Monitoring and modelling marine zooplankton in a changing climate.

Zooplankton are major consumers of phytoplankton primary production in marine ecosystems. As such, they represent a critical link for energy and matter transfer between phytoplankton and bacterioplankton to higher trophic levels and play an important role in global biogeochemical cycles. In this Review, we discuss key responses of zooplankton to ocean warming, including shifts in phenology, range, and body size, and assess the implications to the biological carbon pump and interactions with higher trophic levels. Our synthesis highlights key knowledge gaps and geographic gaps in monitoring coverage that need to be urgently addressed. We also discuss an integrated sampling approach that combines traditional and novel techniques to improve zooplankton observation for the benefit of monitoring zooplankton populations and modelling future scenarios under global changes.

A database of zooplankton biomass in Australian marine waters.

Zooplankton biomass data have been collected in Australian waters since the 1930s, yet most datasets have been unavailable to the research community. We have searched archives, scanned the primary and grey literature, and contacted researchers, to collate 49187 records of marine zooplankton biomass from waters around Australia (0-60°S, 110-160°E). Many of these datasets are relatively small, but when combined, they provide >85 years of zooplankton biomass data for Australian waters from 1932 to the present. Data have been standardised and all available metadata included. We have lodged this dataset with the Australian Ocean Data Network, allowing full public access. The Australian Zooplankton Biomass Database will be valuable for global change studies, research assessing trophic linkages, and for initialising and assessing biogeochemical and ecosystem models of lower trophic levels.

Trophodynamics of Southern Ocean pteropods on the southern Kerguelen Plateau.

Pteropods are a group of small marine gastropods that are highly sensitive to multiple stressors associated with climate change. Their trophic ecology is not well studied, with most research having focused primarily on the effects of ocean acidification on their fragile, aragonite shells. Stable isotopes analysis coupled with isotope-based Bayesian niche metrics is useful for characterizing the trophic structure of biological assemblages. These approaches have not been implemented for pteropod assemblages. We used isotope-based Bayesian niche metrics to investigate the trophic relationships of three co-occurring pteropod species, with distinct feeding behaviors, sampled from the Southern Kerguelen Plateau area in the Indian Sector of the Southern Ocean-a biologically and economically important but poorly studied region. Two of these species were gymnosomes (shell-less pteropods), which are traditionally regarded as specialist predators on other pteropods, and the third species was a thecosome (shelled pteropod), which are typically generalist omnivores. For each species, we aimed to understand (a) variability and overlap among isotopic niches; and (b) whether there was a relationship between body size and trophic position. Observed isotopic niche areas were broadest for gymnosomes, especially Clione limacina antarctica, whose observed isotopic niche area was wider than expected on both δ13C and δ15N value axes. We also found that trophic position significantly increased with increasing body length for Spongiobranchaea australis. We found no indication of a dietary shift toward increased trophic position with increasing body size for Clio pyramidata f. sulcata. Trophic positions ranged from 2.8 to 3.5, revealing an assemblage composed of both primary and secondary consumer behaviors. This study provides a comprehensive comparative analysis on trophodynamics in Southern Ocean pteropod species, and supports previous studies using gut content, fatty acid and stable isotope analyses. Combined, our results illustrate differences in intraspecific trophic behavior that may be attributed to differential feeding strategies at species level.

Can lipid removal affect interpretation of resource partitioning from stable isotopes in Southern Ocean pteropods?

RATIONALE: Stable isotope analysis (SIA) is a powerful tool to estimate dietary links between polar zooplankton. However, the presence of highly variable 12 C-rich lipids may skew estimations as they are depleted in 13 C relative to proteins and carbohydrates, consequently masking carbon signals from food sources. Lipid effects on pteropod-specific values requires examining, since accounting for lipids is rarely conducted among the few existing pteropod-related SIA studies. It is currently unclear whether lipid correction is necessary prior to SIA of pteropods. METHODS: Whole bodies of three species of pteropods (Clio pyramidata f. sulcata, Clione limacina antarctica, and Spongiobranchaea australis) sampled from the Southern Ocean were lipid-extracted chemically to test the effects on δ13 C and δ15 N values (n = 38 individuals in total). We determined the average change in δ13 C values for each treatment, and compared this offset with those from published normalization models. We tested lipid correction effects on isotopic niche dispersion metrics to compare interpretations surrounding food web dynamics. RESULTS: Pteropods with lipids removed had δ13 C values up to 4.5‰ higher than bulk samples. However, lipid extraction also produced higher δ15 N values than bulk samples. Isotopic niche overlaps between untreated pteropods and their potential food sources were significantly different from overlaps generated between lipid-corrected pteropods and their potential food sources. Data converted using several published normalization models did not reveal significant differences among various calculated niche metrics, including standard ellipse and total area. CONCLUSIONS: We recommend accounting for lipids via chemical extraction or mathematical normalization before applying SIA to calculate ecological niche metrics, particularly for organisms with moderate to high lipid content such as polar pteropods. Failure to account for lipids may result in misinterpretations of niche dimensions and overlap and, consequently, trophic interactions.

A database of marine larval fish assemblages in Australian temperate and subtropical waters.

Larval fishes are a useful metric of marine ecosystem state and change, as well as species-specific patterns in phenology. The high level of taxonomic expertise required to identify larval fishes to species level, and the considerable effort required to collect samples, make these data very valuable. Here we collate 3178 samples of larval fish assemblages, from 12 research projects from 1983-present, from temperate and subtropical Australian pelagic waters. This forms a benchmark for the larval fish assemblage for the region, and includes recent monitoring of larval fishes at coastal oceanographic reference stations. Comparing larval fishes among projects can be problematic due to differences in taxonomic resolution, and identifying all taxa to species is challenging, so this study reports a standard taxonomic resolution (of 218 taxa) for this region to help guide future research. This larval fish database serves as a data repository for surveys of larval fish assemblages in the region, and can contribute to analysis of climate-driven changes in the location and timing of the spawning of marine fishes.

A database of chlorophyll a in Australian waters.

Chlorophyll a is the most commonly used indicator of phytoplankton biomass in the marine environment. It is relatively simple and cost effective to measure when compared to phytoplankton abundance and is thus routinely included in many surveys. Here we collate 173, 333 records of chlorophyll a collected since 1965 from Australian waters gathered from researchers on regular coastal monitoring surveys and ocean voyages into a single repository. This dataset includes the chlorophyll a values as measured from samples analysed using spectrophotometry, fluorometry and high performance liquid chromatography (HPLC). The Australian Chlorophyll a database is freely available through the Australian Ocean Data Network portal (https://portal.aodn.org.au/). These data can be used in isolation as an index of phytoplankton biomass or in combination with other data to provide insight into water quality, ecosystem state, and relationships with other trophic levels such as zooplankton or fish.

Widely used marine seismic survey air gun operations negatively impact zooplankton.

Zooplankton underpin the health and productivity of global marine ecosystems. Here we present evidence that suggests seismic surveys cause significant mortality to zooplankton populations. Seismic surveys are used extensively to explore for petroleum resources using intense, low-frequency, acoustic impulse signals. Experimental air gun signal exposure decreased zooplankton abundance when compared with controls, as measured by sonar (~3-4 dB drop within 15-30 min) and net tows (median 64% decrease within 1 h), and caused a two- to threefold increase in dead adult and larval zooplankton. Impacts were observed out to the maximum 1.2 km range sampled, which was more than two orders of magnitude greater than the previously assumed impact range of 10 m. Although no adult krill were present, all larval krill were killed after air gun passage. There is a significant and unacknowledged potential for ocean ecosystem function and productivity to be negatively impacted by present seismic technology.

Effect of marker choice and thermal cycling protocol on zooplankton DNA metabarcoding studies.

DNA metabarcoding is a promising approach for rapidly surveying biodiversity and is likely to become an important tool for measuring ecosystem responses to environmental change. Metabarcoding markers need sufficient taxonomic coverage to detect groups of interest, sufficient sequence divergence to resolve species, and will ideally indicate relative abundance of taxa present. We characterized zooplankton assemblages with three different metabarcoding markers (nuclear 18S rDNA, mitochondrial COI, and mitochondrial 16S rDNA) to compare their performance in terms of taxonomic coverage, taxonomic resolution, and correspondence between morphology- and DNA-based identification. COI amplicons sequenced on separate runs showed that operational taxonomic units representing >0.1% of reads per sample were highly reproducible, although slightly more taxa were detected using a lower annealing temperature. Mitochondrial COI and nuclear 18S showed similar taxonomic coverage across zooplankton phyla. However, mitochondrial COI resolved up to threefold more taxa to species compared to 18S. All markers revealed similar patterns of beta-diversity, although different taxa were identified as the greatest contributors to these patterns for 18S. For calanoid copepod families, all markers displayed a positive relationship between biomass and sequence reads, although the relationship was typically strongest for 18S. The use of COI for metabarcoding has been questioned due to lack of conserved primer-binding sites. However, our results show the taxonomic coverage and resolution provided by degenerate COI primers, combined with a comparatively well-developed reference sequence database, make them valuable metabarcoding markers for biodiversity assessment.

A database of marine phytoplankton abundance, biomass and species composition in Australian waters.

There have been many individual phytoplankton datasets collected across Australia since the mid 1900s, but most are unavailable to the research community. We have searched archives, contacted researchers, and scanned the primary and grey literature to collate 3,621,847 records of marine phytoplankton species from Australian waters from 1844 to the present. Many of these are small datasets collected for local questions, but combined they provide over 170 years of data on phytoplankton communities in Australian waters. Units and taxonomy have been standardised, obviously erroneous data removed, and all metadata included. We have lodged this dataset with the Australian Ocean Data Network (http://portal.aodn.org.au/) allowing public access. The Australian Phytoplankton Database will be invaluable for global change studies, as it allows analysis of ecological indicators of climate change and eutrophication (e.g., changes in distribution; diatom:dinoflagellate ratios). In addition, the standardised conversion of abundance records to biomass provides modellers with quantifiable data to initialise and validate ecosystem models of lower marine trophic levels.

Climate change and Southern Ocean ecosystems I: how changes in physical habitats directly affect marine biota.

Antarctic and Southern Ocean (ASO) marine ecosystems have been changing for at least the last 30 years, including in response to increasing ocean temperatures and changes in the extent and seasonality of sea ice; the magnitude and direction of these changes differ between regions around Antarctica that could see populations of the same species changing differently in different regions. This article reviews current and expected changes in ASO physical habitats in response to climate change. It then reviews how these changes may impact the autecology of marine biota of this polar region: microbes, zooplankton, salps, Antarctic krill, fish, cephalopods, marine mammals, seabirds, and benthos. The general prognosis for ASO marine habitats is for an overall warming and freshening, strengthening of westerly winds, with a potential pole-ward movement of those winds and the frontal systems, and an increase in ocean eddy activity. Many habitat parameters will have regionally specific changes, particularly relating to sea ice characteristics and seasonal dynamics. Lower trophic levels are expected to move south as the ocean conditions in which they are currently found move pole-ward. For Antarctic krill and finfish, the latitudinal breadth of their range will depend on their tolerance of warming oceans and changes to productivity. Ocean acidification is a concern not only for calcifying organisms but also for crustaceans such as Antarctic krill; it is also likely to be the most important change in benthic habitats over the coming century. For marine mammals and birds, the expected changes primarily relate to their flexibility in moving to alternative locations for food and the energetic cost of longer or more complex foraging trips for those that are bound to breeding colonies. Few species are sufficiently well studied to make comprehensive species-specific vulnerability assessments possible. Priorities for future work are discussed.

Long term trends of Hg uptake in resident fish from a polluted estuary.

Mercury contamination of fish is dependent upon a system's ability to transform inorganic Hg into biologically available forms; however, fish biometrics also play an important role. To assess long term trends in Hg concentrations in sand flathead (Platycephalus bassensis) a polynomial model, corrected for fish length, was used to evaluate temporal trends and spatial variability, while growth rates were estimated using the Von Bertalanffy length-at-age model. Hg concentrations showed no decrease over time, and generally remained near recommended consumption levels (0.5 mg kg(-1)). Previously reported spatial differences in Hg concentrations were not supported by the data once the models were corrected for fish length. Growth rate variation accounted for a large part of the previously published spatial differences. These results suggest that inclusion of fish biometrics is necessary to facilitate an accurate interpretation of spatial and temporal trends of contaminant concentrations in long term estuarine and marine monitoring programs.

Crustacea in Arctic and Antarctic sea ice: distribution, diet and life history strategies.

This review concerns crustaceans that associate with sea ice. Particular emphasis is placed on comparing and contrasting the Arctic and Antarctic sea ice habitats, and the subsequent influence of these environments on the life history strategies of the crustacean fauna. Sea ice is the dominant feature of both polar marine ecosystems, playing a central role in physical processes and providing an essential habitat for organisms ranging in size from viruses to whales. Similarities between the Arctic and Antarctic marine ecosystems include variable cover of sea ice over an annual cycle, a light regimen that can extend from months of total darkness to months of continuous light and a pronounced seasonality in primary production. Although there are many similarities, there are also major differences between the two regions: The Antarctic experiences greater seasonal change in its sea ice extent, much of the ice is over very deep water and more than 80% breaks out each year. In contrast, Arctic sea ice often covers comparatively shallow water, doubles in its extent on an annual cycle and the ice may persist for several decades. Crustaceans, particularly copepods and amphipods, are abundant in the sea ice zone at both poles, either living within the brine channel system of the ice-crystal matrix or inhabiting the ice-water interface. Many species associate with ice for only a part of their life cycle, while others appear entirely dependent upon it for reproduction and development. Although similarities exist between the two faunas, many differences are emerging. Most notable are the much higher abundance and biomass of Antarctic copepods, the dominance of the Antarctic sea ice copepod fauna by calanoids, the high euphausiid biomass in Southern Ocean waters and the lack of any species that appear fully dependent on the ice. In the Arctic, the ice-associated fauna is dominated by amphipods. Calanoid copepods are not tightly associated with the ice, while harpacticoids and cyclopoids are abundant. Euphausiids are nearly absent from the high Arctic. Life history strategies are variable, although reproductive cycles and life spans are generally longer than those for temperate congeners. Species at both poles tend to be opportunistic feeders and periods of diapause or other reductions in metabolic expenditure are not uncommon.