cells of corallines (PI. 23/4). Floating diatom chains, fixed on living corallines have been detected as well (P1.23/6). Occasionally, SEM-scanned surfaces of Lithothamnion thalli show diatom frustules that are covered by layers of the enveloping cuticle (P1.23/7-8). At the moment, it is very speculative to evaluate this intra-cuticular occurrence of diatoms. Most probably, the diatoms were simply overgrown by the cuticle after the diatoms inhabited the epithallial ceils. This hypothesis is supported by W~KER & Moss (1984), who have Ostracoda Argilloecia conoidea Cythere lutea Cytheropteron pyramidale Finmarchinella angulata Hemicythere emarginata Hemicytherura clathrata Hirschmannia viridis Palmoconcha laevata Paradoxostoma ensiforme Phlyctocythere fragilis Polycope cf. sublaevis Robertsonites tuberculatus Sclerochilus rudjakovi Semicytherura acuticostata Semicytherura affinis Semicytherura complanata Sernicytherura nigrescens Semicytherura striata Semicytherura undata Xestoleberis depressa
Gastropoda Alvania punctura Ammonicera rota Diaphana rninuta Moelleria costulata Omalogyra atomus R issoa parva Scissurella crispata Foraminifera Cibicides lobatulus
Table 1. List o fnon-denudmg herbivores inhabiting living coralline algal surfaces.
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Fig. 6. The high potential for selforganization in coralline algae that is triggered by herbivore - plant interaction. The spread of coralline algae (A) is made possible by selective inductionofherbivore larvae to metamorphose 03, C, D). This induction is either controlled by host specific bacteria (Jor~rsoNet al. 1991a, b) or, by algal-mediated neuroactive substances (GABA; MoRsE 1991) 03). The grazing activity keeps the riving algal surface clean of fouling organisms (E) thus enhancing spread of coralline algae (A).
investigated modes of attachment of different crustose corallinaceans.
2.2.4.1 The effect of diatom microfouling - a mutual interaction ? The heterotypic relationship between diatoms and coralline algae is not of mutual benefit. Due to reduced lightlevels, growth rates of colonized plants decreased significantly as biomass accumulates (CARPErrrER 1990). Beside shading, there are also pronounced retarded diffusion gradients through a diatom film, which hampers nutrient exchange (Rose & Cusrm~6 1970). Furthermore, oxygen depletion in the dark and in high oxygen and low carbon dioxide concentrations in the light occurs (SAYD-JENszNet al. 1985). It is obvious that non-removal of epiphytic diatom f'dms can have severe negative effects to the colonized plant. Moreover, diatoms generally are very short lived with high rates of cell-division. Therefore, diatom microfouling pressure lasts permanently on coralline algae. Spatfall of invertebrate larvae or spore settling, however, is more or less
concentrated in pulses in early spring when environmental conditions stimulate spawning. This negative impact of diatom microfouling has been proved in experiments by Sa~r,rzcr:(1982) for the unbranched coralline Clathromorphum circumscriptum. Complete removal of limpet grazers for a month enhances heavy fouling by diatoms, cyanobacteria, and filamentous algae. Clathromorphum circumscriptum gains an unhealthy appearance and portion of the thallus dies. 2.2.5 Bacteria Bacteria on the epithallial cells of coralline algae studied are sparse and have been detected in formaline-fixed Lithothamnion cf. glaciale. The bacteria are rod-shaped and 2.5 I.tm to 3 grn in size (P1.22/1-4). If present, they are concentrated around the polysaccharide rich middle lamella of cell boundaries (see also JoHNsoNet al. 1991 a; PI. 22/1-2). In other areas of the same Lithothamnion branch, bacteria are clustered on partly damaged diatom frustules (PI. 22/34), suggesting that bacterial activity is linked with decompo-
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Fig. 7. Conclusive sketch outlining the microscopic interactions and their macroscopic response. The macroscopic approach: CoraUine algal systems form islands within the phaeophytic kelp belt of trophicated seas (A). Focussed on coralline algae, the living surface is almost free of secondary epiphytes ('sea desert' condition) (B). The microscopic approach: The highly competitive success of coraUine algae against fouling organisms is made possible by feedback between corallines and herbivores (C). Excavating grazer, such as sea urchins, limpets and chitons, are positively influenced by living corallines concerning larval settlement and subsequent metamorphosis (C1). Non-excavating herbivory, caused predominantly by 'small' gastropods and ostracods, is directed to remove the diatom films from the corallines (C2). The participiants which are involved in this predator - prey system show no specificity with respect to coralline algae. The slow growth rates of coralline algae in northern Norway make them susceptible to sea level oscillations (D). Therefore, the geological signal in form of distinct layers of autochthonous coralline algal deposits strongly correspond with intervals of constant sea level (FRErWALOet al. 1991).
Phymatolithon sp. crusts provide smooth grazing area with
sition processes (LEwis et al. 1985, Jor~soN & MANN 1986). All in all, bacterial distribution on coralline algal surface cells is extremely heterogenous. 3 Q U A L I T Y OF G R A Z I N G E F F E C T In the bioherms investigated, the overwhelming herbivores is represented by non-excavating organisms, such as benthic foraminifers, ostracods, and 'small' gastropods (Tab. 1). Limpets and chitons are abundant locally where
a low relief. Functional aspects of mollusc radulae as a grazing tool adapted to coralline algae were studied by STENECX(1982) and STENECK& WATL~G (1982). Examinations of the gut content of limpets grazing on Clathromorphum circumscriptum reveal abraded coralline cells as prefered food resource rather than diatoms. Grazing marks caused by limpets (PI. 22/5) or chitons occur only occasionally in the coralline algal bioherm. However, limpet grazing marks are quiteabundanton Clathromorphumsp. intheshallow subtidal zone studied. This observation is in keeping with STErCECK'S (1982) experiments and field studies at Maine. More abundant than limpets and chitons are sea urchins with the key species Strongylocentrotus droebachiensis in the algal framework studied. Echinoid grazing, however, does not effect algae dramatically. Due to the branched growth form of Lithothamnion with distally broadened
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thalli, the destructive impact of echhloid deep-grazing is neglegible (STErCECK1990). Although a number of excavating grazers are present on the algal bioherms, the greatest antifouling effect that results in 'sea desert' appearence is considered to be caused by the micro-herbivores, such as ostracods and 'small gastropods'. Unfortunately, these herbivores leave no grazing mark on the coralline thalli. 4 TOWARDS A MODEL FOR SELF-ORGANIZATION IN CORALLINE ALGAL ECOSYSTEMS
In the proposed model, heterotypic interactions are viewed as interlinked feedback mechanisms which include aspects of bacterial decomposition (LEWISet al. 1985), bacterial or algal-mediated induction of metamorphosis of certain excavating herbivores (Jonson et al. 1991 a, b vs. MORSE1991), microfouling (this study), and grazing impact on coralline algae and its epiphytes (S'rE~CK 1986, this study). 4.1 The feedback mechanism between excavating grazer and coralline algae
The autocyclic feedback suggested here, draws attention to mutual herbivore - coralline algal interactions that are considered to be result of specific evolutionary fine-tuning (Fig. 6; for reviews see HUGHES& GLIDDON1991, S'rENEC)r 1985, 1992). In general, coralline algae develop an initial cruststage immediately after successful settling of spores (CAr3tocn 1988). On living algal crusts, cell aging of distally altered epithallial cells is mediated or enhanced by non-motile hostspecific bacteria. This has been evidenced so far for Clathromorphum, Sporolithon, Mesophyllum, and Lithophyltum (LEwls et al. 1985, Jom~soN et al. 199Ia). As reported from Jot~soN et al. (1991b) these bacteria are distinguished from
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Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Figs. 5.-10.
other forms by their inability to utilize glucose, to hydrolyse complex carbohydrates, to utilize simple amino acids, and to reduce nitrate. These epiphytic bacteria are considered to induce settlement and metamorphosis of larvae, especially larvae of herbivore invertebrates (Jor~soN et al. 1991a, b). The general positive effect of coralline algae that stimulate metamorphosis of herbivores has long been observed in abalones (MoRsE& MORSE1984), limpets (SxENECX1982), chitons (BAR~r & GOUOR 1973), Sea stars (BARKER 1977, Jort~SOY et al. 199 la), and sea urchins (PEARCE& SCHEn3UNC 1990), namely of Strongylocentrotus droebachiensis. Although, another hypothesis for this enhanced settlement on coralline algae suggest neuroactive inducers (y-aminobutric acid = GABA) to induce metamorphosis (MoRsE & MORSE 1984, MORSE1991, PEARCE& Scrmmt.IN~ 1990), the result is the same: a concentration of herbivores on living coralline algae (Figs. 6, 7). It is assumed, that this bacterial or algalmediated biological feedback starts in an early developmental stage of the coralline crust to overcome constant microfouling pressure from the beginning. The metamorphosed herbivores them self benefit from this interaction by taking up pink pigments for camouflaging purpose. Nearly all chitons, limpets, and juvenile sea urchins are pinkcolored in the bioherms studied. Additionally, they find shelter against predatory fishes and sea stars. The SEMobservations show that grazing damage on corallines is low. The distinct ability of coralline algae to translocate photosynthates through pit-connections and cell fusions is outlined by STENECK(1986) as one of the most important evolutionary trends that allows them to survive under high grazing pressure by rapid wound-healing and regeneration. Deep-excavate grazing in the northern Norwegian algal bioherms is predominantly caused by the sea urchin Strongylocentrotus droebachiensis. Nevertheless, the overall grazing destruction is slight due to branching growth
Coralline algal maerl frameworks - Islands within the phaeophytic kelp belt. The macroscopic approach: the coralline algal bioherm as a 'sea desert' and non-excavating herbivore gastropods A view of the central part of a coralline algal bioherm in 7m water depth, Troms district, northern Norway. The reef framework is composed of branched Lithothamnion (I) and encrusting Phymatolithon (2). The white branch tips and crust margins indicate active growth zones of the coral lines. Note the lack of filamentous algae and the presence of sessile epibionts thus giving a 'sea desert' appearence. The section represents approximately 0.4m 2. A view on the reef-fringing rhodolith pavements deriving from detached branched aggregates of Lithothamnion in 7m water depth. The genesis of this type of rhodolith accumulation is storm-triggered. No filamentous and kelp algae are visible, but numerous juvenile Strongylocentrotus droebachiensis sea urchins graze on the rhodoliths. The section represents approximately 0.9 m2. A view on a reef-slab sampled from the central part of the algal bioherm. The living surface is free of secondary macrofouling organisms, whereas the porous subsurface framework provides a variety of niches for sessile invertebrates. The length of this slab is 25 cm. Distally enlarged tips of Lithothamnion branches forming a dense carpet of high architectural strength. Large herbivore organisms are not able to graze along the branches. These branched carpets form the source for branching rhodoliths when becoming detached during severe storms. Scale bar = 0.5 cm. SEM-micrographs of non-excavating herbivore gastropods occurring in the algal bioherm Fig. 5. Ammonicera rota (FORBES& HArCLEu 1850); Fig. 6. Moelleria costulata (MoELLER,1842) Fig. 7. Scissurella crispata FLEM~, 1828; Fig. 8. Lepeta caeca (Mt~LER, 1776) Fig. 9. Omalogyra atomus (PmuPr,I, 1841); Fig. 10. Rissoa guerini R~cLtrZ, 1843
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Fig. 8. A schematic view on the frequency and intensity of storm-triggered physical disturbances in kelp forest and in coralline algal habitats (A). The higher degree of physical disturbances in kelp forests causes rapid fluctuation in community composition of secondary epiphytes (B). A mosaic-like pattern with spatially and temporally changes of dominant species (indicated by different numericals) give rise to a 'neighbourhood-stability' (sensu GRAY1977). The successional stages observed in kelp forest systems often alternate from a pioneer to a diversification stage. Due to the self-organized feedback between grazer and plants in coralline algal systems, a low-diversity climax community structure rapidly emerges after physical disturbances. According to GRAY (1977), this condition represents a system of 'global stability' (C). forms of Lithothamnion cf. glaciale (see also S~NECr: 1990). In the subtidal zone in northern Norway, this distinct growth form is strongly correlated to high population densities of Strongylocentrotus droebachiensis (FRErWALD 1993). 4.2 T h e g r a z i n g feedback - diatom m i c r o f o u l i n g and n o n - e x c a v a t i n g grazers
The possible influence of non-excavating grazers with respect to the large competitive success of coraUine algal bioherms is object here. The coralline algae in the biohenns investigated are densely fouled by diatom films which are thought to be harmful. Removal of these
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Figs. 3.-4.
Fig. 5
Fig. 6. Fig. 7. Fig. 8.
Coralline algzd maerl frameworks - Islands within the phaeophytic kelp belt. The microscopic approach I: Bacteria and the epithallus - cuticle complex A view of intact surface cells of a Lithothamnion from the algal bioherm. Rod-shaped bacteria are visible in the center of this SEM-micrograph. The bacteria concentratearound the polysaccharid rich middle lamella of the surface cells. This pattern is known from other bacteria resting on corallines (JOHNSONet al. 1991 a). Scale bars = 10 ~tm (1), 3 tam (2). A patch of diatom frustules that are partly overgrown by cuticle laminae of Lithothamnion (3). The intracuticular diatom frustules often are settled by rod-shaped bacteria indicating decomposition (4). Scale bars = 30 ~tm (3), 3 txrn (4). Grazing marks of the limpet Tectura testudinalis on epithallial cells of Lithothamnion. The removal of the cuticle with overgrown diatom frustules was incomplete, some frustules are left (see centre of SEMmicrograph). Scale bar = 100 pm. Grazed epithallial cells (upper right) and ungrazed cuticle with partly overgrown Cocconeis sp. frustules (SEM-micrograph). Scale bar = 10 ~un. Thick cuticle of Lithothamnion from the algal bioherm. The cuticle is torn due to shrinking thus giving view on intact epithallial ceils below the cuticle (SEM-micrograph. Scale bar = 30 I.tm. A detailed view on the thick cuticle of Lithothamnion. The cuticle is composed of multilaminae which are able to overgrow diatom frustules. Under the cuticle intact surface cells are visible (SEM-micrograph). Scale bar = 10 I.tm.
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diatom films is not maintained by excavating grazers predominantly. Non-excavating grazers feed on diatoms preferentially, however, without damaging the coralline algal surface. The most abundant non-excavating grazers in the bioherms studied are'small' gastropods and ostracods. Therefore, the non-excavating herbivore - diatom interaction is part of a distinct grazing food chain, whose outcome is the clearance of coralline algal surfaces as a byproduct (Fig. 7). The overall observations suggest strong coralline algal herbivore feedback mechanisms allowing the slow-growing and low-productive corallines to develop distinct ecosystems in close neighbourship to highly productive kelp forest ecosystems. The impact of excavating grazers such as sea urchins, limpets and chitons is directed to remove epithallial cells predominantly rather than diatoms which are the preferred food resource of the mass of non-excavating herbivores. For this reason, grazing marks produced by excavating herbivores are comparatively rare in the subtidal bioherms investigated, but become more abundant in the shallow subtidal zone on Clathromorphum crusts. The herbivore grazing shield enables coralline algae to spread out and occupy large areas in the subtidal zone of wave and swellsheltered habitats. 4.3
The role of physical disturbances
The described herbivore - coralline algal interactions can be regarded as a very effective antifouling strategy. The spatial distribution of slow-growing corallines in northern Norway is limited by physical disturbances (FREIWALD& HZNmCH subm.). Distributional patterns of coralline algal bioherms in the area studied suggest that storm-triggered disturbances play a major role in spatial limitation of coralline
Plate
Fig, 1. Fig. 2.
Fig. 3. Fig. 4.
Fig. 5. Fig. 6. Fig. 7.
Fig. 8.
23
maerl deposits (Figs. 2 and 8a). Within wave-protected skerry archipelagos, storm redeposition events occur much lesser compared to the wave-exposed localities of kelp forests. Within these wave-protected habitats in northern Norway, a low diversity climax community structure is characteristic for algal maerl framework systems (Fig. 8c). The higher frequency and intensity of storm events in kelp forest habitats cause large fluctuations among the kelp epiphyte community (Fig. 8b). The community structure of the secondary epiphytes often fluctuates from pioneer to diversification stages with temporally and spatially different species dominances (GRAY 1977). Therefore, in kelp forests encrusting coralline algae often are restricted to the rhizoid and basal parts of Laminaria stipes, where more stable microenvironmental conditions prevail. 5
INTERACTIONS BETWEEN CORALLINE ALGAL BIOHERMS AND KELP FORESTS
Recently, harmful outbursts of sea urchins have dramatically affected coastal hydrodynamics by destructive overgrazing of kelp forests. Strongylocentrotus droebachiensis outbreaks cause partial or complete destruction in kelp forests along the 500 km long coast of Nova Scotia (CrtaPMaN 1981, MaNN 1982). Due to kelp overgrazing, sea urchin barren grounds with encrusting coralline algae that have existed as understory prevail on hard substrates. This biological disturbance causes a rapid change from a highly productive into a low-productive ecosystem. Sea urchin mass-occurrences are also observed along the northern Norwegian coast (HaczN 1983). I-~CEN (1987) pointS Out that the sea urchin masses are largely diminished after infestation by endoparasitic nematodes. But where do the outbursts of
Coralline algal maerl frameworks - Islands within the phaeophytic kelp belt. The microscopic approach II: foraminifers and diatom microfouling SEM-micrograph of a Cibicides lobatulus attached to Lithothamnion branches. This foraminifer has suspension-feeding and grazing-feeding capabilities. Scale bar = 300 I.tm. SEM-micrograph of a planorbulinid schizont of Cibicides lobatulus, according to NYrIOLM (1961). This schizont stage is found solely in the bioherm and in adjacent reef detritus, whereas the Cibicides lobatulus stage is a characteristic member of hydrodynamically high energy environments along the whole shelf system. Scale bar = 300 t-tin. Planorbulina ovata, attached between branches of Lithothamnion. Scale bar = 300 ~tm. A view on a dense diatom film on a Lithothamnion crust sampled from the algal bioherm (SEM-micrograph). The microfouling community is of low diversity. Diatom films negatively influence metabolic activities of the colonized plant by shading and generating diffusive gradients through the diatom film with respect to nutrient translocation. The oxygen and carbon dioxide budget is also reduced for the fouled coralline algae. Scale bar = 100 I.tm. A detail from the diatom community shown in Figure 4 (SEM-micrograph). A = Cocconeis scutellum, B = Cocconeis sp. Floating diatom colonies in a chain-like arrangement are often found fixed on living coralline algae (SEMmicrograph). Scale bar = 30 I.tm. Three diatoms overgrown by cuticle laminae of Lithothamnion. The cuticle covers the epithallial ceils. It is suggested that the diatoms attached on a previously sloughed epithallus and were subsequently caught by protuding cuticle devopment (SEM-micrograph). Scale bar = 30 ~tm. A detail of the diatom frustules that are overgrown by cuticle. Due to shrinking effects the cuticle is torn so that the frustules are partly visible (SEM-micrograph). Scale bar = 10 btm.
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Strongylocentrotus droebachiensis come from? HAGEN (1983) suggests increased rates of seaward transport of sea urchin larvae due to local hydrographic effects, or, decreased predation on metamorphosed sea urchins (MANN 1977). TV observations of shallow coastal platforms may offer an extended hypothesis. The Strongylocentrotus droebachiensis individuals grazing in the coralline algal bioherms are almost juveniles obtaining test-diameters of 0.5 cm to 1.5 cm. Adult specimens with test-diameters of 3 cm to 5 cm are found occasionally within the algal bioherms but more often in adjacent areas. A real mass-occurrence of living adult Stron gylocentr otus droebachiensis was detected on well-sorted carbonate sands without any macrophytes living there. This observation is consistant with those of LAUR et al. (1986). They have demonstrated that sand substrates do not act as distributional barriers for sea urchins. However, on sandy substrates sea urchins are extremely endangered by rough sea conditions. It is likely that juvenile Strongylocentrotus droebachiensis found in the algal bioherms have to leave this low calorific ecosystem (LITILERt~ LITrLER1980) when becoming larger. The energy demand of adult Strongylocentrotus droebachiensis may not be secured by diatom films and coralline algal cells. The ability of Strongylocentrotus droebachiensis to move on soft substrates permits an invasion of kelp refuges during calm periods. This may explain, why populations of Strongylocentrotus droebachiensis outbursts are dominated by adult specimens (see HACEN 1983). If this assumption Can be substantiated in the future, this interaction between different benthic ecosystems strongly resembles outbreaks of adult Acanthaster planci seastars in the Great Barrier Reef complex (JOHNSON199 la). Acanthaster planci populations derive from rhodolith banks in the deep fore reef section. After metamorphosis, the sea stars live sheltered between Lithothamnion pseudosorum rubble. As adults, large populations move up to the shallow coral reef sites causing severe destruction (JOHNSON 199 la, PANDOLF1 1992, VAN DER LAAN & HOGEWEG1992). 6 LOOKING INTO T H E PAST The reduced rates of annual skeletal growth, the discussed biological feedback mechanisms, and the controlling influence of physical disturbances are intrinsic factors for development of framework constructing coralline algal ecosystems on cold, eutrophic shelves. The great demand of predictable environmental conditions observed in coralline algal communities outlines their significance as important tools to interpret past environments. The occurrence of autochthonous Holocene coralline algal strata in the Troms district clearly mirrored the course of high frequent sea level fluctuations (FRE1WALDet al. 1991, FREIWALD1993). Rhodolith banks always coincide with intervals of stable sea level conditions (Fig. 7). Otherwise the slow-growing corallines could not keep up with rapidly changing sea levels. Intervals of stable sea levels in the area investigated occurred around 6500 BP, 6000 - 5500 BP, 4800 - 3800 BP, and 3400 - 2600 BP (MOLLER1989, FREIWALD1993). Paleogeographic reconstructions based on levellings of sediment profiles and
radiocarbon dating of selected objects give evidence of identical ecological preferences of Holocene coralline algae compared to their modern analogues (FREIWALD1993).
7 CONCLUSIONS Locally extended coralline algal frameworks in subtidal zones of eutrophic seas show an island-like distributional pattern within the phaeophytic kelp belt. Many of these coralline algal environments produce vast amounts of maerltype carbonate deposits. Internal recycling in coralline algal and kelp ecosystems reveal contrasting tendencies. In kelp forests most of the biomass is converted by the detritus food chain, whereas in coralline algal ecosystems the grazing food chain predominates. The highly competitive success of slow-growing and low-producing coralline algae against highly productive kelp forests and filamentous algae is documented in the well-known 'sea desert' appearence of coralline algal bioherms. This phenomenon observed in coralline ecosystems is made possible by microbial feedback mechanisms. Herbivore grazing activities produce a large potential for self-regulation or self-organization. Most of the herbivore organisms belong to the non-excavating feeding group. The members of this group graze permanently on the diatom films without destructive effect to the epithaUial cells of the coralline algae. Diatom microfouling is suspected to be more harmful than seasonal settlement of larvae or spores. The latter spawn in large numbers in early spring predominantly, whereas diatom microfouling take place during entire year. The concentration of different types of grazers on living surfaces of coralline algae enables this low productive ecosystem to thrive well adjacent to highly productive kelp forests by generating a grazing shield. In contrast to kelp algal systems, maerl-forming coralline algae need uniform and predictable environmental conditions, due to their slow growth rates. Therefore, coralline algal ecosystems producing maerl-type carbonate deposits are found preferentially within wave-protected headland or skerry areas in higher latitudes. Seen in this light, carbonate production and even reef development in high latitudes is not the result of exceptional environmental conditions, but of fine-tuned biological feedback mechanisms enabling algal framework constructors to form islands of carbonate production and deposition within the phaeophytic belt. ACKNOWLEDGEMENTS The author wishes to thank E. Fliagel, G. Hillmer and J. Scholz for the organization of the DFG-Colloquium 'Microbial controls of carbonates and reefs' in Hamburg, 1992. I would like to to express my thanks to R. Steneck for his very valuable and constructive review. Special thanks to P. Schafer, R. Henrich, C. Samtleben, A. Munnecke, A. Wehrmann, and I. Werner for their valuable remarks. B.
147 Woelkerling, S. Daume, R. Asmus, K. Bandel and N. Mostafawi are greatly acknowledged for determining the coralline algae, diatoms, gastropods and ostracods. J. Welling improved the English wording. S. Perbandt very kindly prepared the photographs. This contribution arises from the scientific research project "Boreale Flachwasserkarbonate" (He 1671/1) which is part of the D F G priority program 'Globale und regionale Steuerungsprozesse biogener Sedimentation'.
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Manuscript received April 20, 1993 Revised manuscript accepted July 10, 1993
