Whales in the carbon cycle: can recovery remove carbon dioxide?

The great whales (baleen and sperm whales), through their massive size and wide distribution, influence ecosystem and carbon dynamics. Whales directly store carbon in their biomass and contribute to carbon export through sinking carcasses. Whale excreta may stimulate phytoplankton growth and capture atmospheric CO2; such indirect pathways represent the greatest potential for whale-carbon sequestration but are poorly understood. We quantify the carbon values of whales while recognizing the numerous ecosystem, cultural, and moral motivations to protect them. We also propose a framework to quantify the economic value of whale carbon as populations change over time. Finally, we suggest research to address key unknowns (e.g., bioavailability of whale-derived nutrients to phytoplankton, species- and region-specific variability in whale carbon contributions).

Understanding impacts of organic contaminants from aquaculture on the marine environment using a chemical fate model.

As demand for sustainable marine aquaculture (mariculture) and marine food supply surges worldwide, there is a growing need for new tools to assess mariculture impacts on local ecosystems, including the cycling of toxic organic contaminants. With this in mind, we developed the Contaminant Fate in Aquaculture-Modified Ecosystems (CFAME) model. The current model was designed to explore the fate of mariculture-derived organic contaminants in the Marlborough Sounds, New Zealand, known for its Chinook salmon farming industry. Model evaluation indicated robust model design, with 80% of modeled concentrations falling within a factor of ten of measured ones for native biota. Model results showed that mariculture was a source of organic contaminants in the sediment even at the Marlborough Sounds regional level and in wild marine fishes with high trophic levels near the farm area. Future research attention should be directed toward measuring chemicals with low log KAW (<0) and high log KOW values (e.g., >3) in sediment, and chemicals with log KOW values of 3-9 in wild fish.

Experimentally derived biochemical modelling parameters to improve understanding of aquaculture's effect on marine food webs.

To construct robust biogeochemical models for application to marine-based aquaculture settings, careful selection of appropriate model parameters is necessary. This study used an experimental approach to establish biomarkers of farm and marine-derived organic matter, and to derive isotopic turnover rates, and trophic discrimination factors specific to aquaculture associated food webs. A shift towards a farm-derived resource base resulted in consumer tissues more depleted in the carbon-13 isotope (indicated by more negative δ13C values) and a higher proportion of oleic acid, linoleic acid, and alpha-linoleic acid in the fatty acid profile of consumers over time. Measured trophic discrimination factors between dietary sources and consumer tissues demonstrated high variability among species and tissue types, ranging from -0.25‰ to 0.82‰ for Δ13C and from -0.77‰ to 6.8‰ for Δ15N. Stable isotope half-lives were also diverse among species and tissue types, ranging from <7 days to 462 days. Results demonstrated that construction of robust models for tracing assimilation of farm-derived organic matter through marine food webs requires the use of taxa and tissue specific parameters. Turnover rates have applications for understanding assimilative capacity of communities and for managing populations within the ecological footprint of farms.

Organic contaminants in imported salmon feed and their effects on reef ecosystems in New Zealand.

Organic matter from salmon farms has been shown to be assimilated by soft sediment and rocky reef communities within the ecological footprint of salmon farms. Given these findings, another question arises - What other chemicals in salmon feed may be assimilated into wild communities via organic waste from salmon farms? Here we measured a suite of organic contaminants in salmon feed, in organisms used in a controlled feeding experiment, and in reef species collected within the depositional footprint of salmon farms. Gas Chromatography-Tandem Mass Spectrometry was used to quantify trace concentrations of polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and current-use (CPUs) and historic-use pesticides (HUPs) in salmon feed imported to New Zealand. The effect of assimilation of farm-derived organic matter on contaminant profiles differed among species during the controlled feeding experiment and demonstrated that migration of individuals to a farm-associated site has the potential to increase or decrease organic contaminant concentrations. Concentrations of PCBs in Parapercis colias (blue cod), a highly resident, long-lived fish, were significantly higher at farm sites than at reference sites. While these concentrations were relatively low in a global context, this result presents blue cod as an important candidate for future monitoring of organic contaminants around point sources. PCBs and PBDEs measured in wild marine species were all below limits set by the European Union, whereas concentrations of certain HUPs, specifically dichlorodiphenyltrichloroethane (DDT) and its degradation products and endosulfan, may be of concern as a consequence of alternative anthropogenic activities. Overall, feed imported to New Zealand had relatively low levels of most organic contaminants that, at current levels, are unlikely to result in significant ecological effects to wild communities in adjacent habitats.

Changes in microbial community phylogeny and metabolic activity along the water column uncouple at near sediment aphotic layers in fjords.

Fjords are semi-enclosed marine systems with unique physical conditions that influence microbial community composition and structure. Pronounced organic matter and physical condition gradients within fjords provide a natural laboratory for the study of changes in microbial community structure and metabolic potential in response to environmental conditions. Photosynthetic production in euphotic zones sustains deeper aphotic microbial activity via organic matter sinking, augmented by large terrestrial inputs. Previous studies do not consider both prokaryotic and eukaryotic communities when linking metabolic potential and activity, community composition, and environmental gradients. To address this gap we profiled microbial functional potential (Biolog Ecoplates), bacterial abundance, heterotrophic production (3H-Leucine incorporation), and prokaryotic/eukaryotic community composition (16S and 18S rRNA amplicon gene sequencing). Similar factors shaped metabolic potential, activity and community (prokaryotic and eukaryotic) composition across surface/near surface sites. However, increased metabolic diversity at near bottom (aphotic) sites reflected an organic matter influence from sediments. Photosynthetically produced particulate organic matter shaped the upper water column community composition and metabolic potential. In contrast, microbial activity at deeper aphotic waters were strongly influenced by other organic matter input than sinking marine snow (e.g. sediment resuspension of benthic organic matter, remineralisation of terrestrially derived organic matter, etc.), severing the link between community structure and metabolic potential. Taken together, different organic matter sources shape microbial activity, but not community composition, in New Zealand fjords.

A quantitative analysis of organic matter inputs to soft sediment communities surrounding salmon farms in the Marlborough Sounds region of New Zealand.

Local differences in trophic structure and composition of organic matter subsidies can influence the capacity of soft sediment communities to assimilate recycled organic matter from processes such as salmon farm enrichment. The present study combines biochemical analysis with biomass density information on soft sediment taxa collected within the depositional footprint of salmon farms and at reference sites in the Marlborough Sounds, New Zealand. Distinct biochemical signatures confirmed that the flux of organic matter from salmon farms was an important subsidy for soft sediment communities. Isotopic modelling demonstrated that the proportion of biomass supported by farm-derived organic matter did not change in a consistent pattern along the 300 m gradient from each farm site, whereas the average trophic level of communities decreased with increasing proximity to farms. High variability in both the total biomass and the distribution of biomass across trophic levels occurred among sites downstream of farms and among individual farms. Consequently, estimates of basal organic matter assimilation per unit area by communities differed by several orders of magnitude among sites. Total organic matter assimilation tended to decrease with increasing proximity to farms due to a shift towards a more detrital based community. Differences in basal organic matter assimilation among farms did not appear to be directly related to local flow regime, but instead was closely linked to differences in the soft sediment community composition likely influenced by an array of anthropogenic and environmental factors. The results presented here highlight the importance of considering local variability in basal organic matter source pools, and the potential for synergistic and cumulative effects to drive changes in food web trophodynamics when assessing the impacts of aquaculture on soft sediment communities.

Spatial variations in the stable isotope composition of the benthic algae, Halimeda tuna, and implications for paleothermometry.

On Conch Reef, Florida Keys, USA we examined the effects of reef hydrography and topography on the patterns of stable isotope values (δ18O and δ13C) in the benthic green alga, Halimeda tuna. During the summer, benthic temperatures show high-frequency fluctuations (2 to 8 °C) associated with internal waves that advected cool, nutrient-rich water across the reef. The interaction between local water flow and reef morphology resulted in a highly heterogenous physical environment even within isobaths that likely influenced the growth regime of H. tuna. Variability in H. tuna isotopic values even among closely located individuals suggest biological responses to the observed environmental heterogeneity. Although isotopic composition of reef carbonate material can be used to reconstruct past temperatures (T(°C) = 14.2-3.6 (δ18OHalimeda - δ18Oseawater); r2 = 0.92), comparing the temperatures measured across the reef with that predicted by an isotopic thermometer suggests complex interactions between the environment and Halimeda carbonate formation at temporal and spatial scales not normally considered in mixed sediment samples. The divergence in estimated range between measured and predicted temperatures demonstrates the existence of species- and location-specific isotopic relationships with physical and environmental factors that should be considered in contemporary as well as ancient reef settings.

Depth and location influence prokaryotic and eukaryotic microbial community structure in New Zealand fjords.

Systems with strong horizontal and vertical gradients, such as fjords, are useful models for studying environmental forcing. Here we examine microbial (prokaryotic and eukaryotic) community changes associated with the surface low salinity layer (LSL) and underlying seawater in multiple fjords in Fiordland National Park (New Zealand). High rainfall (1200-8000 mm annually) and linked runoff from native forested catchments results in surface LSLs with high tannin concentrations within each fjord. These gradients are expected to drive changes in microbial communities. We used amplicon sequencing (16S and 18S) to assess the impact of these gradients on microbial communities and identified depth linked changes in diversity and community structure. With increasing depth, we observed significant increases in Proteobacteria (15%) and SAR (37%), decreases in Opisthokonta (35%), and transiently increased Bacteroidetes (3% increase from 0 to 40 m, decreasing by 8% at 200 m). Community structure differences were observed along a transect from the head to the mouth, specifically 25% mean relative abundance decreases in Opisthokonta and Bacteroidetes, and increases in SAR (25%) and Proteobacteria (>5%) at the surface, indicating changes based on distance from the ocean. This provides the first in-depth view into the ecological drivers of microbial communities within New Zealand fjords.

Contribution of sea ice microbial production to Antarctic benthic communities is driven by sea ice dynamics and composition of functional guilds.

Organic matter produced by the sea ice microbial community (SIMCo) is an important link between sea ice dynamics and secondary production in near-shore food webs of Antarctica. Sea ice conditions in McMurdo Sound were quantified from time series of MODIS satellite images for Sept. 1 through Feb. 28 of 2007-2015. A predictable sea ice persistence gradient along the length of the Sound and evidence for a distinct change in sea ice dynamics in 2011 were observed. We used stable isotope analysis (δ13 C and δ15 N) of SIMCo, suspended particulate organic matter (SPOM) and shallow water (10-20 m) macroinvertebrates to reveal patterns in trophic structure of, and incorporation of organic matter from SIMCo into, benthic communities at eight sites distributed along the sea ice persistence gradient. Mass-balance analysis revealed distinct trophic architecture among communities and large fluxes of SIMCo into the near-shore food web, with the estimates ranging from 2 to 84% of organic matter derived from SIMCo for individual species. Analysis of patterns in density, and biomass of macroinvertebrate communities among sites allowed us to model net incorporation of organic matter from SIMCo, in terms of biomass per unit area (g/m2 ), into benthic communities. Here, organic matter derived from SIMCo supported 39 to 71 per cent of total biomass. Furthermore, for six species, we observed declines in contribution of SIMCo between years with persistent sea ice (2008-2009) and years with extensive sea ice breakout (2012-2015). Our data demonstrate the vital role of SIMCo in ecosystem function in Antarctica and strong linkages between sea ice dynamics and near-shore secondary productivity. These results have important implications for our understanding of how benthic communities will respond to changes in sea ice dynamics associated with climate change and highlight the important role of shallow water macroinvertebrate communities as sentinels of change for the Antarctic marine ecosystem.

VARIATIONS IN GROWTH, EROSION, PRODUCTIVITY, AND MORPHOLOGY OF ECKLONIA RADIATA (ALARIACEAE; LAMINARIALES) ALONG A FJORD IN SOUTHERN NEW ZEALAND1.

Spatial and temporal patterns of growth, erosion, productivity, and morphology of the dominant habitat-forming kelp Ecklonia radiata (C. Agardh) J. Agardh were studied bimonthly over 1.5 years in a southern New Zealand fjord characterized by strong gradients in light and wave exposure. Spatial differences in growth were observed with rates at two outer coast, high-light, wave-exposed sites reaching 0.42 and 0.45 cm · d-1 , respectively, compared to 0.27 cm · d-1 at an inner, more homogeneous site. Sporophyte productivity was similar among sites, although population productivity was greater at the outer sites due to population density being 5-fold greater than at the inner site. It was expected that the inner site would have no pronounced seasonal pattern in growth and productivity due to its homogeneity; however, all three sites displayed maximum rates in late winter/spring and minimal in autumn. Growth rates were 2-fold greater during the first growth period than the following year. This discrepancy was not correlated to inorganic nitrogen (N) levels, which remained low year-round (<4 µM), and is likely a result of an interaction between light and temperature, and the photosynthetic capability of E. radiata. Variable pigment content indicated photoacclimation at the inner site. Morphological differences were observed between sites, with E. radiata from the inner site having longer, wider, thinner blades and longer stipes. While E. radiata displayed spatial differences in growth, erosion, productivity, and morphology, populations displayed no temporal differences. These results highlight the need for greater understanding of the mechanisms influencing kelp growth and productivity in a unique marine environment.

Hagfish in the New Zealand fjords are supported by chemoautotrophy of forest carbon.

Forest litter is often considered to be a minor energy source to marine communities due to its refractory nature. Large volumes of forest litter are deposited in the New Zealand fjords, and likely recycled into available energy by microbial activity. In this study we used evidence from stable isotope analyses to test whether recycled carbon from chemoautotrophs was an important contributor to the diet of hagfish (Eptatretus cirrhatus). We then analyzed fatty acid biomarkers from the chemoautotrophic clam Solemya parkinsoni and E. cirrhatus to further discriminate the contribution of marine, terrestrial, and chemoautotrophic sources. Bulk isotopic signatures of E. cirrhatus varied considerably (delta13C, from -29.2 per thousand to -16.7 per thousand; delta15N, from -2.8 per thousand to +15.5 per thousand; delta34S, from -21.7 per thousand to +16.7 per thousand) and indicated that a significant percentage of organic matter (38-51%) originated from chemoautotrophs (delta13C, -31.3 per thousand +/- 0.1 per thousand [mean +/- SE]; delta15N, -5.7 per thousand +/- 0.2 per thousand; delta34S, -32.per thousand +/- 3.8 per thousand). Fatty acid biomarkers were depleted in 13C, particularly cis-vaccenic acid (18:1omega7: delta13C, -39.0 per thousand) indicating specific microbial origins of carbon. A high proportion of forest litter in sediments, coupled with isotopic and fatty acid biomarker results, indicates that terrestrial organic matter is a dominant contributor to this marine benthic system. This study demonstrates a clear linkage between terrestrial and marine ecological processes.

Effects of hydrographic barriers on population genetic structure of the sea star Coscinasterias muricata (Echinodermata, Asteroidea) in the New Zealand fiords.

New Zealand's 14 deep-water fiords possess persistent salinity stratification and mean estuarine circulation that may serve to isolate populations of marine organisms that have a dispersal larval phase. In order to investigate this idea, we analysed the population structure of the sea star Coscinasterias muricata using a mitochondrial DNA marker. Genetic differentiation among populations of C. muricata was analysed using 366 base pairs of mtDNA D-loop. We compared populations from the fiords with several others sampled from around New Zealand. At a macro-geographical scale (> 1000 km), restricted gene flow between the North and South Islands was observed. At a meso-geographical scale (10-200 km), significant population structure was found among fiords and between fiords and open coast. The pattern of population genetic structure among the fiords suggests a secondary contact between a northern population and a southern one, separated by a contact or mixing zone. These populations may have diverged by the effects of random genetic drift and population isolation as a consequence of the influence of estuarine circulation on dispersal. In northern Fiordland, genetic structure approximated an isolation by distance model. However, the pattern in genetic differences suggests that distance alone cannot explain the most divergent populations and that fiord hydrography may increase the effect of genetic drift within populations in the fiords. Finally, our study indicates that populations within the fiords underwent recent rapid expansion, followed most probably by genetic drift due to a lack of gene flow among the fiords.