Susan H. Brawley

The effect of micrograzers on algal community structure in a coral reef microcosm

The effect of amphipod grazing on algal community structure was studied within a 75 l refuge tank connected to a 6500 l closed-system, coral reef microcosm. When amphipods (Ampithoe ramondi) were absent or present in low numbers, a high biomass of mostly filamentous algal species resulted, including Bryopsis hypnoides, Centroceras clavulatum, Ceramium flaccidum, Derbesia vaucheriaeformis, Enteromorpha prolifera, Giffordia rallsiae, and Polysiphonia havanensis. These microalgae disappeared when amphipod density increase beyond approximately 1 individual cm-2 of tank surface. The macroalga Hypnea spinella germinated in the system in association with amphipod tube sites. H. spinella plants remained rare until filamentous species were eliminated by amphipod grazing. Feeding trials confirmed that H. spinella was protected from grazing by its size rather than a chemical defense strategy. The H. spinella community we observed is similar to the flora described on algal ridges where physical conditions exclude fish grazing. We suggest that amphipods and similar micrograzers are responsible for the algal community structure of these ridges. Caging experiments may be subject to similar effects from increased amphipod grazing on the algae. Introduction of fish that are amphipod predators into the refuge tank caused an increase in algal species diversity but total H. spinella growth rates fell from 25 g dry wt month-1 to less than 8 g dry wt month-1. We describe amphipod behavior in relation to changes in population density and food supply, and we stress the potential for increasing the productivity of commercial seaweeds through maintenance of appropriate amphipod species in mariculture facilities.

Porphyra: a marine crop shaped by stress

The marine red alga Porphyra is an important marine crop, worth ∼US

EVOLUTION OF THE FUCACEAE (PHAEOPHYCEAE) INFERRED FROM nrDNA‐ITS

1.3 billion per year. Cultivation research now includes farm ecology, breeding, strain conservation and new net-seeding technologies. The success of cultivation is due, in part, to the high stress tolerance of Porphyra. Many species of Porphyra lose 85-95% of their cellular water during the daytime low tide, when they are also exposed to high light and temperature stress. Antioxidant and mycosporine-like amino acid activities have been partially characterized in Porphyra, but, as we discuss here, the Porphyra umbilicalis genome project will further elucidate proteins associated with stress tolerance. Furthermore, phylogenomic and transcriptomic investigations of Porphyra sensu lato could elucidate tradeoffs made during physiological acclimation and factors associated with life-history evolution in this ancient lineage.

SURVIVAL OF FUCOID EMBRYOS IN THE INTERTIDAL ZONE DEPENDS UPON DEVELOPMENTAL STAGE AND MICROHABITAT1

Sequences of the internal transcribed spacer region (ITS‐1, 5.8S, and ITS‐2) of nuclear ribosomal DNA were obtained from 16 species representing all six genera of Fucaceae (Ascophyllum, Fucus, Hesperophycus, Pelvetia, Pelvetiopsis, and Xiphophora) plus one outgroup (Hormosira). Parsimony analysis indicated that the family Fucaceae is monophyletic and that the northern hemisphere taxa are highly divergent from the only southern hemisphere genus, Xiphophora. The genus Pelvetia is not monophyletic because the European P. canaliculata is more closely related to Fucus, Hesperophycus, and Pelvetiopsis than to other Pelvetia species. We establish Silvetia, gen. nov. and transfer the 3 Pacific species of Pelvetia to the new genus. Fucus is monophyletic and not ancestral in the Fucaceae. The ITS sequences identified two strongly supported lineages within Fucus, one with F. serratus sister to the clade containing F. gardneri, F. distichus, and F. evanescens and a second including F. vesiculosus, F. spiralis, F. ceranoides, and F. virsoides. The ITS was not useful for resolving relationships within each of these clusters and between populations of F. vesiculosus. Within‐individual variation in ITS sequences is high in Fucus, a derived genus, compared to Ascophyllum, a more ancestral genus. Mapping of the two characters that form the basis of Powell’s model for speciation in the Fucaceae showed that 1) number of eggs per oogonium has not followed a gradual reduction and that 2) monoecy/dioecy has changed several times during evolution of this family.

Ecological genetics in the North Atlantic: environmental gradients and adaptation at specific loci.

Embryos of the fucoid alga Pelvetia fastigiata (J. Ag.) DeToni were outplanted into the intertidal zone to assess survival during the physical stress brought about by emersion during a single low tide. Survival varied among microhabitats. Under the adult Pelvetia canopy, survival of 6‐h‐, 24‐h‐, 48‐h‐, and 1‐wk‐old embryos was nearly 100%. Almost all embryos of all ages died in exposed habitats on bare rock or within habitats where the Pelvetia canopy was removed experimentally. However, within red algal turfs, where most juvenile Pelvetia occur, survival was unusually age specific: 24‐ to 48‐h‐old embryos survived poorly compared to younger (6 h old) or older embryos (1 wk old). Survival patterns reflected microhabitat temperatures during the experiments. The fate of young post‐settlement stages must be studied at these fine temporal and spatial scales to understand the organization of intertidal communities.

Algae as nutritional and functional food sources: revisiting our understanding

The North Atlantic intertidal community provides a rich set of organismal and environmental material for the study of ecological genetics. Clearly defined environmental gradients exist at multiple spatial scales: there are broad latitudinal trends in temperature, meso-scale changes in salinity along estuaries, and smaller scale gradients in desiccation and temperature spanning the intertidal range. The geology and geography of the American and European coasts provide natural replication of these gradients, allowing for population genetic analyses of parallel adaptation to environmental stress and heterogeneity. Statistical methods have been developed that provide genomic neutrality tests of population differentiation and aid in the process of candidate gene identification. In this paper, we review studies of marine organisms that illustrate associations between an environmental gradient and specific genetic markers. Such highly differentiated markers become candidate genes for adaptation to the environmental factors in question, but the functional significance of genetic variants must be comprehensively evaluated. We present a set of predictions about locus-specific selection across latitudinal, estuarine, and intertidal gradients that are likely to exist in the North Atlantic. We further present new data and analyses that support and contradict these simple selection models. Some taxa show pronounced clinal variation at certain loci against a background of mild clinal variation at many loci. These cases illustrate the procedures necessary for distinguishing selection driven by internal genomic vs. external environmental factors. We suggest that the North Atlantic intertidal community provides a model system for identifying genes that matter in ecology due to the clarity of the environmental stresses and an extensive experimental literature on ecological function. While these organisms are typically poor genetic and genomic models, advances in comparative genomics have provided access to molecular tools that can now be applied to taxa with well-defined ecologies. As many of the organisms we discuss have tight physiological limits driven by climatic factors, this synthesis of molecular population genetics with marine ecology could provide a sensitive means of assessing evolutionary responses to climate change.

Distributional success of the marine seaweedFucus vesiculosus L. in the brackish Baltic Sea correlates with osmotic capabilities of Baltic gametes

Global demand for macroalgal and microalgal foods is growing, and algae are increasingly being consumed for functional benefits beyond the traditional considerations of nutrition and health. There is substantial evidence for the health benefits of algal-derived food products, but there remain considerable challenges in quantifying these benefits, as well as possible adverse effects. First, there is a limited understanding of nutritional composition across algal species, geographical regions, and seasons, all of which can substantially affect their dietary value. The second issue is quantifying which fractions of algal foods are bioavailable to humans, and which factors influence how food constituents are released, ranging from food preparation through genetic differentiation in the gut microbiome. Third is understanding how algal nutritional and functional constituents interact in human metabolism. Superimposed considerations are the effects of harvesting, storage, and food processing techniques that can dramatically influence the potential nutritive value of algal-derived foods. We highlight this rapidly advancing area of algal science with a particular focus on the key research required to assess better the health benefits of an alga or algal product. There are rich opportunities for phycologists in this emerging field, requiring exciting new experimental and collaborative approaches.

Fertilization in natural populations of the dioecious brown alga Fucus ceranoides and the importance of the polyspermy block

To understand the unique success of the marine seaweedFucus vesiculosus L. (PHaeophyceae) in the brackish Baltic Sea, the performance of gametes from Baltic [4.1–6.5‰S (Salinity)] and marine populations was studied. Sperm from BalticF. vesiculosus swam with a path velocity of c. 30–110 μm/s and could fertilize eggs in waters of salinities from 4 to 33‰S. In their natural water, Baltic sperm were not negatively phototactic, unlike marine sperm in seawater; this should decrease the sperm:egg concentration at the seafloor and reduce the likelihood of polyspermy. Marine (Iceland, Sweden) sperm in seawater had a path velocity of c. 80–100 μm/s, but performed poorly and could not fertilize eggs in natural or artificial Baltic water ≤6‰S; therefore, Baltic populations have adapted or acclimated to their brackish habitat. Baltic populations appear better adapted to their natural low salinities because, even after culturing Baltic and marine individuals in water from both the Baltic (6.5‰S) and the marine Skagerrak (21‰S), Baltic sperm were in both cases still able to swim and fertilize eggs at lower salinities (4‰S) than marine sperm; fertilization never occurred between marine gametes at 4–6‰S. However,F. vesiculosus acclimates to some salinities, since sperm from Baltic and marine males that had been cultured at 21‰S swam better (higher velocity, proportion that were motile and/or linearity) in marine salinities (21–33‰S) than when they were cultured at 6.5‰S. The effects of salinity on sperm motility and fertilization were osmolar rather than due to specific ionic requirements, over the tested range. The osmolalities (< c. 100 mmol/kg) at which fertilization success of Baltic gametes decreases nearly to zero correspond to the osmolality of Baltic water at the northernmost limit of distribution ofF. vesiculosus in the Baltic Sea. Therefore, the present range ofF. vesiculosus in the Baltic appears to correspond to the osmotic tolerance of the gametes. Very small natural or anthropogenic increases in ambient osmolality would be likely to cause a substantial expansion of this species into the inner Baltic.

CONTROL OF GAMETE RELEASE IN FUCOID ALGAE: SENSING HYDRODYNAMIC CONDITIONS VIA CARBON ACQUISITION

The brown alga Fucus ceranoides L. was studied in several estuaries on the Isle of Man (Great Britain) in the summers of 1989 and 1990. The objective were to determine the success of natural fertilization in a dioecious organism with external fertilization and to contribute to our understanding of processes such as polyspermy blocks and propagule settlement under natural conditions. Gamete release occurred on a semilunar cycle near full and new moons; at such times, settlement densities of 500 zygotes cm-2 d-1 were common. Gamete release was largely restricted to daytime high tides. Fertilization success was high: about 95 to 100% of all eggs released were fertilized, and 1 to 9% of these zygotes were polyspermic. The incidence of polyspermy increased towards the upper limit of F. ceranoides in the estuary of the river Neb; this may be significant in the context of the Na+-dependent block against polyspermy. Levels of polyspermy were not related to fertilization success (R2=0.06). Rates of pronuclear migration and karyogamy determined in the laboratory were used as an internal clock to estimate when eggs were fertilized in the field. Most eggs were fertilized 30 to 120 min after plants were immersed by the incoming tide, which corresponded to the period 60 min before to 30 min after high tide. The high success of fertilization suggests that polyspermy blocks are important in nature, and, in combination with the high settlement of zygotes, shows that population size in F. ceranoides is determined by post-settlement mortality, not by propagule availability.

STUDIES OF MESOHERBIVORY IN AQUARIA AND IN AN UNBARRICADED MARICULTURE FARM ON THE CHINESE COAST1

We investigated the environmental factors providing signals for gamete re- lease in fucoid algae, with a particular focus on the inhibitory effect of water motion. The release of gametes by Fucus distichus occurred in still water under high light and was associated with the depletion of dissolved inorganic carbon (DIC) in tide pools isolated from the ocean during daytime low tides. Diurnal patterns of gamete release that lasted for 2-3 d, as in natural populations, were found in receptacles cultured in a 12 h light: 12 h dark photoperiod under calm conditions or in a simulated tidal regime. Constant light disrupted the diurnal component of release, however, suggesting that an endogenous cir- cadian periodicity was absent. The effects of increased (DIC) on cultured receptacles under calm conditions were similar to the inhibitory effects of high water motion; both conditions reduced release in several species from both tide pool and intertidal habitats. Bicarbonate concentration, rather than carbon dioxide, or carbonate, was shown to be the component of the DIC system most closely correlated (inversely) with gamete release in the intertidal fucoid Pelvetia compressa. The hypothesis that gamete release is triggered by DIC depletion in the unstirred boundary layer during periods of low water motion in the light was further supported by experiments with P. compressa. These showed that gamete release was not inhibited by high water motion when DIC was absent. In the same experiments, high water motion inhibited release at 2 and 20 mmol/L DIC, confirming that the sensitivity of gamete release to water motion is DIC dependent. The ability of fucoid algae to couple physiological processes (e.g., photosynthesis) with life history events (gamete release) allows external fertilization to occur under favorable hydrodynamic conditions, and may contribute greatly to reproductive success in organisms inhabiting periodically turbulent environments.