Drivers of Mercury Accumulation in Juvenile Antarctic Krill, Epipelagic Fish and Adélie Penguins in Different Regions of the Southern Ocean

Abstract

Antarctica and the Southern Ocean are important sinks in the global mercury (Hg) cycle, and in the marine environment, inorganic Hg can be converted by bacteria to monomethylmercury (MeHg), a highly bioavailable and toxic compound that biomagnifies along food webs. In the Southern Ocean, higher concentrations of Hg and MeHg have typically been reported in the coastal waters of the Ross and Amundsen Seas, where katabatic winds can transport Hg from the Antarctic Plateau and create coastal polynyas, which results in spring depletion events of atmospheric Hg. However, some studies on MeHg biomagnification in Antarctic marine food webs have reported higher Hg concentrations in penguins from sub-Antarctic waters and, unexpectedly, higher levels in juvenile krill than those in adult Antarctic krill. In light of recent estimates of the phytoplankton and zooplankton biomass and distribution in the Southern Ocean, this review suggests that although most studies on MeHg biomagnification refer to the short diatom–krill–vertebrate food chain, alternative and more complex pelagic food webs exist in the Southern Ocean. Thus, juvenile krill and micro- and mesozooplankton grazing on very small autotrophs and heterotrophs, which have high surface-to-volume ratios for MeHg ad-/absorption, may accumulate more Hg than consumers of large diatoms, such as adult krill. In addition, the increased availability of Hg and the different diet contribute to a greater metal accumulation in the feathers of Adélie penguins from the Ross Sea than that of those from the sub-Antarctic.

1. Introduction

The waters of the Antarctic coastal region and the Southern Ocean comprise about 10% of global seas [1], are highly productive and play a key role in sequestering anthropogenic carbon dioxide (CO₂) [2]. Marine organisms that have evolved in these cold and well-oxygenated waters have unique eco-physiological adaptations and are likely to be among the most vulnerable to cumulative stresses caused by climate change and anthropogenic contaminants [3,4]. Indeed, some regions, such as the Antarctic Peninsula, have experienced some of the fastest rates of warming in the Southern Hemisphere [5], and persistent organic pollutants (POPs) produced and used at lower latitudes have been detected in Antarctic organisms since the 1960s [6]. Potentially toxic metals can be released into the Antarctic environment from local natural sources, but their inputs are limited by the low chemical weathering of rocks and soils on a continent almost entirely covered by ice. The impact of local human activities is usually confined to areas surrounding scientific stations [7,8], while a large proportion of trace elements found in snow samples from the Antarctic Plateau originate from other continents at lower latitudes [9]. Long-range atmospheric transport is particularly effective for mercury (Hg), which, unlike other metals, occurs in the atmosphere mainly as gaseous elemental Hg° with a lifetime of 0.5–1 year [10]. In Antarctica, anthropogenic emissions of Hg are negligible, and re-emissions of Hg° from the sea and snow, and a few active volcanoes and fumaroles, are the main natural sources [11]. Due to the global distillation process by which volatile contaminants are transported around the world and condensed and deposited in cold regions [12], Antarctica and the Southern Ocean are important sinks in the global Hg cycle [10]. Moreover, while anthropogenic emissions of Hg° have declined in North America and Europe, artisanal and small-scale gold mining and other human activities are still significant sources in the Southern Hemisphere [13]. The biogeochemical cycle of Hg in the Southern Ocean is influenced by upwelling currents, sea ice and associated biotic communities and is poorly understood. However, in the marine environment, inorganic Hg (iHg) deposited from the atmosphere or released by melting ice and snow can be converted by microorganisms to monomethylmercury (MeHg), a highly bioavailable and potent neurotoxin with a remarkably longer biological half-life than that of iHg [14]. Monomethylmercury is easily assimilated by primary producers and is transferred in increasing concentrations along food webs (biomagnification) [14,15,16].

The biomagnification of MeHg was first detected in pelagic and benthic food webs in Terra Nova Bay (Ross Sea) [14] and has been reported in other Antarctic marine ecosystems [17,18]. Southern Ocean albatrosses such as the wandering albatross Diomedea exulans and large petrels such as Macronectes halli accumulate the highest Hg concentrations ever reported in seabirds due to their diet, lower molting and breeding frequency [19]. However, penguins are the most important Antarctic seabirds and are more suitable as biomonitors of Hg biomagnification in the Southern Ocean because they disperse less in the Southern Hemisphere than flying species [20,21,22]. In reviewing the literature data on Hg concentrations in several penguin species, Gimeno et al. [23] highlighted a latitudinal gradient with higher levels in samples from sub-tropical and maritime Antarctica than in colonies from continental Antarctica. Similar latitudinal patterns of Hg bioaccumulation have been observed in other seabirds [20,24], although higher concentrations of total Hg (tHg) and MeHg have generally been reported near Antarctica than those in lower-latitude waters [25]. However, a recent circumpolar survey of tHg in the feathers of a single species, the Adélie penguin (Pygoscelis adeliae), shows that tHg concentrations are higher in samples from the southernmost colonies [22].

Most studies on Hg biomagnification in Antarctic marine organisms have focused on the short diatom–Antarctic krill–vertebrate food chain, neglecting other epipelagic food webs involving pico- and nanophytoplankton and micro- and mesozooplankton organisms. The transport of ionic mercury (Hg²⁺) and MeHg from seawater into primary producers and micro-heterotrophs (bacteria, protists) occurs mainly by passive mechanisms [26], resulting in the largest Hg bioconcentration step (up to more than 10⁶ times the concentrations in seawater), especially in waters with communities dominated by very small organisms that develop very high surface-to-volume ratios for the ad-/absorption of iHg and MeHg [27,28]. In contrast to other marine organisms, juvenile Antarctic krill (Euphausia superba) have been found to accumulate higher concentrations of iHg and MeHg than adults [29,30,31]. This unexpected result may be due, at least in part, to the consumption of organisms that are much smaller than those grazed by adults. Thus, consumers of juvenile krill and other micro- and mesozooplankton organisms provide an alternative trophic link between primary producers and vertebrates and, by extending the food chain, enhance the biomagnification of MeHg [28].

In Antarctica, climate change will increase land ice melting with the release of contaminants, including legacy Hg [32]. Expected changes in the light and element availability in the marine environment will alter the structure and composition of phytoplankton communities, and some model simulations suggest a possible shift from diatoms to small-cell phytoplankton in the sea ice zone [33,34]. In this context, further knowledge on the biogeochemical cycling of Hg in the Southern Ocean and the bio-ecological factors influencing its biomagnification in seabirds and marine mammals is desirable. Based on recent findings on Hg methylation in polar seas and the regional distribution of phytoplankton and zooplankton communities in the Southern Ocean, this review discusses the available data on Hg concentrations in the most representative species of Antarctic pelagic food webs. By addressing the numerous factors that influence Hg bioaccumulation in Antarctic marine organisms, we will attempt to (1) evaluate how and why juvenile Antarctic krill accumulate more iHg and MeHg than adults and (2) assess regional variations in the Hg bioavailability in different regions of the Southern Ocean by analyzing the available data on Hg concentrations in Adélie penguin feathers collected from the continent and sub-Antarctic islands.

2. Mercury and Methylmercury in the Southern Ocean

Mercury is emitted to the atmosphere from anthropogenic and natural sources mainly in gaseous elemental form (Hg°), which is deposited on the Earth’s surface mostly as reactive Hg²⁺ via wet or dry atmospheric deposition. The metal can be re-volatilized by natural processes, and the cycling of Hg between air, water, land and biota can occur for centuries before the metal is finally deposited in deep ocean and lake sediments or soils [11].

Since the early work on the global distribution of atmospheric Hg°, its concentrations in the Southern Hemisphere (~1.0 ng m⁻³) have been found to be lower and more evenly distributed than those at remote sites in the Northern Hemisphere (~1.4 ng m⁻³) [35]. In the Southern Ocean, slightly higher levels have been measured in the coastal marine boundary layer when influenced by air masses from inland Antarctica [36]. In fact, Hg deposited on the snowpack of the vast Antarctic Plateau can be re-emitted into the atmosphere, and katabatic winds flowing from the plateau towards the Southern Ocean transport Hg° to coastal ecosystems [37,38]. In addition, katabatic winds can contribute to the formation of coastal polynyas, and in spring, marine halogens released from the freezing sea surface oxidize Hg°, leading to rapid Hg²⁺ deposition (i.e., atmospheric mercury depletion events (AMDEs)) [39]. Further spatio-temporal variations in Hg concentrations in the marine boundary layer are also driven by the photoreduction of Hg²⁺ at the sea surface, which increases during the day, making the Southern Ocean a source of Hg° emissions, especially in summer [40].

In general, Hg concentrations in Southern Ocean waters are in the same range as those reported for other oceans. The average total Hg concentrations in ocean waters are about 1.5 pmol L⁻¹ [41], and Cossa et al. report that in the open Southern Ocean from Tasmania to the East Antarctic coast, they range from 0.63 to 2.76 pmol L⁻¹, and the MeHg concentrations range from 0.02 to 0.86 pmol L⁻¹ [42]. Values increase from the surface to intermediate depths, reaching maximum concentrations in waters with minimal oxygen (O₂) [42]. In coastal waters with snow and sea ice, the concentrations of total and reactive Hg are much higher than in the open ocean. Therefore, a net deposition of atmospheric Hg in surface waters near the ice edge and a metal enrichment in the brine during sea ice formation have been suggested [43]. In the Weddell Sea waters, higher although not statistically significant tHg concentrations were measured in spring (2.6 ± 1.3 pmol L⁻¹) than in winter (2.0 ± 1.0 pmol L⁻¹), and the values increased in surface waters at three stations during AMDEs. The average MeHg concentrations in the Weddell Sea were 0.07 ± 0.09 pmol L⁻¹ in spring, which were one-half lower than those measured in the Ross and Amundsen Seas in summer (0.13 ± 0.19 pmol L⁻¹) [43]. Spatio-temporal variations in the concentrations of the different chemical forms of Hg in Antarctic seawater have been reported in other studies [44], suggesting regional changes in Hg bioavailability. Since MeHg is mainly produced in situ by microorganisms from dissolved Hg²⁺, available data on its spatial distribution in the Southern Ocean could help to formulate hypotheses about the areas where Antarctic organisms and food webs are most prone to MeHg biomagnification.

Anaerobic microorganisms such as sulfate- and iron (Fe)-reducing bacteria and methanogens are known to produce MeHg in marine sediments and waters [45]. Thus, higher MeHg concentrations have often been reported in Antarctic subsurface and bottom waters with low dissolved O₂, where sinking organic materials are mineralized by heterotrophic microorganisms. Fecal pellets and organic particles in the water column may also provide a suitable microenvironment for the activity of anaerobic methylating bacteria. However, laboratory experiments with Canadian Arctic waters [46] and stable Hg isotopic signatures of marine particulates, zooplankton and pelagic fish [47] suggest that MeHg may also be formed in oxic waters. A potential Hg-methylating microorganism has been identified in Antarctic sea ice [48] and has also been found in the oxic subsurface waters of all oceans [49]. The actual bioavailability of MeHg in the marine environment depends on the rates of methylation and demethylation, and the latter may be due to Hg-resistant bacteria as well as abiotic pathways such as the action of UV radiation in surface waters (photodemethylation). In polar seas, the halogen photooxidation of Hg° at the air–sea ice interface may increase the availability of Hg²⁺ for methylating bacteria in brine pockets and/or biofilms associated with trapped and decaying organic matter [48]. A significant positive correlation between MeHg concentrations in the upper 50 m of the water column and the hourly fraction of sea ice was found in unfiltered seawater from the Ross and Amundsen Seas, suggesting that the melting of first-year sea ice may release MeHg [25].

3. The Bioconcentration of Mercury in Phytoplankton and Its Transfer to Grazing Zooplankton

Since the Ross expedition (1839–1843), it has been known that the net phytoplankton in many regions of the Southern Ocean is largely dominated by species of colonial or chain-forming diatoms, many of which have circumpolar distributions. However, Antarctic phytoplankton also includes other photosynthetic protists, such as haptophytes, dinoflagellates and silicoflagellates, and their relative abundance varies geographically, with time and depth [50]. The Southern Ocean is one of the most productive seas, and especially in the marginal ice zones, the major vertical fluxes of carbon are usually due to blooms of diatoms or the haptophyte Phaeocystis antarctica [50]. Diatom blooms are generally thought to be favored by conditions of water stratification, high light and iron availability, while those of Ph. antarctica occur under conditions of water mixing, low irradiance and high Fe availability [50]. A recent survey in the Ross and Amundsen Seas [51] also indicates that diatoms dominate in warmer and saltier waters, while haptophytes prefer cold waters. However, during most of the year, nano-flagellates, cyanobacteria, coccolithophores, dinoflagellates and small diatoms account for a large fraction of the chlorophyll in the Southern Ocean water and sea ice, and photoautotrophs coexist with heterotrophic bacteria and viruses [52]. Carbon and the other elements ad-/absorbed by these small organisms are ingested mainly by micro- and mesozooplankton with small oral apparatuses [27,28]. On the contrary, a high proportion of the elements sequestered during blooms of larger or colonial algae are likely to sink to the depths [52]. Thus, local variations in the sea ice and nutrient availability influence the biomass and size of the dominant phytoplankton cells and promote the establishment of alternative food webs. Microzooplankton feeding on cryptophytes, prasinophytes or unicellular Ph. antarctica, which have a greater surface area for the ad-/absorption of iHg and MeHg, will drive the higher biomagnification of MeHg by macrozooplankton and fish, while Antarctic krill and other large crustaceans feeding mainly on diatoms [53] will accumulate less MeHg. The selective collection and analysis of pico- and nanophytoplankton samples from seawater is a very difficult task. However, recent measurements in different sizes of phyto- and zooplankton from the Mediterranean Sea show decreasing concentrations of iHg from pico- to nanophytoplankton and from micro- to meso- and macrozooplankton, with the latter having much higher MeHg concentrations [27,28]. Since zooplankton organisms have longer life cycles than phytoplankton, they can probably eliminate part of the iHg burden, while MeHg will gradually accumulate in their bodies to levels that depend mainly on their age (i.e., exposure time) and diet composition.

4. Higher Contents of Total Mercury and Methylmercury in Juvenile Krill than in Adult Krill

The Antarctic krill has a circumpolar distribution, is one of the largest biomasses on Earth and is the main energy source for squid, fish, seabirds and mammals in several regions of the Southern Ocean. E. superba lives for about 6 years and reaches a length of 6 cm (i.e., a size about two orders of magnitude larger than its dominant prey), creating a short and very-energy-efficient food chain that reduces the transfer of MeHg to higher trophic levels. However, there are also less efficient pelagic food webs in the Southern Ocean that enhance the biomagnification of MeHg. For example, the amphipod Themisto gaudichaudii, which consumes fish eggs, copepods and chaetognaths, has, in the same marine area, 2.5 times higher Hg concentrations than Antarctic krill [17].

The data summarized in Table 1 essentially indicate that Antarctic krill accumulate rather low concentrations of tHg and MeHg, and that the levels are higher in juveniles than in adults and increase near the continent, especially in the Ross Sea (Figure 1a).

Table 1. Concentrations (ng g⁻¹ dry wt, mean ± SD or median *) of tHg and MeHg in Euphausia superba from different regions of the Southern Ocean.

Location	Maturity/Sex	tHg	MeHg	Ref.
South Orkney Islands	Juvenile	71 ± 23	8 ± 3	[31]
	Female	54 ± 18	8 ± 2
	Male	48 ± 11	8 ± 3
South Georgia Island	Juvenile	14 ± 5	8 ± 2	[31]
	Female	6 ± 2	2 ± 0.2
	Male	7 ± 2	3 ± 0.1
Antarctic Polar Front	Juvenile	17 ± 6	5 ± 1	[31]
West of Anvers Island (Coastal)	Juvenile	19.4 ± 13.6	1.38 ± 0.89	[29]
	Adult	8.06 ± 1.84	0.74 ± 0.53
West Antarctic Peninsula Sea Ice Edge (Shelf)	Juvenile	7.25 ± 1.20	1.07 ± 0.25	[29]
	Adult	4.47 ± 1.12	1.03 ± 0.24
Sea Ice Edge (Slope)	Juvenile	7.88 ± 7.81	1.82 ± 0.47
	Adult	2.20 ± 0.52	0.13 ± 0.06
West Antarctic Peninsula	Juvenile	34 *	3.25 *	[54]
	Female	18 *	2.01 *
	Male	18 *	2.01 *
N/W Weddell Sea	All specimens	(19–56) 32		[55]
Ross Sea (Offshore)	All specimens	77 ± 26		[14]
Ross Sea/Marguerite Bay/Livingston Island	All specimens	25 ± 2		[56]
King George Island	All specimens	18 ± 5		[57]
Livingston Island	All specimens	7 ± 8		[18]

Table 1. Concentrations (ng g⁻¹ dry wt, mean ± SD or median *) of tHg and MeHg in Euphausia superba from different regions of the Southern Ocean.

Location	Maturity/Sex	tHg	MeHg	Ref.
South Orkney Islands	Juvenile	71 ± 23	8 ± 3	[31]
	Female	54 ± 18	8 ± 2
	Male	48 ± 11	8 ± 3
South Georgia Island	Juvenile	14 ± 5	8 ± 2	[31]
	Female	6 ± 2	2 ± 0.2
	Male	7 ± 2	3 ± 0.1
Antarctic Polar Front	Juvenile	17 ± 6	5 ± 1	[31]
West of Anvers Island (Coastal)	Juvenile	19.4 ± 13.6	1.38 ± 0.89	[29]
	Adult	8.06 ± 1.84	0.74 ± 0.53
West Antarctic Peninsula Sea Ice Edge (Shelf)	Juvenile	7.25 ± 1.20	1.07 ± 0.25	[29]
	Adult	4.47 ± 1.12	1.03 ± 0.24
Sea Ice Edge (Slope)	Juvenile	7.88 ± 7.81	1.82 ± 0.47
	Adult	2.20 ± 0.52	0.13 ± 0.06
West Antarctic Peninsula	Juvenile	34 *	3.25 *	[54]
	Female	18 *	2.01 *
	Male	18 *	2.01 *
N/W Weddell Sea	All specimens	(19–56) 32		[55]
Ross Sea (Offshore)	All specimens	77 ± 26		[14]
Ross Sea/Marguerite Bay/Livingston Island	All specimens	25 ± 2		[56]
King George Island	All specimens	18 ± 5		[57]
Livingston Island	All specimens	7 ± 8		[18]

Figure 1. Indicative values of total Hg concentrations (ng g⁻¹ dry wt): (a) in Antarctic krill and Adélie penguin feathers; data from [22] and references in Table 1; (b) in Adélie penguin feathers [22] and mosses [38,39,58].

Figure 1. Indicative values of total Hg concentrations (ng g⁻¹ dry wt): (a) in Antarctic krill and Adélie penguin feathers; data from [22] and references in Table 1; (b) in Adélie penguin feathers [22] and mosses [38,39,58].

As a rule, older individuals of marine organisms have limited growth and consume larger prey with higher Hg contents. Considering that juvenile krill’s progressive growth should “dilute” Hg concentrations and that their more frequent molting cycles may contribute to Hg elimination, their higher Hg content compared to adults (Table 1) is surprising. It has been hypothesized that this could be due to a possible release of Hg during egg laying and/or the better ability of adult krill to demethylate and excrete Hg [30]. However, it seems more likely that the consumption of small autotrophic and heterotrophic plankton (efficient bioaccumulators of Hg and MeHg from water) contributes to Hg accumulation in juveniles, whereas adults capture diatom chains rather than individual cells and are unable to graze particles with an equivalent spherical diameter < 10 µm [53]. As noted by Conroy et al. [59], phytoplankton grazing alone cannot support the growth of juvenile krill, which therefore feed on small heterotrophic protists and metazoans. Mercury concentrations in amphipods and ostracods from South Georgia Island were higher than those in E. superba, and among different Euphausia species, the highest values were measured in E. spinifera [17], which mainly ingests cells in the range of 0.7–20 µm [60]. Moreover, juvenile krill have a much lower mobility than adults and develop and stay longer in deeper waters where, especially in highly productive areas, the low oxygen content favors the formation of MeHg by anaerobic microorganisms [61]. Indeed, in the Antarctic Peninsula, the tHg and MeHg concentrations in juvenile krill were significantly higher (p < 0.001) than those in in adults only during a highly productive summer [29]. Furthermore, juveniles are more closely associated with sea ice and spend more time than adults in coastal waters [62], where the bioavailability of Hg and MeHg increases [25,36]. For instance, the much higher Hg concentrations in krill samples from the South Orkney Islands compared to those from South Georgia Island (Table 1) are likely due to differences in the water temperature and sea ice between the two sites [31]. It can therefore be concluded that juvenile krill have higher Hg concentrations than adults because they consume smaller organisms in marine environments that are typically characterized by the higher availability of Hg and MeHg.

5. Plankton Regional Distribution and Mercury Accumulation in Cryopelagic and Epipelagic Fish

A recent estimate of the circumpolar biomass values of phytoplankton, mesozooplankton, Antarctic krill and salps in the epipelagic zone (from 0 to 250 m depth) of the Southern Ocean reports much higher biomass values for mesozooplankton (67 MT) than for phytoplankton (36 MT) or krill (30 MT) [63]. Phytoplankton is mainly concentrated at higher latitudes, especially in areas with polynyas of the Ross, Amundsen and Bellingshausen Seas, and west of the Antarctic Peninsula. Mesozooplankton hotspots occur at mid-latitudes, near islands, while Antarctic krill and salps are mainly concentrated at mid-latitudes in the Atlantic and Pacific sectors. Thus, when tracking Hg transfer in Antarctic fish, seabirds and marine mammals, it should be kept in mind that only in some regions do they feed almost exclusively on Antarctic krill. The Antarctic silverfish Pleuragramma antarcticum, for instance, is an offshore epipelagic species that feeds on mollusks, tintinnids and copepods and is a very important energy source for Adélie penguins [20,64,65,66]. Other fishes, such as the bald rockcod (Pagothenia borchgrevinki) and the dusky rockcod (Trematomus newnesi), are associated with the under-surface of the ice (cryopelagic) and feed on copepods and euphausiids living within or around sea ice (sympagic). Especially in summer, these fishes also feed in the upper water column and may contribute to Hg uptake by penguins [66]. Most of the available data refer to Hg concentrations in fish muscle, reflecting long-term exposure (

Table 2. Total Hg concentrations (ng g⁻¹ dry wt) in the muscle or whole-adult specimens of epipelagic and cryopelagic fishes from coastal Antarctica.

Location	Fish Species	tHg Muscle	tHg Whole Fish	Ref.
Ross Sea	Pleuragramma antarcticum	120 ± 70 a	80 ± 35 a	[64]
Adélie Land	Pl. antarcticum	65 ± 9		[66]
King George Is.	Pl. antarcticum	40 ± 10 a		[68]
Syowa Station	Pagothenia borchgrevinki	26 ± 10	13 ± 4	[67]
Adélie Land	P. borchgrevinki	67 ± 40		[66]
Ross Sea	P. borchgrevinki	605 ± 166 a		[69]
Adélie Land	Trematomus newnesi	79 ± 24		[66]
Ross Sea	T. newnesi	545 ± 101		[69]
Ross Sea	T. newnesi	290 ± 240		[14]

^a Values expressed on dry wt basis using a wet–dry mass ratio of 5 [70].

). However, penguins eat whole fish, and the amount of Hg actually ingested can be estimated by considering that in the whole bodies of Pl. antarcticum and P. borchgrevinki, the total Hg contents are about 67% and 50%, respectively, of those present in the muscle [64,67].

As with Antarctic krill, fish from the Ross Sea have much higher Hg concentrations than samples collected elsewhere in the Southern Ocean (Table 2). In the Ross Sea, the Antarctic silverfish accumulates more Hg than Antarctic krill (Table 1), but at much lower levels than cryopelagic rockcods. Silverfish can live up to 20 years and reach a length of about 20 cm, while bald and dusky rockcods are slightly larger and live in coastal environments where high productivity and melting glaciers and sea ice increase the bioavailability of iHg and MeHg [25,36].

6. Adélie Penguins as Biomonitors of the Circumpolar Availability of Mercury

While ingested iHg is poorly absorbed and is mostly excreted in feces and urine, MeHg is efficiently absorbed, enters the liver and bloodstream and reaches other organs and tissues. In the livers of seabirds and marine mammals, MeHg is demethylated, and the resulting iHg binds to selenium to form inert tiemannite crystals [71]. Between molts, circulating Hg binds to keratin proteins of growing feathers or fur and is excreted during molting. Unlike other seabirds, penguins molt their entire plumage simultaneously each year, and the Hg accumulated in feathers between molts reflects exposure to Hg over several months to a year [20,21]. Due to its circumpolar distribution and year-round foraging in the Southern Ocean, the Adélie penguin has been selected as a bioindicator species by the Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR) [72]. During the breeding season, Adélie penguins forage in marine areas adjacent to the colony and then travel enormous distances to feed in the marginal ice zone, but their diet is unlikely to change significantly throughout the year [20]. Feather analysis therefore allows for the assessment of the Hg availability and biomagnification over relatively large Antarctic and sub-Antarctic marine areas. Feather sampling is a non-invasive and reliable monitoring approach, and a recent paper presents the distribution of the tHg concentrations in P. adeliae feathers from 24 colonies distributed across continental and maritime Antarctica [22]. In essence, the study shows the following:

-

Within the same marine area, P. adeliae feathers often have lower Hg concentrations than those of other penguin species or flying seabirds, which are likely to feed in deeper waters on organisms of higher trophic levels;

-

The mean Hg content of Adélie chick feathers is usually lower than that of adult feathers (0.22 ± 0.08 and 0.49 ± 0.23 µg g⁻¹ dry wt, respectively);

-

Overall, differences in the Hg contents between the sexes were not statistically significant;

-

Samples from East Antarctica had Hg concentrations intermediate between the low values in the Maritime and western Antarctic Peninsula and the highest values in the Ross Sea (Figure 1);

-

The highest Hg bioaccumulation in penguins from the Ross Sea was probably due to possible natural sources of Hg and higher fish consumption compared to the other colonies with a krill-dominated diet [22].

These results are consistent with the above-mentioned current knowledge on the cycling of Hg in Antarctic waters, the regional distribution of plankton communities and the diverse feeding ecology and food webs in Southern Ocean waters. Using only one penguin species as a biomonitor, the hypothesized latitudinal gradient with higher tHg concentrations in penguins from lower latitudes [23] does not exist, and the highest values occur in samples from high latitudes where seawater contains higher concentrations of Hg.

7. The Enhanced Bioaccumulation of Hg in the Ross Sea Food Webs

The Ross Sea is a large embayment of continental Antarctica with the largest continental shelf and one of the highest productivity rates in the Southern Ocean. It is covered by sea ice for about 9 months of the year, and strong, persistent katabatic winds cause the recurrent formation of coastal polynyas that produce sea ice and the sinking of cold, dense water. Due to the unique oceanographic and physico-chemical features of the Ross Sea, seabirds and marine mammals feed on species different from those normally consumed in other regions of the Southern Ocean [73]. To protect this unique marine ecosystem, the Ross Sea Marine Protected Area [74], the largest protected area in the world, came into force in 2017. Approximately one-third of the world’s Adélie penguins nest in ice-free areas along the Ross Sea coast, feeding under pack ice, in coastal fast ice or in open, ice-free waters, depending on the local sea ice characteristics [65]. Although differences in their foraging distances and prey have been found even between two colonies separated by only 75 km [65], the Antarctic silverfish and the crystal krill (Euphausia crystallorophias) are usually the most important prey of Adélie penguins above 74° S [75,76]. Along the coast of Victoria Land, slightly higher tHg concentrations were found in penguin feathers from Ross Island than in those from Cape Hallett and Cape Adare [21], and a recent larger study [22] confirms that samples collected above 74° S, and particularly from Terra Nova Bay, have higher tHg concentrations (Figure 1b). Interestingly, a biomonitoring survey of lichens and mosses along coastal Victoria Land [38,39,58] showed much higher Hg concentrations in samples collected in ice-free areas in front of the coastal polynya of Terra Nova Bay (Figure 1b).

The active volcano Mount Erebus (3792 m a.s.l.) likely contributes to Hg deposition in the Ross Sea, and biomonitors appear to indicate additional Hg inputs from AMDEs in the coastal polynya. However, the penguin diet is also likely to play an important role in Hg accumulation. In early spring, the platelet ice that forms in Terra Nova Bay supports an important nursery for Pl. antarcticum [77], and penguins in the bay were found to consume more fish than those in colonies further north [75]. Moreover, although Antarctic silverfish are the main summer food of Adélie penguins, a stronger benthic–pelagic coupling has been suggested in coastal ecosystems of the Ross Sea than in other Antarctic regions [73], and Adélie penguins nesting on Inexpressible Island also ate Trematomus bernacchii [65], a widespread benthic fish in the Ross Sea known for its ability to accumulate Hg [14].

8. Conclusions

Antarctica and the Southern Ocean are sinks for Hg° transported from long distances and emitted by local natural and anthropogenic sources. In addition, legacy Hg is released into the Southern Ocean from melting snow and ice. In areas of the water column with low oxygen concentrations and in the sedimentary environment, anaerobic microorganisms can convert iHg to MeHg. This highly toxic and bioavailable compound biomagnifies along benthic and pelagic marine food webs. Recent studies suggest that MeHg may also be produced in oxygenated surface waters and Antarctic sea ice. In the Southern Ocean, higher Hg concentrations have often been reported in the coastal environments of the Ross and Amundsen Seas, where katabatic winds cause the formation of coastal polynyas that promote Hg depletion events in spring. Katabatic winds can also transport into coastal areas the Hg released into the atmosphere from snow and ice on the Antarctic Plateau. Thus, the cycling of Hg between snow, ice, seawater and marine organisms in the Southern Ocean is complex and still poorly understood. Studies on MeHg biomagnification along Antarctic food webs often refer to the diatom–krill–marine vertebrate food chain, neglecting the fact that energy transfer from photoautotrophs to seabirds and marine mammals may involve multiple zooplankton and fish taxa. These alternative food webs contribute to increasing the amount of MeHg transferred to end users. Recent estimates indicate that the biomass of mesozooplankton in the Southern Ocean is much higher than that of phytoplankton and krill, suggesting that, in epipelagic waters, many herbivorous species, much smaller than E. superba, play a more important role than previously thought in transferring energy and persistent contaminants to macrozooplankton and fish. Due to their small feeding apparatus, micro- and mesozooplankton organisms prey on micro-heterotrophs and small algal cells, which develop a very high area-to-volume ratio for the adsorption of iHg and MeHg. Therefore, all macrozooplankton species that feed on micro- and mesozooplankton are at a higher trophic level and accumulate more MeHg than E. superba, which is unable to feed on small particles and feeds mainly on diatom chains. Probably for this reason, adult Antarctic krill have lower tHg concentrations than those of juveniles or other euphausiid species such as E. spinifera, which feed on very small organisms and particles. Also, unlike adults, juvenile Antarctic krill feed mainly in coastal areas where the bioavailability of iHg and MeHg is higher.

In summary, this review indicates that the regional distribution of tHg concentrations in Antarctic krill and cryopelagic and epipelagic fishes mirrors that found in Southern Ocean waters, with the higher bioavailability of iHg and MeHg in the Ross Sea. Although the tHg levels in some penguin species and other marine organisms were found to be higher in sub-tropical waters than in samples from continental Antarctica, the circumpolar distribution of the Hg concentrations in Adélie penguin feathers demonstrates that the assumed latitudinal gradient does not exist. Adélie penguins feed mainly at shallower depths and lower in the food chain than many other Antarctic seabirds. This species accumulates the lowest Hg concentrations in areas where it feeds almost exclusively on Antarctic krill, and the highest in the southern Ross Sea, where the silverfish Pl. antarcticum and the crystal krill E. crystallorophias are the main components of its diet.

While this review helps to clarify some aspects of Hg transfer in Southern Ocean food webs, it also draws the attention of the scientific community to some research questions that need to be addressed for a better understanding of the biogeochemical cycling of Hg in the Southern Ocean. In particular, there is a need for better knowledge of the MeHg formation in sea ice and oxic surface waters, the structure and composition of marine food webs in different Antarctic regions, the amount of Hg and MeHg released by seasonal sea ice melt and the role of cryopelagic communities.