Mycosporine-like amino acid content in four species of sea anemones in the genus Anthopleura reflects phylogenetic but not environmental or symbiotic relationships

We examine the occurrence of UV-absorbing, mycosporine-like amino acids (MAAs) in four sympatric species of sea anemones in the genus Anthopleura, all collected from intertidal habitats on the Pacific Coast of temperate North America. We compare patterns of MAAs in A. elegantissima of several types: specimens having predominately zooxanthellae (dinoflagellates comprising at least two species) or zoochlorellae as symbionts; those containing algal endosymbionts of both kinds, and naturally occurring aposymbiotic specimens that lack the endosymbionts typically found in most specimens. We also compare MAAs in zooxanthellate specimens of A. sola and A. xanthogrammica, and specimens from the asymbiotic species A. artemisia. Our findings indicate that the complements of the four major MAAs in these species of Anthopleura (mycosporine-taurine, shinorine, porphyra-334, and mycosporine-2 glycine) broadly reflect phylogenetic differences among the anemones rather than the taxon of endosymbionts, presence or absence of symbionts, or environmental factors. An exception, however, occurs in A. elegantissima, where mycosporine-2 glycine increases in concentration with the density of zooxanthellae. Our evidence also shows that A. elegantissima can accumulate MAAs from its food, which may explain the occasional occurrence of minor MAAs in some individuals.     

Phylogenetic placement of "zoochlorellae" (Chlorophyta), algal symbiont of the temperate sea anemone Anthopleura elegantissima

At northern latitudes the sea anemones Anthopleura elegantissima and its congener A. xanthogrammica contain unidentified green chlorophytes (zoochlorellae) in addition to dinophytes belonging to the genus Symbiodinium. This dual algal symbiosis, involving members of distinct algal phyla in one host, has been extensively studied from the perspective of the ecological and energetic consequences of hosting one symbiotic type over the other. However, the identity of the green algal symbiont has remained elusive. We determined the phylogenetic position of the marine zoochlorellae inhabiting A. elegantissima by comparing sequence data from two cellular compartments, the nuclear 18S ribosomal RNA gene region and the plastid-encoded rbcL gene. The results support the inclusion of these zoochlorellae in a clade of green algae that form symbioses with animal (Anthopleura elegantissima), fungal (the lichen genus Nephroma), and seed plant (Ginkgo) partners. This clade is distinct from the Chlorella symbionts of Hydra. The phylogenetic diversity of algal hosts observed in this clade indicates a predisposition for this group of algae to participate in symbioses. An integrative approach to the study of these algae, both within the host and in culture, should yield important clues about how algae become symbionts in other organisms.     

Nutritional role of two algal symbionts in the temperate sea anemone Anthopleura elegantissima brandt

The intertidal sea anemone Anthopleura elegantissima in the Pacific Northwest may host a single type of algal symbiont or two different algal symbionts simultaneously: zooxanthellae (Symbiodinium muscatinei) and zoochlorellae (green algae; Trebouxiophyceae, Chlorophyta). A seasonal comparison of zooxanthellate and zoochlorellate anemones showed stable symbiont population densities in summer and winter, with densities of zoochlorellae about 4 times those of zooxanthellae. Photosynthesis-irradiance curves of freshly isolated symbionts show that the productivity (P(max) cell) of freshly isolated zooxanthellae was about 2.5 times that of zoochlorellae during July; comparable rates were obtained in other months. Models of algal carbon flux show that zoochlorellae may supply the host with more photosynthetic carbon per unit anemone biomass than zooxanthellae supply. Zooxanthellate anemone tissue was 2 per thousand ((13)C) and 5 per thousand ((15)N) enriched and zoochlorellate anemone tissue was 6 per thousand ((13)C) and 8 per thousand ((15)N) enriched over their respective symbionts, suggesting that zoochlorellate anemones receive less nutrition from their symbionts than do zooxanthellate individuals. The disparity between predicted contributions from the algal carbon budgets and the stable isotopic composition suggests that short-term measures of algal contributions may not reflect actual nutritional inputs to the host. Isotopic data support the hypothesis of substantial reliance on external food sources. This additional nutrition may allow both algae to persist in this temperate intertidal anemone in spite of differences in seasonal photosynthetic carbon contributions.     

Chemosensory and feeding responses of the nudibranch Aeolidia papillosa to the symbiotic sea anemone Anthopleura elegantissima

Abstract. The aeolid nudibranch Aeolidia papillosa is an important predator on the sea anemone Anthopleura elegantissima , a host to two kinds of endosymbiotic algae: zooxanthellae and zoochlorellae. The possible influence of the algae on the nudibranch's predatory response to this anemone was examined in a laboratory study. In chemosensory experiments, the nudibranch detected and chose anemone scent over a seawater control, but in both chemosensory and feeding experiments showed no preference for zooxanthellate or zoochlorellate anemones. Ingestive conditioning on zooxanthellate or zoochlorellate anemones had no effect on choice of these two anemone types in chemosensory experiments. Comparisons of the productivity and photosynthetic pigments of algae obtained from nudibranch feces and from anemones show that both algae survive passage through the nudibranch gut. The productivity of fecal zooxanthellae was 1.6X greater than that of zooxanthellae freshly isolated from anemones, although the chlorophyll a content of fecal zooxanthellae was reduced. The productivity and amount of pigments were the same for zoochlorellae in nudibranch feces and freshly isolated from anemones. Comparing fecal and isolated algae, there was no significant difference in the percentage of zooxanthellae in the process of cell division. However, the percentage of dividing cells was 2.6X higher in fecal than in freshly isolated zoochlorellae (18% and 6.9% respectively). Although the endosymbiotic algae do not make their host more or less attractive to the nudibranch, this predator may play an important role in maintaining the symbiotic relationship of Anthopleura elegantissima with zooxanthellae and zoochlorellae by providing viable algae in its feces as a source for the anemone host.     

The intertidal distribution of two algal symbionts hosted by Anthopleura xanthogrammica (Brandt 1835)

This paper quantifies the spatial distribution of zooxanthellae (ZX) and zoochlorellae (ZC), two algal symbionts common to the temperate anemone, Anthopleura xanthogrammica, in relation to shore height. Anemones in tidepools and crevices had varying algal proportions: >0.90 ZC (green anemones), 0.10 to 0.90 ZX (mixed), and >0.90 ZX (brown). Brown anemones are primarily found in the high intertidal and the upper region of tidepools. Mixed anemones are most common at intermediate shore heights and green anemones are exclusive to the low shore and at increasing depth in tidepools. Microhabitat was also important to algal proportion, as anemones in crevices had greater proportions of ZC than anemones in tidepools at the same shore height. In a reciprocal transplant experiment, A. xanthogrammica were moved between high and low shallow tidepools. All anemones moved from a low to a high tidepool exhibited a shift from ZC to ZX populations, while the anemones transplanted from high to low tidepools maintained ZX dominance. This is the first documentation that field algal populations can shift from ZC to ZX in Anthopleura. The field survey and transplant study results support the hypothesis that the relative abundance of ZX and ZC in A. xanthogrammica is influenced by the environmental gradient associated with shore height and microhabitat.     

Amino acid sequence of the Anthopleura xanthogrammica heart stimulant, anthopleurin-B

Anthopleurin-B, the most potent peptide heart stimulant from the sea anemone Anthopleura xanthogrammica, was shown to exist as a single polypeptide chain consisting of 49 amino acid residues. The sequence of the peptide was shown to be: Gly-Val-Pro-Cys-Leu-Cys-Asp-Ser-Asp-Gly- Pro-Arg-Pro-Arg-Gly-Asn-Thr-Leu-Ser-Gly-Ile-Leu-Trp-Phe-Tyr-Pro-Ser- Gly-Cys-Pro-Ser-Gly-Trp-His-Asn-Cys-Lys-Ala-His-Gly-Pro-Asn-Ile-Gly- Trp-Cys-Cys-Lys-Lys. The carboxymethylcysteine derivative, tryptic and chymotryptic peptides (obtained from the derivative and separated by high performance liquid chromatography) were sequenced by manual Edman degradation. Although six carboxymethylcysteine residues were formed by reduction and alkylation of the polypeptide, no cysteine residues were detectable in the native protein, indicating that there are three cystine residues in anthopleurin-B. The amino acid sequence differs in 7 places from anthopleurin-A: at residues 3 (Pro for Ser), 12 (Arg for Ser), 13 (Pro for Val), 21 (Ile for Thr), 24 (Phe for Leu), 42 (Asn for Thr), and 49 (Lys for Gln). These differences are important since anthopleurin-B is about a 12.5-fold better heart stimulant than anthopleurin-A from A. xanthogrammica, anthopleurin-C from Anthopleura elegantissima, and toxin II from Anemonia sulcata.     

BROAD THERMAL TOLERANCE OF THE SYMBIOTIC DINOFLAGELLATE SYMBIODINIUM MUSCATINEI (DINOPHYTA) IN THE SEA ANEMONE ANTHOPLEURA ELEGANTISSIMA (CNIDARIA) FROM NORTHERN LATITUDES1

The sea anemone Anthopleura elegantissima (Brandt) hosts two species of symbiotic dinoflagellates, known as zooxanthellae, which coexist within the host at southern latitudes only. One of these species, Symbiodinium muscatinei LaJeunesse et Trench, has a broad latitudinal distribution, occurring in intertidal anemones from Washington state to Southern California. To investigate whether high thermal tolerance contributes to the ability of S. muscatinei to inhabit anemones from northern and southern regions, the upper thermal tolerance limit for photosynthesis of symbionts in northern (48°24′ N) populations of A. elegantissima was determined by subjecting anemones to a gradual increase in temperature from 12°C to 30°C over a 10‐week period. Light‐saturated photosynthetic rates of isolated zooxanthellae were the same over the range of 12°C–24°C and declined significantly at 26°C, which is 14°C and 5°C above average summertime seawater temperatures in northern Puget Sound and Southern California, respectively. At 28°C, zooxanthellae isolated from the anemones, and those expelled by their hosts, exhibited extremely low rates of photosynthesis and highly reduced chl content. The photosynthetic rates and chl content of expelled zooxanthellae were lower than those of retained zooxanthellae. The high thermal tolerance of S. muscatinei isolated from northern populations of anemones supports the broad latitudinal distribution of this symbiont, allowing it to coexist with S. californium (#383, Banaszak et al. 1993 ) in southern populations of anemones.     

BREAKING UP AND GETTING TOGETHER: EVOLUTION OF SYMBIOSIS AND CLONING BY FISSION IN SEA ANEMONES (GENUS ANTHOPLEURA)

Abstract Clonal growth and symbiosis with photosynthetic zooxanthellae typify many genera of marine organisms, suggesting that these traits are usually conserved. However, some, such as Anthopleura , a genus of sea anemones, contain members lacking one or both of these traits. The evolutionary origins of these traits in 13 species of Anthopleura were inferred from a molecular phylogeny derived from 395 bp of the mitochondrial 16S rRNA gene and 410 bp of the mitochondrial cytochrome oxidase subunit III gene. Sequences from these genes were combined and analyzed by maximum-parsimony, maximum-likelihood, and neighbor-joining methods. Best trees from each method indicated a minimum of four changes in growth mode and that symbiosis with zooxanthellae has arisen independently in eastern and western Pacific species. Alternative trees in which species sharing growth modes or the symbiotic condition were constrained to be monophyletic were significantly worse than best trees. Although clade composition was mostly consistent with geographic sympatry, A. artemisia from California was included in the western Pacific clade. Likewise, A. midori from Japan was not placed in a clade containing only other Asian congeners. The history of Anthopleura includes repeated shifts between clonality and solitariness, repeated attainment of symbiosis with zooxanthellae, and intercontinental dispersal.     

Competition for space among sessile marine invertebrates: changes in HSP70 expression in two Pacific cnidarians.

The role of stress proteins-either constitutive (HSC) or inducible (HSP)-of the HSP70 family in intra- and interspecific competition for space was examined in two sessile Pacific cnidarians. Anthopleura elegantissima, an intertidal anemone, and Corynactis californica, a subtidal corallimorpharian, express HSP70 in the absence of apparent physical stress. HSP70 protein expression is concentrated in the tentacles of A. elegantissima when the animal is exposed to contact with other benthic organisms. Under the same conditions, however, HSP concentrations are similar in the body and tentacles of C. californica. When two different clones of A. elegantissima interact in the field, the outside polyps (warriors) express more HSP70 than the inside ones (2.4 versus 0.6 ng HSP70/microg Protein). When different C. californica clones interact, HSP70 expression in the outside and inside polyps is similar (1.5 versus 1.8 ng HSP70/microg P) and is fairly constant in the corallimorpharian in the different interspecific encounters. HSP70 expression is related to the different kinds of aggression encountered by both cnidarians. HSP70 expression may be involved in the recovery of tissues damaged by the allelochemical, cytotoxical, or corrosive substances produced by different enemies. C. californica clones appear prepared for war, as evidenced by the high constant expression of HSP70 in the polyps. A. elegantissima exhibits differential HSP70 expression depending on the identity of each neighboring intra- or interspecific sessile competitor. We propose that stress proteins can be used to quantify space competition or aggression among sessile marine invertebrates.     

Mixotrophy in ciliates

Mixotrophy is the occurrence of phagotrophy and phototrophy in the same organism. In ciliates the intracellular phototroph can be unicellular green algae (zoochlorellae), dinoflagellates (zooxanthellae), cryptomonads or sequestered chloroplasts from ingested algae. An intermediate mixotrophic mechanism is that where the phagotroph ingests algal cells, maintains them intact and functional in the cytoplasm for some time, but the algae are afterwards digested. This seems to occur in some species of Mesodinium. Ciliates with phototrophic endosymbionts have evolved independently in marine and freshwater habitats. The enslaved algal cells or chloroplasts provide host cells with organic matter. Mixotrophs flourish in oxygen-rich, but also in micro-aerobic waters and in the complete absence of oxygen. In the latter case, the aerobic host retains aerobic metabolism, sustained by the oxygen produced by the phototrophic endosymbionts or the sequestered chloroplasts. Mixotrophic ciliates can attain spectacular abundances in some habitats, and entirely dominate the ciliate community.     

Calorimetric Studies of Behavior, Metabolism and Energetics of Sessile Intertidal Animals

SYNOPSIS: Behaviors to conserve water during intertidal exposureat the same time impair respiratory gas exchange, so that observedresponses to emersion may reflect compromises between theseincompatible needs. Behavioral isolation of the tissues fromair results in the complete or partial reliance on anoxic energymetabolism, which is most reliably measured directly as heatdissipation. Combined direct calorimetry and indirect calorimetry(respirometry) enable the partitioning of total metabolic heatdissipation into its aerobic and anoxic components, which mayvary according to physical and biological factors. The musselMytilus edulis is tolerant of anoxia and saves water and energyduring aerial exposure in its rocky intertidal habitat by closingits shell valves and becoming largely anoxic. Like most suspensionfeeders in this habitat, its compensation for reduced feedingtime involves energy conservation; there is little evidencefor energy supplementation such as increases in feeding rateor absorption efficiency. Ammonia production continues duringaerial exposure and is involved in acid-base balance in thehemolymph and mantle cavity fluid. Infaunal cockles (Cardiumedule) and mussels (Geukensia demissa) gape their shell valves,remain largely aerobic and have high rates of heat dissipationduring intertidal exposure, a response which appears relatedto the lower desiccation potential and exploitation of richertrophic resources in their soft-sediment habitats. The variableexpansion of the symbiotic sea anemone Anthopleura elegantissimareflects interaction among the responses to desiccation, irradianceand continued photosynthesis by its zooxanthellae during exposureto air.     

Localization of a symbiosis-related protein, Sym32, in the Anthopleura elegantissima-Symbiodinium muscatinei Association

Cnidarian-dinoflagellate symbioses are widespread in the marine environment. Growing concern over the health of coral reef ecosystems has revealed a fundamental lack of knowledge of how cnidarian-algal associations are regulated at the cellular and molecular level. We are interested in identifying genes that mediate interactions between the partners, and we are using the temperate sea anemone Anthopleura elegantissima as a model. We previously described a host gene, sym32, encoding a fasciclin domain protein, that is differentially expressed in symbiotic and aposymbiotic A. elegantissima. Here, we describe the subcellular localization of the sym32 protein. In aposymbiotic (symbiont-free) hosts, sym32 was located in vesicles that occur along the apical edges of gastrodermal cells. In symbiotic hosts, such vesicles were absent, but sym32 was present within the symbiosome membranes. Sym32 (or a cross-reactive protein) was also present in the accumulation bodies of the symbionts. Although the anti-sym32 antiserum was not sufficiently specific to detect the target protein in cultured Symbiodinium bermudense cells, Western blots of proteins from two Symbiodinium species revealed a protein doublet of 45 and 48 kDa, suggesting that the symbionts may also produce a fasciclin domain protein. We suggest that host sym32 is relocated from gastrodermal vesicles to the symbiosome membrane when symbionts are taken into host cells by phagocytosis.     

CARBOHYDRATE MOVEMENT FROM AUTOTROPHS TO HETEROTROPHS IN PARASITIC and MUTUALISTIC SYMBIOSIS

1. The bulk of the fixed carbon which moves from autotroph to heterotroph in most symbiotic associations is in a single compound, a carbohydrate. Techniques employing ¹⁴C have been most valuable for investigating this movement. 2. Most ‘zoochlorellae’ belong to the Chlorococcales, and they release carbohydrate to the animal tissue as either glucose or maltose. In some molluscs, the ‘zoochlorellae’ are actually chloroplasts, possibly derived from siphonaceous algae. Although it is known that these chloroplasts supply photosynthetically fixed carbon to the animal tissue, the form of the carbon compounds which move is not known. In Convoluta roscoffensis the ‘zoochlorellae’ belong to the Pyramimonadales, but carbohydrate movement has not yet been directly studied in this association. 3. Most ‘zooxanthellae’ belong to the Dinophyceae. In associations involving co-elenterates and molluscs, glycerol is the main carbohydrate moving to the animal. Homogenates of the host animal tissue stimulate excretion by isolated zooxanthellae. 4. In lichens, symbiotic blue-green algae release glucose to the fungus, but the various genera of green algae that have been studied all release polyols (either ery-thritol, ribitol or sorbitol). Lichen fungi rapidly synthesize mannitol from all these compounds. When lichen algae are isolated into pure culture, they soon lose the ability to excrete carbohydrate, and intracellular production of the carbohydrate that is excreted either becomes much reduced, or ceases altogether. 5. Mostly indirect evidence indicates that sucrose is the main carbohydrate moving from flowering plants to their associated symbiotic fungi. Diversion of the translocation stream towards the site of the association occurs. The fungi convert host sugars to their own carbohydrates, principally trehalose and polyols. 6. ‘Saprophytic’ higher plants are all obligately mycotrophic and receive carbohydrate from their associated fungi. In at least some associations, the fungus is simultaneously associated with an autotrophic higher plant, which is the ultimate source of carbohydrate for the association. 7. Some parasitic higher plants possess chlorophyll, but the extent to which they depend on their host for carbohydrate varies with different species. Green mistletoes evidently derive negligible carbon from their hosts, but other green parasites derive at least some. There is no evidence that any of the chlorophyll-containing parasites export carbohydrate back to their hosts. Parasitic higher plants which lack chlorophyll presumably derive all their carbohydrates from their hosts, but experimental investigations of this are scarce. 8. Comparison between different types of symbiotic association show that a number of common features emerge. 9. The algal symbionts of both invertebrates and lichens have, in comparison to free-living forms, reduced growth rates and greater incorporation of fixed carbon into soluble carbohydrates. They excrete a much greater proportion of their fixed carbon than free-living forms, and most of it is usually as a single carbohydrate. Particularly striking is the fact that the excreted carbohydrate is one which is either not the major intracellular carbohydrate, or one which ceases or nearly ceases to be produced in culture. 10. The translocation stream of autotrophic higher plants is diverted towards the site of association with either fungi or parasitic higher plants, but it is not known how this is achieved. 11. In all associations, the cell walls of the autotroph become reduced or modified at the site of contact with the heterotroph, but it seems likely that this is not directly connected with the mechanism of carbohydrate transfer between the symbionts. 12. In many associations, the heterotroph rapidly converts host sugars into other compounds (frequently into its own carbohydrates which are usually different from those of the host). This may serve to maintain a concentration gradient and so ensure a continued flow from the host. 13. Polyols feature prominently in symbiotic and parasitic associations, not only as the carbohydrates of many plant heterotrophs, but also as the form of carbohydrate released by both zooxanthellae and the green algae of lichens to their heterotrophic partners.     

Contrast Between Solitary and Clonal Lifestyles in the Sea Anemone Anthopleura elegantissima

The common intertidal sea anemone Anthopleura elegantissima(Brandt) occurs in two forms the clonal aggregating form andthe solitary form The obvious differences between the two apparentlyresult from the presence of asexual reproduction in the clonalaggregating form and its absence in the solitary form resultingdifferences in growth form suit the two anemones to differentlifestyles The clonal form is well suited to life higher inthe mid intertidal Asexual reproduction resulting in moderatelysmall individual size and close association with clonematesimproves its resistance to physical stress (drag and desiccation)and makes it a superior competitor in exposed habitats higherin the intertidal where species diversity and predator pressureare low The larger solitary animals live in more protected microhabitatslower in the intertidal and subtidal and are probably more resistantto predation and less able to withstand physical stress or intenseintraspecific competition The two forms also have differentbiogeographic ranges While the clonal aggregations are quitecommon at rocky sites at least as far north as Vancouver Islandin British Columbia populations of solitaries have not beenfound north of Point Reyes California Apparently the two formsare re productively isolated phenotype frequencies are verydifferent for clonals and solitaries living at the same locationswhile the between-sample variation within each form is relativelysmall These differences in phenotype frequencies biogeographicrange and microhabitat suggest that the clonal anemones andthe solitary anemones known as Anthopleura elegantissima areactually a sibling species pair.     

Nudibranch-sponge feeding dynamics: Benefits of symbiont-containing sponge to Archidoris montereyensis (Cooper, 1862) and recovery of nudibranch feeding scars by Halichondria panicea (Pallas, 1766)

Selected interactions between the encrusting sponge Halichondria panicea and its primary predator, the dorid nudibranch Archidoris montereyensis, were investigated in a high-latitude rocky intertidal community spatially dominated by H. panicea. Feeding experiments were conducted in which A. montereyensis pairs were provided with sponge containing symbiotic zoochlorellae or sponge in which the zoochlorellae population had been reduced or removed by shading. Nudibranchs consuming H. panicea with symbiotic zoochlorellae had higher feeding, growth, and egg production rates than individuals eating aposymbiotic sponge. We simulated A. montereyensis predation on H. panicea by creating typically sized feeding grooves in the sponge. H. panicea's response was high linear growth rates into the experimental feeding grooves, generally recovering most of the groove area within 4 weeks. Overall, the sponge's rapid response to tissue damage minimizes grazing impacts and substrate loss and reduces susceptibility to wave removal.     

Diet,food preference,and algal availability for fishes and crabs on intertidal reef communities in southern California

Synopsis Herbivory by wide-ranging fishes is common over tropical reefs, but rare in temperate latitudes where the effects of herbivorous fishes are thought to be minimal. Along the west coast of North America, herbivory by fishes on nearshore reefs is largely restricted to a few members of the Kyphosidae, distributed south of Pt. Conception. This paper presents information on natural diets and results from feeding choice experiments for two abundant kyphosids from intertidal habitats in San Diego, California —Girella nigricans andHermosilla azurea, and similar data for the lined shore crab,Pachygrapsus crassipes, which also forages over intertidal reefs. These results are compared with the availability of algae in intertidal habitats measured during summer and winter, on both disturbed and undisturbed habitats. The diets of juveniles ofG. nigricans andH. azurea collected from nearshore habitats were dominated by animal prey (mainly amphipods), but adults of these fishes, andP. crassipes, consumed algae nearly exclusively, with 26, 10, and 14 taxa of algae identified fromG. nigricans, H. azurea, andP. crassipes, respectively. Algae with sheet-like morphologies (e.g.Ulva sp.,Enteromorpha sp., members of the Delesseriaceae) were the principal algae in the diets of the fishes, and calcareous algae (e.g.Corallina sp.,Lithothrix aspergillum) and sheet-like algae (Enteromorpha sp.) comprised the greatest identifiable portion of the shore crab's diet. Feeding choice experiments indicated that the fishes preferred filamentous algae (e.g.Centroceras clavulatum, Polysiphonia sp.,Chondria californica) and sheet-like algae (e.g.Enteromorpha sp.,Ulva sp.,Cryptopleura crispa) over other algal morphologies, whereas the shore crab chose jointed calcareous algae (e.g.Lithothrix aspergillum, Corallina vancouveriensis, Jania sp.) most frequently. The diets and preferences for algae by the fishes were generally most similar to the assemblage of algae available in early successional (disturbed) habitats during summer when sheet-like and filamentous algae are abundant. The shore crab exhibited the opposite trend with a diet more similar to late successional (undisturbed) habitats.     

Latitudinal variation in intertidal algal community structure: the influence of grazing and vegetative propagation

Summary The hypothesis that sea urchin grazing and interactions with turf-forming red algae prevent large brown algae from forming an extensive canopy in the low intertidal zone of southern California was tested with field experiments at two study sites. Experimental removal of sea urchins resulted in rapid algal recruitment. Crustose coralline algae which typically dominate the substratum in areas with dense urchin populations were quickly overgrown by several species of short-lived green, brown and red algae. The removal of urchins also significantly increased the recruitment of two long-lived species of large brown algae (Egregia laevigata and Cystoseira osmundacea at one study site and E. laevigata and Halidrys dioica at the other). The experimental plots at both sites were eventually dominated by perennial red algae.A two-factorial experiment demonstrated that sea urchin grazing and preemption of space by red algae in areas where urchins are less abundant are responsible for the rarity of large brown algae in the low intertidal of southern California. The three dominant perennial red algae, Gigartina canaliculata, Laurencia pacifica and Gastroclonium coulteri, recruit seasonally from settled spores but can rapidly fill open space with vigorous vegetative growth throughout the year. These species encroach laterally into space created by the deaths of large brown algae or by other disturbances. Once extensive turfs of these red algae are established further invasion is inhibited. This interaction of algae which proliferate vegetatively with algae which recruit only from settled spores is analogous to those which occur between solitary and colonial marine invertebrates and between solitary and cloning terrestrial plants.It is suggested that a north-south gradient in the abundance of vegetatively propagating species, in grazing intensity and in the frequency of space-clearing disturbances, may account for latitudinal variation in intertidal algal community structure along the Pacific coast of North America.     

Trophic ecology of a freshwater sponge (Spongilla lacustris) revealed by stable isotope analysis

The vital roles that sponges play in marine habitats are well-known. However, sponges inhabiting freshwaters have been largely ignored despite having widespread distributions and often high local abundances. We used natural abundance stable isotope signatures of carbon and nitrogen (δ ¹³C and δ ¹⁵N) to infer the primary food source of the cosmopolitan freshwater sponge Spongilla lacustris. Our results suggest that S. lacustris feed largely on pelagic resources and may therefore link pelagic and benthic food webs. A facultative association between S. lacustris and endosymbiotic green algae caused S. lacustris to have significantly depleted carbon and nitrogen signatures that may reflect carbon and nitrogen exchange between sponges and their symbiotic algae. Isotopic data from specialist sponge consumers demonstrated that sponges hosting zoochlorellae were the major component of the diet of the spongillafly Climacia areolaris and the sponge-eating caddisfly Ceraclea resurgens suggesting that the symbiosis between freshwater sponges and algae is important to sponge predator trophic ecology. Our results help define the role of sponges in freshwater ecosystems and shed new light on the evolution and ecological consequences of a complex tri-trophic symbiosis involving freshwater sponges, zoochlorellae, and spongivorous insects.