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Every spring for the past two decades, depletion of stratospheric ozone has caused increases in ultraviolet B radiation (UVB, 280–320 nm) reaching Antarctic terrestrial and aquatic habitats. Research efforts to evaluate the impact of this phenomenon have focused on phytoplankton under the assumption that ecosystem effects will most likely originate through reductions in primary productivity; however, phytoplankton do not represent the only significant component in ecosystem response to elevated UVB. Antarctic bacterioplankton are adversely affected by UVB exposure; and invertebrates and fish, particularly early developmental stages that reside in the plankton, are sensitive to UVB. There is little information available on UV responses of larger Antarctic marine animals (e.g., birds, seals and whales). Understanding the balance between direct biological damage and species-specific potentials for UV tolerance (protection and recovery) relative to trophic dynamics and biogeochemical cycling is a crucial factor in evaluating the overall impact of ozone depletion. After more than a decade of research, much information has been gathered about UV-photobiology in Antarctica; however, a definitive quantitative assessment of the effect of ozone depletion on the Antarctic ecosystem still eludes us. It is only obvious that ozone depletion has not had a catastrophic effect in the Antarctic region. The long-term consequences of possible subtle shifts in species composition and trophic interactions are still uncertain.
Secondary metabolites are widespread among lower phyla and understanding their functional role(s) in the producing organism has been under study in recent decades. Considerable progress has been made in understanding chemical ecological interactions among terrestrial organisms, and similar research in the marine realm has been initiated in recent years. Polar regions are more difficult to access and thus progress has been slower. Nevertheless, the extreme and often unique marine environments surrounding Antarctica as well as the many unusual trophic interactions in antarctic marine communities might well be expected to select for novel secondary metabolites and/or novel functional roles for secondary metabolites. Indeed, recent studies have documented novel, chemically-mediated interactions between molluscs and amphipods, between algae, urchins and anemones, and between sponges and their predators. The Porifera are the dominant phylum on the McMurdo Sound benthos, and representatives of this phylum have been shown to elaborate sea star feeding deterrents, inhibitors of fouling or infectious organisms, and metabolites which mediate predation via molt inhibition. As a result of studies on Antarctic sponges, new insights into functional roles of pigments and the ability of sponges to sequester metabolites have been gained, and a new mechanism of chemical defense has been described. Herein we describe recent results of our studies of trophic interactions between sponges and their predators that are mediated by specific sponge secondary metabolites. Moreover, we highlight unusual chemically-mediated interactions in antarctic marine invertebrates other than sponges.
Marine benthic communities living in shallow-water habitats (<100 m depth) in Antarctica possess characteristics reminiscent of Paleozoic marine communities and modern deep-sea communities. The absence of crabs and sharks, the limited diversity of teleosts and skates, the dominance of slow-moving invertebrates at higher trophic levels, and the occurrence of dense ophiuroid and crinoid populations indicate that skeleton-breaking predation is limited in Antarctica today, as it was worldwide during the Paleozoic and as it is in the deep sea today. The community structure of the antarctic benthos has its evolutionary roots in the Eocene. Data from fossil assemblages at Seymour Island, Antarctic Peninsula suggest that shallow-water communities were similar to communities at lower latitudes until they were affected by global cooling, which accelerated in the late Eocene to early Oligocene. That long-term cooling trend ultimately resulted in the polar climate and peculiar community structure found in Antarctica today. Declining temperatures beginning late in the Eocene are associated with the disappearance of crabs, sharks, and most teleosts. The sudden drop in predation pressure allowed dense ophiuroid and crinoid populations to appear and flourish. These late Eocene echinoderm populations exhibit low frequencies of sublethal damage (regenerating arms), demonstrating that there was little or no predation from skeleton-breaking fish and decapods. Current scenarios of global climate change include predictions of increased upwelling and consequent cooling in temperate and subtropical upwelling zones. Limited ecological evidence suggests that such cooling could disrupt trophic relationships and favor retrograde community structures in those local areas.
A major objective of the multidisciplinary Palmer Long Term Ecological Research (LTER) program is to obtain a comprehensive understanding of various components of the Antarctic marine ecosystem—the assemblage of plants, animals, ocean, sea ice, and island components south of the Antarctic Convergence. Phytoplankton production plays a key role in this polar ecosystem, and factors that regulate production include those that control cell growth (light, temperature, nutrients) and those that control cell accumulation rate and hence population growth (water column stability, advection, grazing, and sinking). Several of these factors are mediated by the annual advance and retreat of sea ice. In this study, we examine the results from nearly a decade (1991–2000) of ecological research in the western Antarctic Peninsula region. We evaluate the spatial and temporal variability of phytoplankton biomass (estimated as chlorophyll-a concentration) and primary production (determined in-situ aboard ship as well as estimated from ocean color satellite data). We also present the spatial and temporal variability of sea ice extent (estimated from passive microwave satellite data). While the data record is relatively short from a long-term perspective, evidence is accumulating that statistically links the variability in sea ice to the variability in primary production. Even though this marine ecosystem displays extreme interannual variability in both phytoplankton biomass and primary production, persistent spatial patterns have been observed over the many years of study (e.g., an on to offshore gradient in biomass and a growing season characterized by episodic phytoplankton blooms). This high interannual variability at the base of the food chain influences organisms at all trophic levels.
The seasonally ice-covered regions of the Southern Ocean have distinctive ecological systems due to the growth of microalgae in sea ice. Although sea ice microalgal production is exceeded by phytoplankton production on an annual basis in most offshore regions of the Southern Ocean, blooms of sea ice algae differ considerably from the phytoplankton in terms of timing and distribution. Thus sea ice algae provide food resources for higher trophic level organisms in seasons and regions where water column biological production is low or negligible. A flux of biogenic material from sea ice to the water column and benthos follows ice melt, and some of the algal species are known to occur in ensuing phytoplankton blooms. A review of algal species in pack ice and offshore plankton showed that dominance is common for three species: Phaeocystis antarctica, Fragilariopsis cylindrus and Fragilariopsis curta. The degree to which dominance by these species is a product of successional processes in sea ice communities could be an important in determining their biogeochemical contribution to the Southern Ocean and their ability to seed blooms in marginal ice zones.
“Recruitment potential” in Antarctic krill in the Palmer Long-Term Ecological Research (LTER) study region west of the Antarctic Peninsula varied significantly over the 7-yr time series between January 1993 and January 1999. Timing of ovarian maturation, the percent of the population reproducing, and individual reproductive output (batch volume, embryo diameter) were measured. Indices have been developed to quantify the timing and intensity of reproduction in Antarctic krill. One finding important to estimates of population fecundity for this long-lived species is that the percent of the population reproducing can vary widely, from 10 to 98%. Each season was characterized as having delayed, average or advanced ovarian development. In this study we relate these indices to direct and indirect indicators of spring or annual food availability. The timing of the spring sea ice retreat and the extent of sea ice in the spring (September through November) appear to significantly affect the intensity and timing of reproduction in the population. Intensity of reproduction was highest under “average” conditions, and oöcyte development fastest with conditions of a late retreat and high spring sea ice extent.
The only apex predators that live year-round at high latitudes of the Ross Sea are the Weddell seal and emperor penguin. The seasonal distribution, foraging depths, and diet of these two species appear to overlap. What makes it possible for emperor penguins and Weddell seals to co-exist at high latitude throughout the winter when other marine tetrapods apparently cannot? Both species have similar adaptations for exploitation of the deep-water habitat, forage on the same species, and routinely make long and deep dives. Yet, despite these similarities, there is probably little trophic overlap between the adults of both species due to geographical and seasonal differences in habitat use. For example, during the winter months while female emperor penguins are ranging widely in the pack ice, adult seals are foraging and fattening for the upcoming summer fast, literally beneath the feet of the male penguins. However, there is more extensive overlap between juvenile seals and adult penguins, and shifts in prey abundance and/or distribution would likely affect these two groups similarly. In contrast, juvenile penguins appear to avoid inter- and intra- specific competition by leaving the Ross Sea once they molt.
Measurements of δ13C, δ15N, and C/N for a variety of Antarctic peninsula fauna and flora were used to quantify the importance of benthic brown algae to resident organisms and determine food web relationships among this diverse littoral fauna. δ13C values ranged from−16.8‰ for benthic algal herbivores (limpets) to −29.8‰ for the krill, Euphausia superba; the average pooled value for brown macroalgae, including their attached filamentous diatoms, was−20.6‰. There was no correlation between biomass δ13C or δ15N with C/N content, and consequently both δ13C and δ15N values were useful in evaluating trophic relationships. δ15N values of the fauna ranged from 3.1 to 12.5‰, with lowest values recorded in suspension feeders (e.g., bryozoans) and highest values in Adelie penguins (12.5‰) collected in 1989. The comparatively lower δ15N value for a Chinstrap penguin (6.9‰) collected in 1997 is attributed to the different dietary food sources consumed by these species as reflected in their respective δ13C values. Significant amounts of benthic macroalgal carbon is incorporated into the tissues of invertebrates and fishes that occupy up to four trophic levels. For many benthic and epibenthic species, including various crustaceans and molluscs, assimilation of benthic algal carbon through detrital pathways ranges from 30 to 100%. Consequently, the trophic importance of benthic brown algae may well extend to many pelagic organisms that are key prey species for birds, fishes, and marine mammals. These data support the hypothesis that benthic seaweeeds, together with their associated epiphytic diatoms, provide an important carbon source that is readily incorporated into Antarctic peninsula food webs.
Unlike temperate fishes, Antarctic fishes of the notothenioid suborder, whose body temperatures (−2 to 1°C) conform to the Southern Ocean, must express their genomes in an extremely cold thermal regime. To determine whether these fishes have evolved compensatory adjustments that maintain efficient gene transcription at low temperatures, we have initiated studies of the cis-acting regulatory elements that control globin gene expression in the Antarctic rockcod Notothenia coriiceps and in its close relative, the temperate New Zealand black cod N. angustata (habitat temperature = 6 to 15°C). The genes encoding the major α1 and β globins of these fishes are tightly linked in head-to-head (5′ to 5′) orientation. The intergenic regions separating the globin genes in the two fishes, ∼4.3 kb in N. coriiceps and ∼3.2 kb in N. angustata, are highly similar in sequence, the major difference being the absence of a 1.1-kb, repeat-containing segment in the latter. To assess the promoter and enhancer activities of the intergenic regions, each was cloned into the luciferase-reporter vector pGL3-Basic, and the constructs were transfected into MEL cells. Upon DMSO induction of MEL cell differentiation, each of the α/β-intergenic regions functioned in both orientations as erythroid-responsive transcriptional regulators. However, expression of luciferase mediated by the N. coriiceps intergene was 6-fold greater in the α orientation than that for the N. angustata intergene and 2-fold greater for the β. The greater transcription-stimulating activity of the N. coriiceps intergene can be attributed to two enhancers composed of combinations of CAC/Sp1 and GATA motifs and located in direct repeat elements. N. angustata, which lacked repetitive structure in its intergene, contained a single copy of the enhancer. We propose that cold adaptation of globin gene expression in N. coriiceps evolved in part through duplication and refinement of critical cis-acting regulatory elements as the Southern Ocean cooled during the past 25 million years.
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