Biomonitoring and assessing total mercury

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Biomonitoring and assessing total mercury concentrations and pools in forested areas. 49 ...... NSERC via its Discovery and Collaborative Research. Programs ..... Carbonaceous biolithes: world averages for trace element contents in black ...


Biomonitoring 2015; 2: 47–63

Research Article

Open Access

Mina Nasr, Paul A. Arp*

Biomonitoring and assessing total mercury concentrations and pools in forested areas DOI 10.1515/bimo-2015-0008 Received August 22, 2015; accepted: December 10, 2015

Abstract: This article focusses on the bio-monitoring of total Hg (THg), sulfur (TS) and carbon (TC) concentrations and pool sizes in forest vegetation and soil layers within the context of a maritime-to-inland transect study in southwestern New Brunswick. This transect stretches from the Grand Manan Island in the Bay of Fundy to the mainland coast (Little Lepreau to New River Beach) and 100 km northward to Fredericton. Along the Bay, frequent summer fogs are thought to have led to increased THg concentrations in forest vegetation and soils such that island THg > coast THg > inland THg concentrations. Transect sampling was done in two phases: (i) a general vegetation and soil survey, and (ii) focusing on specific soil layers (forest floor, top portion of the mineral soils), and select moss and mushrooms species. By way of multiple regression, it was found that soil, moss and mushroom THg and TS were strongly related to one another, with THg decreasing from the island to the inland locations. The accumulated Hg pool within the mineral soil, however, far exceeded (i) the estimated THg pools of the forest biomass (trees, moss and mushrooms) and the forest floor, and (ii) the literature-reported and case-study inferred net input/output rates for annual atmospheric Hg deposition and sequestration, Hg volatilization, and Hg leaching. Partitioning the total soil Hg pool into geogenically and atmospherically derived portions suggested that mineral soils in temperate to boreal forest regions have accumulated and retained atmospherically derived Hg over thousand years and more. These results are summarized in terms of further guiding forest THg monitoring and modelling efforts in terms of specific vegetation and soil sampling targets.

*Corresponding author: Paul A. Arp, Faculty of Forestry and Environmental Management, University of New Brunswick, Fredericton, E3B 5A3, New Brunswick, Canada, E-mail: [email protected] Mina Nasr, Faculty of Forestry and Environmental Management, University of New Brunswick, Fredericton, E3B 5A3, New Brunswick, Canada

Keywords: Total Hg concentrations, pools, fluxes, THg turnover rates; foliage, wood, moss carpets, lichens, mushrooms, forest floor, mineral soil.

1 Introduction The biomonitoring of mercury (Hg) accumulations and concentrations in forest vegetation and soils provides an important means to determine how much of atmospherically transported Hg is sequestered and retained across forested landscapes [1-4]. Relating these accumulations to direct atmospheric deposition as opposed to other Hg sources is, however, difficult because of highly varying biophysical and biochemical Hg transformation and transference processes as Hg passes from the forest foliage to the forest floor, from there into the underlying mineral soil layers, and then into organisms that feed on roots and soil organic matter [5-9]. Tree foliage, lichens, mosses, fungal fruiting bodies (mushrooms) and soils are obvious targets for monitoring atmospheric Hg deposition. In particular, forest canopies are known to sequester atmospheric Hg in particulate, reactive and elemental forms [1,7,10-11]. In foliage, this sequestration occurs through stomatal absorption (gaseous Hg only), and through non-stomatal Hg adsorption as well [11]. Other canopy-residing organisms, such as leaf-like and elongated lichen species, also adsorb Hg [12]. Foliar Hg concentrations increase from the beginning to the end of each growing season [13]. On both open and shaded ground, atmospheric Hg is taken up by ground vegetation, and by mosses in particular [3,14,15], with moss THg increasing quickly in mosses transplanted from low to high Hg exposure locations [16-17]. In mushrooms, THg concentrations also increase with increasing Hg exposure downwind from coal burning power generators and smelters [18-24]. Most of the canopy-absorbed or adsorbed Hg is either washed down from foliage, epiphytes, twigs and branches during heavy fog and rain events, or is part of canopy litterfall [25-26], thereby adding to the Hg pool of

© 2016 Mina Nasr, Paul A. Arp, published by De Gruyter Open. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivs 3.0 License.

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 M. Nasr, P.A. Arp

the forest floor [27-30]. From the forest floor, some of the accumulated Hg enters the mineral soil below on account of biomixing and leaching [31-32]; yet another part may leave the forest floor on account of surface run-off [32]. This lateral transfer is facilitated by Hg-carrying dissolved or particulate organic matter [33], and this process is increased by greater surface exposure and increasing organic matter solubility with increasing forest floor pH [34]. Only a small portion of soil-retained Hg enters streams and lakes from uplands through groundwater seepage [35-36], with some of this in the form of MeHg [37,38]. In wetlands, sediments and poorly drained soils, some of the accumulating Hg is methylized by sulphate and iron-reducing bacteria to form toxic CH3Hg+ (MeHg) ions [39-43]. Some of the forest-sequestered Hg volatilizes back into the atmosphere from the canopy, the forest floor, snow-covered ground, and open-water surfaces [44-47]. At the surface, this is mainly due to organically facilitated photochemical reduction of Hg2+ to volatile Hg0. The rate of volatilization from forest floor and mineral soils generally increases with increasing temperature, biological activity and sun exposure, but remains low in cool and shaded areas [48,49]. Some of the soil-produced Hg0 evades this process through wetting and re-wetting displacements [50]. Mushroom-accumulated Hg also evades on decay, but more so from mushrooms with low rather than high TS concentrations [8,51]. The largest Hg losses from forests occur through forest fires, and mostly from the burning forest vegetation and the forest floor, and less from the underlying mineral soil layers [52]. A portion of soil-accumulated Hg is derived from the weathering of geogenic mineral sources [53]. Higher weathering rates of soil parent materials, however, do not necessarily lead to higher Hg concentrations in soil layers. In all cases, S-containing soil organic matter has a high affinity for Hg by way of organic matter – metal complexation [54]. In contrast, the affinity between Hg and soil minerals such as feldspar and quartz is quite low to absent [55]. Nevertheless, Hg concentrations increase in mineral soils above bedrock shear zones [56], in glacial drifts from Hg-containing ore zones [57], and above metamorphosed mafic, ultramafic, and sedimentary rocks (e.g., black shales) with a high Hg and S mineral content [58], with HgS being very insoluble. For the most part, vegetation, forest floor and soil-accumulated Hg is bound to organic and mineral matter due to strong Hg-S binding [8,51,54,59]. The uptake of Hg by vascular plants, lichens, mosses and mushrooms [60-61] raises concerns about potentially detrimental effects of Hg bioaccumulation on terrestrial organisms [62-64]. Root uptake of Hg by vascular plants,

however, tends to be low, since Hg is strongly held by S-containing soil organic matter [48,65-66]. In addition, root uptake of Hg may be low due to Hg transference from mycorrhizal root tips to fungal fruiting bodies [67-68]. Hence, forest fungi provide a bioaccumulation pathway for soil-accumulated Hg, notably through myceliaingesting earthworms and mushroom-consuming insects, slugs and animals [69-74]. This article provides a qualitative and quantitative overview of how THg concentrations and mass pools vary in forests above and below ground. This overview is based on the forest THg concentration sampling surveys in [8,51], and is supplemented with additional THg concentration and pool size characterizations. This study was centered on southwestern New Brunswick (NB, Fig. 1), with sampling locations located on an island in the Bay of Fundy (Grand Manan), along the mainland coast (Cranberry Head to New River Beach), and inland within the University of New Brunswick Forest in Fredericton, 100 km north of the coast. Concerns about high Hg accumulation in terrestrial and aquatic biota within this area have been expressed [75-77]. Enhanced bioaccumulation of Hg could be due to frequent and persisting summer fogs that add to the

Figure 1. Locator map for the case study sampling locations. Island: Grand Manan; Coast: Cranberry Head, New River Beach; Inland: Fredericton, UNB Forest.

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Biomonitoring and assessing total mercury concentrations and pools in forested areas 

canopy-level capture of ocean-upwelling Hg and MeHg [78-80]. One would therefore expect a downward islandto-inland gradient of Hg within the forest vegetation and soils, being highest along high cliffs along the southern tip of Grand Manan and lowest at the 100 km inland location. This gradient, if present, should also express itself within the THg concentration and pool size variations of the forest biomass (foliage, wood roots), the forest floor, and the mineral soil.

2 Methods As described in [8] and [51], samples were collected from early summer to early fall for 3 consequent years (2003–2005), Fig. 1 and Table 1. This was done in two phases. Phase 1 involved a random vegetation and soil survey (all soil layers), while Phase 2 focused on retrieving moss, mushroom and forest floor (L, F, H) and A-layers only. Phase 1 (early summer, 2003) yielded: 1. 504 samples pertaining to ground vegetation (herb, shrub, fern, grass, moss), tree parts (foliage, branch, bark, wood chip), lichens (soil based and tree lichen), and saprophytic mushrooms (soil and tree based); 2. 84 substrates samples including beach gravel (n = 4), lagoon and bog peat (n = 22), brackish and clear water mud (n = 14), muck from swamps (n = 4), and forest floor and mineral soil layers (n = 40).

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Phase 2 (late summer, fall 2004, 2005) yielded: 1. 518 forest floor, 141 topsoil samples (L, F, H, and Ah, Ahe and Ae), and 30 mid- to sub- soil samples (Bf, Bm, BC, C), with organic matter content decreasing in the order Ah > Ahe > Ae, and soil leaching increasing in the same order; 2. 170 moss samples: Pleurozium schreberi, Polytrichum juniperinum, Ptilium crista-castrensis, and Sphagnum sp.; 3. 727 ectomycorrhizal mushrooms (13 genus: 29 species) taken from moss and non-moss covered locations, and 11 saprophytic mushrooms taken from woody debris and dead tree trunks (3 species). Forest cover varied from mixedwoods with conifers dominant to tolerant hardwoods dominant. Bedrock type was primarily siliceous igneous (Jurassic basalt on Grand Manan), Precambrian meta-sedimentary (mainland coast), and Carboniferous sedimentary (inland location), covered by combinations of ablation till on basal till. Soils varied from shallow podzols and brunisols on uplands to gleysols in wet areas [81]. Elemental analyses were performed on freeze-dried samples for THg concentrations (ppb, dw); method EPA 7473, using a DMA-80 analyzer), and TC, TS, and TN (%, dw; LECO® CNS-2000 analyzer). The statistical evaluations involved basic summaries, analysis of variance (ANOVA), post-hoc difference testing (Scheffe,

Table 1. Geographic positions of the sampling locations. Forest Location

GPS location, decimal degrees

Sampling area

 

 

West

North

ha

Inland

Fredericton, University of New Brunswick Forest

66.6419

45.9199

1.56

66.6416

45.9193

66.6369

45.9168

3.31

66.6406

45.9161

3.84

66.6433

45.9097

2.22

66.67454

45.9133

5.23

Cranberry Head 1

66.338

45.1349

97.59

Cranberry Head 2

66.3355

45.1273

New River Beach

66.5235

45.1226

18.3

Little Lepreau

66.4876

45.1386

11.87

 

Chance Harbour

66.3659

45.1395

10.36

Island

Seal Cove

66.8507

44.6433

24.11

Deep Cove

66.8762

44.6161

9.76

Southern Head

66.8833

44.6061

23.39

  Coast

 

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 M. Nasr, P.A. Arp

Bonferroni/Dunn), and single to multiple regression analyses. The analyses were performed by soil layer type, location (island, coast, and inland), moss species (green tissues only), and fungal genus, with mushrooms analyzed by cap versus stalk and developmental stage (emergent, mature, senescent). The best-fitted THg multiple regression results for mosses, mushrooms, and L-, F-, H- and A-layer soils are presented below in simplified form, and by detail in the Appendix. The THg and TC concentrations were used to estimate per hectare THg and TC pool sizes (mass) per stand compartment, i.e., for (i) foliage; (ii) wood (branches, twigs, bark and bole combined); (iii) coarse (> 5 mm) and fine (≤ 5 mm) roots; (iv) soil layers (L, F, H, Ah, Ae, Bf, Bm, BC, C); (v) mosses; (vi) ectomycorrhizal mushrooms and mycelia. Some of the Hg and C concentrations and pool sizes were based on literature references. The calculations proceeded as follows: soil mass per layer (ton ha-1) = depth per layer (m) × density per layer (ton/m-3) × 104 m2 ha-1 TC pool per layer (ton ha-1) = soil mass per layer (ton ha-1) × TC (%)× 10-2 THg pool per layer (g ha-1) = soil mass (ton ha-1) × THg (ppb) × 10-3 TC pool per plant compartment (ton ha-1) = mass per plant compartment (ton ha-1) × TC (%) × 10-2 THg pool per plant compartment (g ha-1) = mass per plant compartment (g ha-1) × THg (%) × 10-3 Soil depth and density were specified based on generalized soil survey data for the New Brunswick [81]. Since the geogenic Hg component in soils and tills away from major hydrothermal deposition zones is generally low [82], subsoil THg concentration was set at 23  ppb. The mass of geogenic derived THg (THggeo) was then calculated by setting THggeo (g ha-1) = mineral soil mass (ton ha-1) × 23 ppb × 10-3, with mineral soil mass (ton ha-1) = total soil mass (ton ha-1) – total soil TC mass (ton ha-1) × 1.72 g ha-1 where total soil mass and total soil TC mass represent the combined A to C soil layers. The atmospherically derived portion of the THg pool within the mineral soils (denoted below as THgatm) was estimated as the difference between the combined THg pools within the mineral soil and THggeo, i.e., THgatm(g ha-1) = combined soil THg pool (g ha-1) - THggeo (g ha-1).

3 Results and Discussion 3.1 THg in vegetation Mean THg concentrations varied by the above-ground vegetation components as follows (Table 2, vegetation samples from Phase 1 and 2 combined): Peas, rosehips < tree leaves (early summer) < leaves (flowering plant) < apple blossoms < berries < twigs < shrub leaves < sedge < needles (average) < ferns < aquatic vegetation < grasses < bark < liverwort < mosses < tree fungi < lichens < saprophytic fungi < ectomycorrhizal fungi. Within the tree needles, THg concentration increased by year: 1st year THg < 2nd year THg < 3rd year THg < 4th year THg (ANOVA p-value < 0.0001; post-hoc zero difference p-values < 0.0001). Foliage THg concentration increased steadily from leaf-out to leaf-fall [83], but with coniferous foliage accumulating Hg more slowly at 6 to 10 ppb a-1 (Table 2) than deciduous foliage, for which THg concentration would rise from about 5 to 10 ppb in spring to 30 to 45 ppb a-1 prior to leaf-fall [83]. These values would vary (i) by changing Hg concentrations in the air within and outside forest canopies [28,84], and also (ii) by Hg-retaining TS. This is shown in Fig. 2 by way of the THg versus TS results for wood, bark, twig and foliage from a forest biomass residue study across Nova Scotia [85] for which: bole wood THg, TS < bark THg, TS ≈ twig THg, TS < foliage THg, TS, with bark THg being the most variable (ANOVA p-value < 0.0001, post-hoc zero-difference p-values < 0.0005, except for bark and twig THg and TS). Separating the bark component into branch/twig bark and stem bark (bark samples type coded 1, otherwise 0) yielded the following regression equation for tree THg in relation to TS across all tree components (wood, twig, bark and foliage): THg(ppb) = (548 ± 0.025) TS(%) + (13 ± 3) branch/ twig_bark - (19 ± 5) stem_bark; R2 = 0.80. The THg contrast between branch/twig bark versus stem bark may be due to the thicker bark and a lower presence of lichens on stems than branches and twigs. The best-fitted scatter plots in Fig. 2 for tree THg versus tree TS show no particular differences by tree species, but a greater THg versus TS scatter for the bark samples than for the foliage, twig and wood samples. This scatter may also be due to the variable presence of lichens across the bark samples. In comparison, lichens THg was generally higher than foliage, twig and bark THg, with Usnea having the highest

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n

Vegetation: miscel- Peas, rosehips 2 laneous, upland & Deciduous foliage (alder, 4 wetland apple, white birch) Flowers (aster, dandelion) 4 Flowers (apple blossom) 2 Berries (bunch berry, cree- 18 ping strawberry, raspbery, sarsaparilla) Shrub foliage (Chama17 edaphne calyculata, Gaultheria, Kalmia angustifolia) Sedge 3 Fern (fiddlehead stage) 4 Labrador tea, foliage 4 Grass 9 Liverwort (Bazzania ptili- 7 dium) Aquatic vegetation Chaetomortha, Nela5 gonium, Cystodonium, Purpureum, Laminaria, Saccharina Coniferous foliage: 1st year 30 balsam fir; black, 2nd year 30 red & white spruce; 3rd year 29 cedar 4th year 18 Wood: cedar, fir, Stems 41 larch, red and white Twigs 19 spruce, white pine Bark 29 Mosses Ptilium crista-castrensis 46 Sphagnum sp. 71 Polytrichum juniperinum 28 Pleurozium schreberi 25 Lichens Reindeer moss, Wax paper 34 lichens Old Man’s Beard (Usnea) 99 Conks (Shelf fungi) Inner flesh 2 Surface 7

Vegetation components

0,6 5,2 6,5 8,7 0,7 13,0 17,2 28 91 113 147 10 24 61,2 241

244 64,1 251

5,2 0,8 14,1 1,4 41,7

14,3 14,9 21,5 25,2 59,5

6,6 11,7 18,3 23,8 4,8 47,3 46,0 79 152 185 267 124

2,5

11,4

1,0

2,0 3,4 1,0

4,8 5,3 7,5

16,1

2,2 1,9

Min

3,6 4,6

Mean

Table 2: Summary of total Hg concentrations (THg, ppb) by vegetation type.

635 66,9 552

20,3 32,0 48,9 49,8 11,1 93,7 97,6 137 215 258 400 337

64,0

31,4 37,8 34,8 91,2 74,6

45,9

8,1 7,1 17,5

4,9 7,1

Max

116 4 14

4,7 5,9 9,3 10,9 1,5 24,0 21,1 28 27 37 54 74

27,0

14,8 17,0 9,2 27,7 13,4

10,4

2,7 2,6 5,0

1,9 2,7

StD

 

Sediments, organic

Sediments, mineral

Soil

Mushrooms, ectomycorrhizal fungi, by genus

Mushrooms, saprophytic fungi

Vegetation components

Fresh water streams 4 Brackish water lagoons 12 Fresh water streams 4

13 192 44 23 211 272 35 237 277 4 10 4

28 10 66 74 71

Hydnum Tylopilus Leccinum Suillus Lactarius

Xanthoconium Cortinarius Bankera Boletus L F H Ah, Ae Bf, Bm, BC, C Gravel Peat Brackish water lagoons

92

Russula

84

2 30 9

Entoloma strictius Cantharellus Craterellus

Amanita

4 5

Psathyrella foenisecii Maramius oreades

n

20,3 11,6 51,1

962 1336 1761 2836 141 260 299 105 88 2,9 168 8,6

712

249 297 399 414 482

242

1133 74 133

736 963

Mean

19,2 6,6 38,8

200 98 308 459 19 12 87 13 22 2,5 141 7,1

30

76 30 50 30 17

3

798 12 68

120 146

Min

21,3 15,8 63,4

2025 10475 3698 5805 536 818 616 789 296 3,3 212 10

4855

546 530 2876 2927 2145

2860

1467 249 222

578 2420

Max

1,2 3,9 14,2

482 1201 853 1653 80 120 138 81 43 0,5 35 1,7

783

121 156 489 611 443

406

473 66 53

218 970

StD

 Biomonitoring and assessing total mercury concentrations and pools in forested areas   51

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 M. Nasr, P.A. Arp

Figure 2. Scatterplot of THg versus TS for wood, bark, twig and foliage samples: Nova Scotia forest biomass residue study project [85], by tree component (left) and species (right); bf balsam fir, bs black spruce, rs red spruce, ws white spruce, yb yellow birch.

values (Table 2, ANOVA p-value < 0.0001). This suggests that the long-lasting and slow-growing beard-like structure of Usnea provides an effective means for atmospheric THg interception and retention [31, 79-80]. Wax paper lichens also accumulated more THg than foliage and twigs, but not as much as Usnea (Table 2). Ground-based vegetation (grasses, herbs, mosses) had generally higher THg concentrations than tree foliage. This would be due to direct interception of canopy throughfall, stomatal re-absorption of volatized forestfloor Hg, and reduced Hg volatilization under cooler and shaded conditions. For roots, THg concentrations generally varied from 10 ppb in coarse roots to about 300 ppb in fine roots < 5 mm thick [86].

3.2 Moss THg The THg concentrations for the four moss species of this study followed the order (ANOVA p-value < 0.0001, posthoc zero difference p-values < 0.0005; [51]): Pleurozium schreberi > Polytrichum juniperinum > Sphagnum sp. > Ptilium crista-castrensis. The species-to-species differences were also significant, with the difference between Polytrichum and Sphagnum being least significant (p-value = 0.05). The large difference between Pleurozium and Ptilium THg concentrations is remarkable because these species often grow together on damp and dark understory conditions. The significant difference in mean TS concentrations (i.e., Pleurozium TS = 0.181 +/- 0.012 SE % > Ptilium TS = 0.134 +/- 0.004 SE %; post-hoc zero p-value < 0.0001) accounts for the corresponding THg concentration difference, at

least in part. The differential growth rates, i.e., Ptilium > Pleurozium, may further contribute to this difference. In comparison, the intermediate Sphagnum THg concentration < Polytrichum THg concentration would be due to similar mean TS concentrations (0.163 +/- 0.006SE % and 0.168 +/- 0.005SE%, respectively), with Sphagnum and Polytrichum carpets generally developing under wet and sun-exposed versus dry and shaded conditions, respectively. In addition, Polytrichum carpets may accumulate Hg not only by way of canopy throughfall, but also through rhizoidal uptake from their underlying soil and forest litter substrates [87]. Multiple regression analyses it was confirmed that moss THg was not only species specific, but also increased with increasing moss TS. In addition, moss THg increased with increasing F-layer THg but decreased with increasing soil TS, i.e., increased litter and forest floor TS content reduced the THg accumulations in moss carpets. The best-fitted regression model (Appendix) produced the following equation: Moss THg (ppb) = 206.0 - 178.8 Ptilium - 112.7 Sphagnum 69.6 Polytrichum + 0.15 F-layer + THg (ppb) +339 moss TS (%) - 243.2 F-layer TS (%); R2 = 0.90.

3.3 Mushroom THg Mushroom THg varied significantly (ANOVA p-value < 0.0001) by species/genus type, substrate type (wood, forest floor, mineral soil), and by mycorrhizal versus saprotrophic fungi [51]. Among the mycorrhizal genus, Cantharellus, Craterellus and Russula had low THg concentrations, but the saprophytic species had even

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Biomonitoring and assessing total mercury concentrations and pools in forested areas 

lower THg concentrations (post-hoc difference p-values < 0.0001). For the multiple regression analyse, mushroom and soil layer THg and TS were converted into log10THg and log10TS concentrations because (i) mushroom THg varied by three orders of magnitude, (ii) the actual versus best-fitted log10THg scatterplots were linear and fairly evenly distributed, and (iii) all best-fitted THg values after converting back from log10THg would be positive. The best-fitted result (Appendix) produced the following equation: Mushroom log10THg (ppb) = 0.73 Cortinarius + 0.82 Bankera + 0.26 Lactarius - 0.80 Cantharellus + 0.25 Developmental stage + 0.07 Cap/Stalk + 0.47 Fungal log10TS (%) + 0.4 F-layer log10THg (ppb) + 0.80 F-layer log10TC (%) - 0.67 F-layer log10TS(%); R2 = 0.80 This equation indicates that: 1. Cortinarius and Bankera are effective Hg accumulators, while Cantharellus is not (post-hoc zero-difference p-values < 0.0001). 2. Cap THg > stalk THg concentration (post-hoc zerodifference p-values < 0.0001). This is also in part due to a significant Cap TS > stalk TS difference (post-hoc zero-difference p-values < 0.0001). 3. Mushroom THg decreases by development stage (emergent > mature > senescent, with post-hoc zero difference p-values < 0.0001), except for Boletus edulis, Cortinarius armillatus, Cortinarius semisanguineus, and Xanthoconium separans, for which THg remains steady from emergence to senescence [51]. 4. Mushroom THg increases significantly for each species with increasing mushroom TS concentration (zero correlation p-value < 0.0001). 5. Mushroom THg increases with increasing F-layer THg and TC concentrations (zero-correlation p-value < 0.0001). 6. Mushroom THg increases with decreasing F-layer TS concentration (zero correlation p-value < 0.0001). Note that the above relationships for mushroom THg with increasing mushroom TS, F-layer THg and decreasing F-layer TS are similar to the regression results for moss THg. Furthermore, the changes in mushroom THg from stalk to cap, from emergence to senesce, and by species and genus are all, at least in part, related to corresponding changes in mushroom TS [51].

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3.4 Soil THg Mean soil THg concentrations varied as follows (Table 3): Beach gravel < Lagoon peat < Mud < Muck < Mineral soil < Bog peat < Forest floor Across the soil layers (Table 3), soil THg decreased from highest concentrations in the forest floor to lowest concentrations in the subsoil (post-hoc difference p–value < 0.0001) as follows: C < BC < B < Ae < Ah < L < F coast for L-layer THg, (ii) island > coast > inland for F-layer THg, and (iii) island > inland for H-layer THg. Reviewing the National Atmospheric Deposition Program (NADP) maps for wet atmospheric Hg deposition across the study area revealed that these differences cannot be discerned from monitoring precipitation events alone. The location-related differences would therefore be related to a combination of dry and gaseous atmospheric Hg deposition and absorption [1]. The following best-fitted multiple regression model (Appendix) addresses the combined location, moss, and soil layer, TS and TC concentration effects on soil THg concentration, as follows: Soil THg (ppb) = 160.8 + 89.5 F-layer + 137.1 × H-layer -10.9 layer thickness (cm) + 33.8 Location + 558.2 soil TS(%) + 58.3 Pleurozium + 44 Sphagnum -1.2 TC(%); R2 = 0.49 with (i) the island, coast, inland locations coded 1, 0 and -1, respectively, (ii) soils samples from the L-, F-, H- and A-layers each coded 1 when applicable, and 0 otherwise, (iii) and soil samples covered by mosses also coded 1 and 0 otherwise. In summary, this equation: 1. confirms the location effect such that soil THg (island) > soil THg (coast) > soil THg (inland); 2. indicates that Sphagnum and Pleurozium carpets each increase THg in the soil below (p-value < 0.0001), but for different reasons: slow-growing Pleurozium carpets would pass S and Hg into the underlying soil, while soil THg and TS underneath Sphagnum - 10.1515/bimo-2015-0008 Downloaded from De Gruyter Online at 09/15/2016 07:43:39AM via free access

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Table 3. Summary of soil THg concentrations (ppb, dw), by layer type.  

 

Substrate

THg, ppb

 

 

 

 

n

Mean

Min

Max

STDev

Beach gravel

4

2,9

2,5

3,3

0,5

Lagoon peat

12

11,6

6,6

15,8

3,9

Mineral sediments

14

19,8

7,1

31,7

9,1

Brackish sediments

4

8,6

7,1

10,0

1,7

Stream sediments

10

24,3

18,4

27,5

4,7

Organic sediments

4

51,1

38,8

63,4

14,2

Bog peat

10

168,1

123,1

262,0

50,1

Forest floor

518

214,0

12,3

817,8

123,4

L layer

211

141,0

19,4

535,7

80,4

F layer

272

259,8

12,3

817,8

120,2

H layer

35

298,9

86,5

616,0

138,2

Mineral soil

171

97,8

9,1

382,4

73,5

Ah,

60

144,6

16,2

363,5

69,3

Ae

81

83,8

12,6

382,4

65,5

Bf, Bm, BC, C

30

39,9

9,1

174,6

37,7

Tilla: outliers > 40 ppb removed

21

22,3

5,0

40,0

10,3

Tillb = Average of Bf, Bm, BC / 1.66 Till: estimated by assuming that THg/TC remains the same across subsoil (Table 3) Bedrocka a b

24,0 23,0  

 

 

 

 

8

2,4

0,2

3,5

1,0

Data source: Kejimkujik National Park, Nova Scotia [88]. Topsoil THg / subsoil THg = 1.66. Data source: Europe [89].

may simply increase due to lateral accumulation particulate and dissolved organic matter in mosscovered depressions; 3. implies that soil THg increases with soil TS (p-value < 0.0001), thereby confirming S as a soil-dominant Hg retention factor; 4. shows the trend of the relatively low THg concentrations within the L- and A-layers relative to the F- and H-layers (p-value < 0.0001); 5. indicates that THg concentrations increase with decreasing L-, F-, and/or H-layer thickness (posthoc zero p-value < 0.0001), with thinner L-, F-, and H-layers being the result of (a) higher organic matter decomposition and fermentation rates, and (b) with C losses occurring faster than the accompanying N, S and THg losses [90-92]; hence THg should be negatively correlated with TC, as reflected by the negative TC coefficient.

3.5 Estimating pool sizes and pool transference rates Table 4 provides a benchmark summary for the THg and TC pool sizes across the various forest vegetation and soil compartments, i.e., foliage, wood, roots, forest floor and soil layers. The pool values for tree biomass, moss carpets, mushrooms and fungal mycelia were obtained from the literature (Table 4, footnotes). For THg, the following pool size order was obtained: Mineral soil THg pool > forest floor THg > tree component THg (foliage, wood, bark, root) > moss carpet THg > mushroom and fungal mycelia THg. To generalize, this order would also apply to fully stocked, mature, deeply-rooted and coarse-fragment-free upland forest conditions in temperate to boreal climate

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Biomonitoring and assessing total mercury concentrations and pools in forested areas 

regimes on glaciated landforms. To specify further, these landforms would be underlain by siliceous bedrock formations, and the THg pools so estimated would not be affected by locally occurring surface exposures of Hg-containing sulfide deposits [53,105]. In addition, the Table 4 entries for the THg and TC pools can be adjusted to conform to local biomass (such as foliage, wood, roots) and soil (soil layer depths, bulk density, organic matter content, and coarse fragment content) specifications. For example, halving the depth of each soil layer in Table 4 would reduce the THg retention capacity of the soil from 560.9 to 280.5 g ha-1. Adjusting the coarse fragment content from 0 to 50% would further cut the soil-based THg retention capacity to 140.3 g ha-1. By modifying these specifications case-by-case, THg entries fall into the reported THg range for northern temperate-boreal forests and forest soils [25,26,106]. The THg input and output rates for the tree biomass, forest floor and combined mineral soil pools were estimated as follows: 1. The net atmospheric THg sequestration rate per year was set to equal the existing THg pool of the forest foliage, which would generally correspond to the combined annual litter and throughfall THg contributions, thereby estimated to amount to 170 mg ha-1 a-1. This value falls into the range of typical net atmospheric Hg sequestration rates for temperate upland deciduous and coniferous forests (see Ref. [4]. 2. Chemical weathering of bedrock minerals under temperate climates amounts to about 1.2 kg ha-1 with stream discharge rates at 100 cm a-1 [107]). This translates into a Hg release rate from soil and bedrock minerals of about 0.28 mg ha-1 a‑1 when THg = 23 ppb. 3. Forest floor leaching losses for Hg would amount to about 120 mg ha-1 a‑1, assuming an average dissolved organic matter concentration of 50 mg L-1, a forest floor leaching rate of 1000 mm a-1, and setting THg (ng L-1) = 0.86 DOC (mg L-1)0.67 [56, 108]. This corresponds to the 120−150 mg ha-1 a-1 estimates in [31]. 4. Stream-based Hg losses from upland forests, mediated by lateral transfer of dissolved organic matter and sediments from soil erosion amount to about 20 mg ha-1 a-1 [108,109]. 5. Biological and photochemically-induced Hg volatilization from forest soils varies from about 10 to 70 mg ha-1 a-1 (see also [4, 92]). Generally, these losses would decrease with increased shading and decreasing temperatures [49,110]. 6. Typically, other than fine-root THg, plant THg is not correlated with soil THg [65]. In addition, the transfer of Hg from soil to plant due to root uptake is

 55

generally low, and Hg hyper-accumulation by plants is rare, with, e.g., Chinese brake fern (Pteris vittata) being an exception [111]. While fungal mycelia do bioconcentrate some of the accumulated soil THg [8], most of that Hg remains in the soil. Only a small part of mycelium-accumulated Hg would be transferred to the fungal fruiting bodies, with some of that (i) taken up by mushroom-consuming organisms, or (ii) volatilized as part of mushroom decay. The remaining THg would return to the forest floor, and this would especially be so for mushrooms with high TS [8]. For the general purpose of quantifying THg pool sizes and transfer rates, Table 4 can therefore be used for: 1. Initializing vegetation, forest biomass and THg pools for the purpose of forest biomass and THg mass balance modelling. 2. Determining how vegetation, forest floor and soil mass, TC, and THg would generally vary based on soil profile, parent material, and forest cover specifications. 3. Estimating how much THg would be lost during and after, e.g., (i) forest fires affecting all of the above ground biomass and forest floor, and (ii) harvesting (wood exports only, (Fig. 3). 4. Estimating how much atmospheric Hg would be re-sequestered as forests re-grow towards maturity. 5. Estimating other related THg pool size. For example: Soil MeHg ≈ 0.001 Soil THg, and Forest floor MeHg ≈ 0.003 to 0.025 forest floor THg [118]. Earthworm THg (ppb) = 0.08 + 0.61 soil THg (ppb); 2 R = 0.35 [112] Earthworm MeHg (ppb) = 0.019 + 0.103 earthworm THg (ppb); R2 = 0.88 [112]. Mushroom MeHg(ppb) = (0.048 +/- 0.010) mushroom THg [112].

3.6 Separating soil THg into atmospheric and geogenic components The soil mass and TC pools for the 78 cm deep and coarse-fragment free soil in Table 4 amount to 11,670 and 163 metric tons ha-1, respectively. The corresponding THg pool amounts to 562 g ha-1. Assuming that the soil parent material is mostly derived from glacial till with THg = 23 ppb, then the geogenic THg pool (THggeo) would amount to 220 g ha-1. The portion of the atmospherically deposited and sequestered THg pool would then amount to THgatm = 344 g ha-1. Comparing this - 10.1515/bimo-2015-0008 Downloaded from De Gruyter Online at 09/15/2016 07:43:39AM via free access

56 

 M. Nasr, P.A. Arp

Table 4: A mixed-wood forest example for estimating representative values for soil and vegetation TC and THg concentrations and pools, by biomass compartment, and by soil and moss layer according to soil thickness and bulk density. Also shown: the estimated proportioning between the geogenic and atmosphere-sequestered THg pools (THggeo and THgatm, respectively), and the THgatm/THgfoliage and THg/TC ratios.  

Depth a Density a Masstotala

 

cm

g cm-3

TC

ton ha-1

%a

THg

ton ha-1

ppba

Massmin g ha-1

Thggeo

ton ha-1

THgatm i

g ha-1

THg / THgatm/TC THgfoliage ppm

Foliage

-

-

8

53.2d

4,3

20,9

0,17

-

-

0,17

1,0

0,039

Wood

-

-

100

52d

52,0

6,4

0,64

-

-

0,64

3,8

0,012

Bark

 

 

18

55

9,9

17,6

0,32

-

-

0,32

1,9

 

Coarse roots

-

-

24

50d

12,0

10

0,25

-

-

0,25

1,5

0,021

Fine roots ( THg (stalks), with THg decreasing with generally low TS values due to growth dilution and/or senescence-induced THg losses [8]. The best-fitted regression models (Appendix) captured 49 to 90% of the topsoil (forest floor and A-layers), moss and mushroom THg variations. Across these variations, moss and mushroom TS correlated positively with THg, but soil TS had a negative impact on moss and mushroom THg. A portion of these variations was also affected by location (i.e., THg island > THg coast > THg inland), likely due to fog-enhanced Hg sequestration immediately inland from steeply rising cliffs. The significance of this effect was, however, somewhat obscured by inconsistent and insufficient species and soil type representation per location. For general biomonitoring purposes, Usnea sp. are popular targets because they are ubiquitous, longlived, and can be sampled year-round with little effort. It is, however, difficult to quantify the year-by-year contributions of these organisms to the overall litter-based THg contributions of the forest floor. The same applies to assessing the litterfall contributions of many lichens species that grow on tree twigs, branches, and trunks. Collecting and analyzing coniferous foliage by age would be most helpful in determining how foliar sequestration of atmospheric Hg is progressing over a period of about 1 to 5 years after correcting for the foliar TS variations (also see [120]). Forest floor sampling provides another convenient target for monitoring and modelling THg concentrations and pool sizes in the THg accumulating L-, F- and H-layers. For location-specific and forest type comparisons, F-layer sampling would reveal significant trends more readily than the other layers because: (i) L-layers vary strongly in composition (ranging from foliage to coarse woody debris in variable amounts), and (ii) H- and A-layers often grade into each other through microsite variations in bio-physical mixing [121]. Monitoring the rates of litterfall and decay under field conditions through year-after-year placement of mesh fabrics on top of newly fallen and decaying litter layer at the end of the litterfall season would ascertain how much THg accumulates and would be lost from each mesh-separated layer succession. In this, attention needs to be given to mound versus pit sampling: mound sampling would produce more consistent results than pit sampling, because the samples from the latter would vary by the extent of lateral inflow and water pooling, and subsequent differences in overall litter accumulation and decomposition rates.

Using moss species as THg deposition and throughfall indicators also introduces a number of variables that are difficult to control because of abundance and species/ location variations in growth rates, shading, throughfall and litterfall. In this regard, slow-growing Pleurozium carpets would be best for monitoring moss-related THg uptake across locations with similar canopy closure and low litterfall, The monitoring of mushroom THg leads to further substrate- and time–dependent sampling complexities due to the varying relationship between THg and TS by species, stage of mushroom development, and mycelial growth and substrate preferences. For example, certain Boletus, Bankera and Cortinarius species would be good monitoring targets for mushroom uptake from soils because their stalk and cap THg remains relatively stable by development age, and their mycelial networks are longlived and extend across organic and mineral soil layers [8]. In contrast, Cantharellus species provide poor monitoring targets because their mushroom THg drops steadily from emergence to senescence, and their mycelial networks are short-ranging, short-lived, and mostly centered on readily digestible C substrates [51]. The above suggests that the soil build-up of atmospherically-deposited Hg occurs slowly over a thousand years or more in view of the relatively small layer-by-layer THg input and output rates. This slow but nevertheless persistent build-up would, as demonstrated, add to the originally geogenic THg pool. That particular pool would be higher or lower depending on soil depth and on the extent to which Hg-enriched minerals are present in the soil parent material. The extent to which the atmospherically-derived THg pool accumulates in soils would increase from open fields to fully stocked forests, and would be zero on ice- and snow-covered fields and terrain [106]. In summary, assessments similar to the above would complement and sharpen current efforts in monitoring and modelling terrestrial THg concentrations and pools in forests, soils and watersheds, as these would vary by geographically by local to regional rates in atmospheric Hg deposition, extent and type of vegetation cover, TS concentrations in vegetation components and soil layers, and local variations in forest biomass and soil profile. Acknowledgements: This work received support from NSERC via its Discovery and Collaborative Research Programs (COMERN, SFMN), and also from Environment Canada’s Clean Air Regulatory Agenda (CARA) project on mercury.

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Biomonitoring and assessing total mercury concentrations and pools in forested areas 

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Biomonitoring and assessing total mercury concentrations and pools in forested areas 

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Appendix. Case-study results [122]: Best-fitted multiple regression models for moss, mushroom and soil THg.

Dependent variable

Regression coefficient

SE

t-value

p value

R2

Partial correlation with dependent variable

206.6 −178.8

15.3 7.7

13.5 −23.3