Charles D. Amsler

Algal chemical ecology

1. The chemistry of algal secondary metabolism by J. Alan Maschek and Bill J. Baker* 2. Macroalgal chemical defenses and their roles in structuring tropical marine communities by Renato Crespo Pereira* and Bernardo Antonio Perez da Gama 3. Macroalgal chemical defenses and their roles in structuring temperate marine communities by Veijo Jormalainen* and Tuija Honkanen 4. Macroalgal chemical defenses in polar marine communities by Charles D. Amsler*, James B. McClintock, and Bill J. Baker 5. Macroalgal and cyanobacterial chemical defenses in freshwater communities by Frank A. Camacho 6. New perspectives for addressing patterns of secondary metabolites in marine macroalgae by Karen N. Pelletreau and Nancy M. Targett* 7. Macroalgal models in testing and extending defense theories by Henrik Pavia* and Gunilla B. Toth 8. Ecological and physiological roles of dimethylsulfoniopropionate (DMSP) and DMSP cleavage in marine macroalgae by Kathryn L. Van Alstyne 9. Influence of algal secondary metabolites on plankton community structure by Georg Pohnert 10. Herbivore offense in the sea: the detoxification and transport of secondary metabolites by Erik E. Sotka* and Kristen E. Whalen 11. Secondary metabolite defenses against pathogens and biofoulers by Amy L. Lane and Julia Kubanek* 12. Oxidative burst and related responses in biotic interactions of algae by Philippe Potin 13. Defense strategies of algae and cyanobacteria against solar ultraviolet radiation by Ulf Karsten 14. Algal sensory chemical ecology by Charles D. Amsler

Ecology of Antarctic Marine Sponges: An Overview'

Abstract Sponges are important components of marine benthic communities of Antarctica. Numbers of species are high, within the lower range for tropical latitudes, similar to those in the Arctic, and comparable or higher than those of temperate marine environments. Many have circumpolar distributions and in some habitats hexactinellids dominate benthic biomass. Antarctic sponge assemblages contribute considerable structural heterogeneity for colonizing epibionts. They also represent a significant source of nutrients to prospective predators, including a suite of spongivorous sea stars whose selective foraging behaviors have important ramifications upon community structure. The highly seasonal plankton blooms that typify the Antarctic continental shelf are paradoxical when considering the planktivorous diets of sponges. Throughout much of the year Antarctic sponges must either exploit alternate sources of nutrition such as dissolved organic carbon or be physiologically adapted to withstand resource constraints. In contrast to predictions that global patterns of predation should select for an inverse correlation between latitude and chemical defenses in marine sponges, such defenses are not uncommon in Antarctic sponges. Some species sequester their defensive metabolites in the outermost layers where they are optimally effective against sea star predation. Secondary metabolites have also been shown to short-circuit molting in sponge-feeding amphipods and prevent fouling by diatoms. Coloration in Antarctic sponges may be the result of relict pigments originally selected for aposematism or UV screens yet conserved because of their defensive properties. This hypothesis is supported by the bioactive properties of pigments examined to date in a suite of common Antarctic sponges.

Dispersal in Kelps: Factors Affecting Spore Swimming and Competency

The distance over which propagules can successfully colonize new sites de- pends on processes that increase the time they remain competent while being dispersed. As do feeding larvae, algal spores can contribute to their own nutrition (via photosynthesis) during dispersal. We explored the dispersal potential of the kelps Macrocystis pyrifera and Ptervgophora californica in laboratory experiments by examining (1) how long their spores can swim, (2) the contribution of energy derived from photosynthesis to spore swimming duration, and (3) the ability of spores to germinate and attach after they stop swimming. Results indicate that under photosynthetically saturating irradiance no spores of either species can swim longer than 120 h; < 10% of the spores were still swimming after 72 h. When placed in the dark, spores did not swim longer than 72 h; < 10% remained swimming after 48 h. More importantly, spores did not die after they stopped swimming; most germinated in the water column and retained their capacity to produce viable sporophyte recruits. The ability of spores to attach after they stopped swimming differed between the two species; settlement density declined in Macrocystis and increased in Pterygophora. Thus, the viable planktonic stage of these algae is not necessarily restricted to the spore but may include later life history stages. These results provide biological evidence that the spores and germlings of these kelps can remain competent in the plankton for extended periods of time, which is consistent with our previous findings that their dispersal can occur over greater distances than previously thought possible.

Rapid dissolution of shells of weakly calcified Antarctic benthic macroorganisms indicates high vulnerability to ocean acidification.

Abstract Antarctic calcified macroorganisms are particularly vulnerable to ocean acidification because many are weakly calcified, the dissolution rates of calcium carbonate are inversely related to temperature, and high latitude seas are predicted to become undersaturated in aragonite by the year 2100. We examined the post-mortem dissolution rates of aragonitic and calcitic shells from four species of Antarctic benthic marine invertebrates (two bivalves, one limpet, one brachiopod) and the thallus of a limpet shell-encrusting coralline alga exposed to acidified pH (7.4) or non-acidified pH (8.2) seawater at a constant temperature of 4°C. Within a period of only 14–35 days, shells of all four species held in pH 7.4 seawater had suffered significant dissolution. Despite calcite being 35% less soluble in seawater than aragonite, there was surprisingly, no consistent pattern of calcitic shells having slower dissolution rates than aragonitic shells. Outer surfaces of shells held in pH 7.4 seawater exhibited deterioration by day 35, and by day 56 there was exposure of aragonitic or calcitic prisms within the shell architecture of three of the macroinvertebrate species. Dissolution of coralline algae was confirmed by differences in weight loss in limpet shells with and without coralline algae. By day 56, thalli of the coralline alga held in pH 7.4 displayed a loss of definition of the conceptacle pores and cracking was evident at the zone of interface with limpet shells. Experimental studies are needed to evaluate whether there are adequate compensatory mechanisms in these and other calcified Antarctic benthic macroorganisms to cope with anticipated ocean acidification. In their absence, these organisms, and the communities they comprise, are likely to be among the first to experience the cascading impacts of ocean acidification.

LACK OF DEFENSE OR PHLOROTANNIN INDUCTION BY UV RADIATION OR MESOGRAZERS IN DESMARESTIA ANCEPS AND D. MENZIESII (PHAEOPHYCEAE)1

Phlorotannins are polyphenoloic metabolites occurring only in the Phaeophyceae that have numerous putative primary roles (e.g. cell‐wall construction and storage) as well as secondary metabolic roles, which include herbivore feeding deterrence and protection from UV radiation. The proposed role of phlorotannins in the defense against UV radiation is of particular importance in the Antarctic due to depletion of the stratospheric ozone layer in that area. Several studies of brown algae have found evidence of an induction response (the production of defensive metabolites, including phlorotannins) after grazing by various mesograzers, after simulated grazing/wounding, and after exposure to increases in UV radiation. This study aimed to determine if phlorotannin production or other defenses in two dominant, endemic Antarctic species (Desmarestia menziesii Montagne and Desmarestia anceps J. Agardh) could be induced by an increase in exposure to UV radiation or by natural and artificial grazing. An in situ experiment failed to detect any effect of UV radiation on phlorotannin concentrations in either species or on subsequent palatability in feeding bioassays. A laboratory‐based experiment did not detect any effect of mesoherbivore grazing or simulated grazing (wounding) on palatability or the concentration of phlorotannins in D. menziesii. Instead, phlorotannin concentrations increased in all treatments in both experiments, consistent with an increase in overall resource availability due to an increase in available PAR compared with the in situ irradiance at the algal collection sites.

Filamentous algal endophytes in macrophytic Antarctic algae: prevalence in hosts and palatability to mesoherbivores

Amsler C.D., Amsler M.O., McClintock J.B. and Baker B.J. 2009. Filamentous algal endophytes in macrophytic Antarctic algae: prevalence in hosts and palatability to mesoherbivores. Phycologia 48: 324–334. DOI: 10.2216/08-79.1. Five individuals, each from 13 common species of large macroalgae (‘macrophytes’) from the western Antarctic Peninsula, were surveyed for the presence of filamentous algal endophytes both macroscopically and microscopically using dissecting and compound microscopes. Of the 13 species surveyed, endophytes were either rare or absent in five. The remaining species all supported endophytes in most or usually all individuals with maximum endophyte densities per species ranging from 3% to 75% of the thallus area. Thallus fragments from all individuals with endophytes were placed into culture, and 99 unialgal, filamentous brown algal strains were isolated. The ITS1 gene was sequenced in each strain to sort these into distinct genotypes. Brown algal endophytes grew well in culture, and 10 distinct filamentous genotypes were present. The green endophytes did not grow well in culture, and only two green algal species present in the thallus fragments were isolated. No-choice feeding rate bioassays were performed with thallus fragments of all 13 macrophyte species and with cultures of seven filamentous brown endophytes and both green endophytes. Feeding rates on the endophytes were 2–3 orders of magnitude higher than rates on 12 of the macrophyte species and 2- to 6-fold higher than on the only truly palatable macrophyte, Palmaria decipiens. These data support the hypothesis that Antarctic macrophytes are commonly endophytized and that the endophytes benefit from the association by being protected, at least in part, from amphipod herbivory.

The Mg-Calcite Composition of Antarctic Echinoderms: Important Implications for Predicting the Impacts of Ocean Acidification

The Southern Ocean is considered to be the canary in the coal mine with respect to the first effects of ocean acidification (OA). This vulnerability is due to naturally low carbonate ion concentrations that result from the effect of low temperature on acid-base dissociation coefficients, from the high solubility of CO2 at low temperature, and from ocean mixing. Consequently, the two calcium carbonate polymorphs, aragonite and calcite, are expected to become undersaturated in the Southern Ocean within 50 and 100 years, respectively. Marine invertebrates such as echinoderms, whose skeletons are classified as high-magnesium carbonate (>4% mol MgCO3), are even more vulnerable to OA than organisms whose skeletons consist primarily of aragonite or calcite, with respect to both increased susceptibility to skeletal dissolution and further challenge to their production of skeletal elements. Currently, despite their critical importance to predicting the effects of OA, there is almost no information on the Mg-calcite composition of Antarctic echinoderms, a group known to be a major contributor to the global marine carbon cycle. Here we report the Mg-calcite compositions of 26 species of Antarctic echinoderms, representing four classes. As seen in tropical and temperate echinoderms, Mg-calcite levels varied with taxonomic class, with sea stars generally having the highest levels. When combined with published data for echinoderms from primarily temperate and tropical latitudes, our findings support the hypothesis that Mg-calcite level varies inversely with latitude. Sea stars and brittle stars, key players in Antarctic benthic communities, are likely to be the first echinoderms to be challenged by near-term OA.

Chemical defenses against diatom fouling in Antarctic marine sponges

Antarctic sponges are commonly fouled by diatoms, sometimes so heavily as to occlude pores employed in filter feeding and respiration. This fouling becomes heavier during the annual summer microalgal bloom. Polar and non‐polar extracts of eight species of marine sponges from McMurdo Sound, Antarctica were assayed for cytotoxicity against sympatric fouling diatoms. To identify compounds potentially released by sponges as defenses against diatom biofouling, only fractions of crude extracts that were soluble in seawater or 2% methanol in seawater were assayed. Significant bioactivity was present in seven of the eight species. Both Mycale acerata and Homaxinella balfourensis displayed moderate levels of defense against diatoms even though they are not or are only weakly chemically defended against bacteria and predators. Calyx acuarius extracts, which do have antipredator and antibacterial effects, had no effect on diatoms except at levels many fold higher than present in the intact animal. These results strongly suggest some level of specificity for chemical defenses against diatom fouling in antarctic sponges.

Tissue-specific palatability and chemical defenses against macropredators and pathogens in the common articulate brachiopod Liothyrella uva from the Antarctic Peninsula

The punctate terebratulid brachiopod Liothyrella uva is the most common brachiopod species in Antarctica. Whole brachiopods, either live or freeze dried and ground into a powder and suspended in alginate, were unpalatable to the sympatric macropredators Odontaster validus (an abundant, omnivorous sea star) and Notothenia coriiceps (an abundant, omnivorous, epibenthic fish). The unpalatability of these ground tissues coupled with that of lipophilic extracts of whole L. uva presented in alginate pellets to O. validus, suggests an involvement of chemical defenses. Several isolated brachiopod tissues were also unpalatable to O. validus after being freeze dried, ground and suspended in alginate, but only the pedicle was unpalatable in such preparations to both O. validus and N. coriiceps. This observation is consistent with the Optimal Defense Theory since the pedicle is the only tissue not protected inside the brachiopod shell. There was, however, no correlation between the energetic content and unpalatability of any of the individual tissues. Organic extracts of tissues involved in feeding (lophophore and intestine–stomach) had relatively strong antimicrobial activity when assayed against several strains of Antarctic bacteria. However, the lophophore was palatable to both macropredators, suggesting nonoverlapping chemical defenses are involved in protection against predators and pathogens.

Seaweeds and Their Communities in Polar Regions

Polar seaweeds typically begin to grow in late winter–spring, around the time of sea-ice breakup. They can grow under very low light enabling distributions to depths of 40 m. Moreover, they are physiologically adapted to low temperatures. Intertidal species exhibit a remarkable stress tolerance against freezing, desiccation, and salinity changes. Endemism is much greater in the Antarctic compared to the Arctic species. On rocky shores of the Antarctic Peninsula and of Spitsbergen >80% of the bottom can be covered by seaweeds with standing biomass levels 20 kg wet wt m2. Species richness and biomass declines, however, toward higher latitudes. Seaweeds are the dominant organisms in coastal waters and thus play important roles in benthic food webs and are likely to be of particular importance to benthic detrital food chains. Chemical defenses against herbivores are common in Antarctic, but not in Arctic seaweeds. More research is needed especially to study the effects of global climate changes.