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Metal fingerprints enhance recycling

Wing, S. R., Wing, L. C., Shatova, O. A., & Van Hale, R. (2017). Marine micronutrient vectors: seabirds, marine mammals and fishes egest high concentrations of bioactive metals in the subantarctic island ecosystem. Marine Ecology Progress Series563, 13-23.


There are vast expanses of the oceans surface called high nutrient low chlorophyll regions (HNLC) where primary production is limited by one or more nutrient. The HNLC regions, however, do host pockets of primary production that indicate some source of the limiting ingredients to remote areas.

Figure 1: modified for Google Earth and mimicked of Figure 1 in source article

In the Southern Ocean production north and south of the Subtropical Frontal Zone (SFZ) (Figure 1) is limited by nutrient availability. South of the SFZ in subantarctic water the limiting nutrients are bioactive metals (Mn, Fe, Co, I, Cu, Zn, As, Cd), and north of the SFZ in subtropical water production is limited by macronutrients nitrogen and phosphorous. At the SFZ, where the water masses meet and mix, productivity is not limited. Researchers speculate that the bioaccumulation of bioactive metals in the upper trophic level predators occurs when they consume lower trophic levels (suspended particulate organic matter (SPOM), macro-algae, and macro-zooplankton) at the SFZ. When the predators release waste, the metals are recycled back into the water column, resulting in a biological pathway for limited nutrients. If waste is released in areas away from the SFZ that are limited by micronutrients, the sudden availability can enable primary production.   The bioaccumulation also occurs in the muscles of the top predators. Bioaccumulated metals are recycled when the predator dies, and the carcass is consumed by another top predator, whom eventually produces waste.

The researchers on this project sought to understand how significant the influence food web structure is on primary production in the Southern Ocean.


The investigation was focused on determining the trophic levels in the food web and if there is evidence of bioactive metal accumulation within the food web. Researchers collected organisms and fecal material representing various trophic levels around Snares Island, north of the SFZ (Figure 1). Samples were analyzed for bioactive metal content and the isotopic compositions of nitrogen (δ15N) and carbon (δ13C), and the results were evaluated with statistics and models.

were collected in 2012 and 2013 from the area around Snares Island. Because multiple levels of a food web were desired, a variety of fishing techniques were employed. Niskin bottles were used to collect SPOM from 6 sites at water depths 0m, 10m, and 30m water depths. Two kelp species were collected from 4 sites, presumably by hand. Macro-zooplankton were trawled from 3 sites. Six coastal fish species were caught with fishing poles. Guano from 8 species of seabird was collected, presumably by hand, and fecal matter for Hooker’s sea lions and New Zealand fur seals was collected via spoon. The Auckland Islands’ results used in this study were from a prior publication by Wing et al. (2014).

Laboratory analysis included determining the isotopic composition of δ13C and δ15N in all samples via Isotope Ration Mass Spectrometry (IR-MS) and bioactive metal concentration by Inductively Coupled Plasma-Mass Spectrometry (ICP-MS).

Laboratory results were analyzed statistically to ultimately determine if the variance in the bioactive metal concentrations between trophic levels was a function of how a food web is organized or the geographic location/water mass. Researchers used a variety of statistical tests to compare the metal contents in the fecal matter of 4 trophic level groups from the Snares Islands and Auckland Islands. Results were clustered to determine trophic level and %SPOM. An analysis of variance (ANOVA) was used to test for differences in bioaccumulation of bioactive metals by species in each trophic group. A discriminant function analysis (DFA) was used as a prediction tool to determine whether the bioactive metal concentrations of fecal matter of individual species could be accurately classified according to the independently defined trophic levels from the study. Permutation multi-variant analysis (PERMANOVA) was applied to determine if the connection between trophic level and bioactive metals varied between different oceanic regions.

Trophic positions within the food web for each species were established based on what it ate and what position on the trophic level is was. Mixing models for δ13C and d15N were employed to determine the relative importance of two organic matter sources at the base of the food web. The isotopic composition of the muscle tissue from the fish yielded the most useful d13C and δ15N because it is a reflection of a long-term diet, where as fecal matter reflects the most recent meal consumed. The fecal material may also undergo reactions that impact the isotopic signal.


Clustering revealed four separate trophic levels supported by the pelagic productivity and macro-algae around Snares Islands (Figure 2 in source article). From lowest rank to highest rank there were coastal foragers, pelagic foragers, high predators, and top predators. The southern black-backed gull represented the coastal forager level. The pelagic foragers included sooty shearwater, red-billed gull, sea perch, blue cod, small-scaled notothenid, cap pigeon, and antarctic tern. The high predators included scarlet wrasse, Snares crested penguin, brown skua, Buller’s albatross, and banded wrasse.   The top predators were the New Zealand fur seal and Hooker’s sea lion.

The accumulation of bioactive metals at different trophic levels was evident (Figure 3 and Table 2 in source article). Metal concentrations were generally higher in pelagic predators than in the foragers and SPOM (Figure 4 in source article). It was also noted that accumulation varied among species within each trophic level. The variability can be explained by the animals diet. For instance, black-backed gulls in the coastal margin have a diet rich of macro-algae. Because the macro-algae have high content of Co and Mn, the black-backed gulls fecal matter also has elevated Co and Mn concentrations.

The DFA results suggest that the trophic levels have distinct concentrations of bioactive metals. Roughly 92% of the time, the analysis was able to correctly identify the trophic level based on the bioactive metal concentration. This is a major result that implies there is a ‘trace metal fingerprint’ associated with different levels of the food web. Mn, Fe, Co, Zn, and Cd where the most helpful in matching fecal matter to trophic level. Furthermore, it supports that fecal metal from high trophic levels is a source of bioactive metals in HNLC regions.

The PERMANOVA analysis yielded that metals varied more between trophic levels then water masses at the locations suggesting the biological pathway is a driver in productivity in the area.


The researchers on this project sought to understand how significant the influence food web structure is on primary production in the Southern Ocean and they concluded that the success of the pelagic and coastal habitats around Snares Island depends of the productivity of New Zealand fur seals and Hooker’s sea lions.   Important limiting nutrients are being bioaccumulated in the upper trophic levels, and the waste products are supporting productivity in the regions that are otherwise nutrient-limited around the Snares Islands and Auckland Islands. It should be noted that although wind blow dust and weathered rock material is a source of metal to the HNCL zones, the form in which it is delivered is not necessarily readily available for biological uptake.


Anne M. Hartwell
Hello, welcome to Oceanbites! My name is Annie, I’m an earth scientist (geology and oceanography). My favorite job as a scientist is working in the laboratory and the field because I love interacting with my research!


2 Responses to “Metal fingerprints enhance recycling”

  1. Fascinating! Thank you:)

    Posted by Karen Pratt | June 18, 2017, 2:21 am

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