Testate amoeba records indicate regional 20th-century lowering of water tables in ombrotrophic peatlands in central-northern Alberta, Canada
Running head: Recent apparent drying in Alberta peatlands
Simon van Bellen1,2*, Gabriel Magnan1,2, Lauren Davies3, Duane Froese3, Gillian Mullan-Boudreau1, Claudio Zaccone4, Michelle Garneau2,5, William Shotyk1
1Department of Renewable Resources, University of Alberta, Edmonton, Canada 2Geotop-Université du Québec à Montréal, Montreal, Canada
3Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Canada
4Department of the Sciences of Agriculture, Food and Environment, University of Foggia, Foggia, Italy
5Département de géographie, Université du Québec à Montréal, Montreal, Canada *Corresponding author: van_bellen.simon@uqam.ca; +1 514 742 8204
Keywords: Little Ice Age, water table, transfer function, oil sands, peat bog, functional trait, Sphagnum, permafrost
Paper type: Primary Research Article 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23
Abstract
Testate amoebae are abundant in the surface layers of northern peatlands. Analysis of their fossilized shell (test) assemblages allows for reconstructions of local water-table depths (WTD). We have reconstructed WTD dynamics for five peat cores from peatlands ranging in distance from the Athabasca bituminous sands (ABS) region in western Canada. Amoeba assemblages were combined with plant macrofossil records, acid-insoluble ash (AIA) fluxes and instrumental climate data to identify drivers for environmental change. Two functional traits of testate amoebae, mixotrophy and the tendency to integrate xenogenic mineral matter in test construction, were quantified to infer possible effects of AIA flux on testate amoeba presence. Age-depth models showed the sections each covered at least the last ~315 years, with some spanning the last
millennium. Testate amoeba assemblages were likely affected by permafrost
development in two of the peatlands, yet the most important shift in assemblages was detected after 1960 CE. This shift represents a significant apparent lowering of water tables in four out of five cores, with a mean drop of ~15 cm. Over the last 50 years, assemblages shifted towards more xerophilous taxa, a trend which was best explained by increasing Sphagnum s. Acutifolia and, to a lesser extent, mean summer temperature. This trend was most evident in the two cores from the sites located farthest away from the ABS region. AIA flux variations did not show a clear effect on mineral-agglutinating taxa, nor on S. s. Acutifolia presence. We therefore suggest the drying trend was forced by the establishment of S. s. Acutifolia, driven by enhanced productivity following regional warming. Such recent apparent drying of peatlands, which may only be 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46
reconstructed by appropriate indicators combined with high chronological control, may affect vulnerability to future burning and promote emissions of CO2.
Introduction
Testate amoebae are unicellular protists which are diverse and abundant in wet soils and especially in ombrotrophic peatlands, where they live in near-surface layers (Heal, 1962). They are considered ubiquitous (Finlay, Esteban, Clarke, & Olmo, 2001), resulting from an efficient dispersal, although some species are likely restricted to certain parts of the world (Foissner, 2006; Smith & Wilkinson, 2007). Upon burial in accumulating acidic and anoxic peat, theirshell (‘test’) remains generally well-preserved, even at millennial timescales. After identification to genus or species level, fossil assemblages of testate amoebae can therefore be used to reconstruct past environmental conditions (Charman & Warner, 1997). Many testate amoebae are predators on bacteria and fungi and accumulate silica in test construction, hence they play a major role in nutrient and silica cycling (Aoki, Hoshino, & Matsubara, 2007; Mitchell, Charman, & Warner, 2008). Finally, mixotrophic testate amoebae, which partly rely on photosynthesis, contribute to carbon sequestration and a decrease in abundance of such amoebae in Sphagnum peatlands, for instance due to climate warming, could lead to reduced carbon fixation (Jassey et al., 2015).
Testate amoebae are generally sensitive to peat moisture content and many studies have aimed to reconstruct past water-table levels in peatlands around the globe, by the use of 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69
transfer functions (Amesbury et al., 2016; Booth, 2008; Charman, Blundell, & Accrotelm members, 2007; Lamarre, Magnan, Garneau, & Boucher, 2013; Lamentowicz &
Mitchell, 2005; Swindles, Lamentowicz, Reczuga, & Galloway, 2016; van Bellen et al., 2014; Wilmshurst, Wiser, & Charman, 2003). Nevertheless, a range of environmental variables are known to be related to, and possibly directly affect testate amoebae, including pH (Charman & Warner, 1992; Lamentowicz & Mitchell, 2005), dust
deposition (Fiałkiewicz-Kozieł et al., 2015; Payne, 2012) and fire occurrence (Marcisz et al., 2015; Turner & Swindles, 2012). The identification of testate amoeba functional traits and the calculation of trait indices allow for inferring past changes in local water tables and other environmental conditions, such as disturbance events and light conditions (Fournier, Lara, Jassey, & Mitchell, 2015; Marcisz et al., 2016; Marcisz et al., 2014; van Bellen et al., 2017).
Here we present a study of testate amoeba assemblages from boreal peatlands of central and northern Alberta, Canada. Some of the peatlands in this vast region showed
discontinuous permafrost aggradation during the Little Ice Age (LIA), between 1550 and 1850 CE, generally followed by a well-documented, widespread degradation during the 20th century (Beilman, Vitt, & Halsey, 2001; Magnan et al., 2018; Vitt, Halsey, Bauer, & Campbell, 2000a). Permafrost peatlands may accumulate important amounts of organic carbon over long timespans, because decomposition is suppressed in frozen organic deposits. However, productivity needs to be sustained by sufficient moisture for plant growth (Swindles et al., 2015b; Tarnocai et al., 2009; Treat et al., 2016). Permafrost development may result in heaving of the upper layer, which provokes dry surface 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92
conditions and the establishment of trees, such as Picea mariana (Miller) BSP, lichens and Ericaceae under dry climatic conditions (Belland & Vitt, 1995; Zoltai & Tarnocai, 1971). In this case, the cycle of decadal to centennial scale permafrost development and degradation may have a net effect of reduction of the carbon sink (Lamarre, Garneau, & Asnong, 2012; Turetsky, Wieder, Vitt, Evans, & Scott, 2007). Generally, permafrost degradation is associated with enhanced emissions of methane, as organic matter becomes available for decay under wet, anaerobic conditions (Turetsky, Wieder, Vitt, Evans, & Scott, 2007). However, in the long term, rising water tables and climatic warming may stimulate productivity and thus enhance the accumulation of peat (Camill, Lynch, Clark, Adams, & Jordan, 2001; Swindles et al., 2015b). In the permafrost
peatlands of central Canada, climate warming is likely to have been a key mechanism for ecological and hydrological change during the second half of the 20th century, as mean annual temperatures increased with up to 0.5°C per decade (Camill, 2005).
As peatland surface moisture contents change with permafrost development and degradation, shifts in testate amoeba assemblages are likely during these processes (Lamarre, Garneau, & Asnong, 2012; Swindles et al., 2015c). During the LIA, palsa development in subarctic eastern Canada induced a shift toward a highly decayed, slowly accumulating peat with a dominance of the testate amoebae Difflugia pulex, Difflugia pristis type and Pseudodifflugia fulva type (Lamarre, Garneau, & Asnong, 2012). Shifts in testate amoeba communities in relation to permafrost development remain poorly documented and the specific micro-environmental variables that drive assemblages in such conditions are largely unknown. During the second half of the 20th century, the Fort 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115
McMurray region in northern Alberta underwent climatic warming as well as an important expansion of industrial activity, namely mining and upgrading of the Athabasca bituminous sands (ABS). Some of the studied peatlands are found in the vicinity of open pit bitumen mines and upgraders. These mines, and their associated tailings beaches and ponds as well as extensive network of gravel roads, generate large volumes of mineral dusts which is clearly seen in Sphagnum moss collected from these same sites (Mullan-Boudreau et al., 2017a). Studies of mineral matter in peat cores from these bogs reveal an increase in dust deposition over time since mining and upgrading began in 1967 CE, with impacts increasing with distance toward industry (Mullan-Boudreau et al., 2017b). Atmospheric deposition of mineral dusts, whether they are supplied by natural or anthropogenic sources, may affect testate amoeba communities and these effects may be identified using selected functional traits of the tests. For instance, testate amoebae which integrate mineral xenosomes in test construction may be more abundant under conditions of elevated mineral dust deposition rates (Fiałkiewicz-Kozieł et al., 2015; Lamentowicz et al., 2009) and therefore this functional trait may be linked with dust fluxes. The main genera of mineral-agglutinating testate amoebae include Difflugia, Heleopera, Cyclopyxis, Centropyxis and Trigonopyxis. A second functional trait which may be linked with dust deposition is mixotrophy, defined as the ability to live in symbiosis with green algae, which may provide an additional food source through photosynthesis when prey is rare (Jassey et al., 2013). Enhanced inputs of atmospheric dusts are likely to limit potential for mixotrophic taxa, which have been reported to be sensitive to disturbance in a broader sense, such as drainage and fire (Marcisz et al., 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137
2016). The main mixotrophic taxa include Archerella flavum, Heleopera sphagni, Hyalosphenia papilio and Placocista spinosa.
We aimed to reconstruct environmental conditions and water-table dynamics of northern Alberta peatlands for the last millennium using testate amoeba records combined with a transfer function (Lamarre, Magnan, Garneau, & Boucher, 2013), testate amoeba
functional traits and measures of environmental variables. In addition, we aimed to verify to which extent variations in water tables and testate amoeba assemblages corresponded with changes in climate and other environmental variables based on the identification of permafrost episodes and 20th century vegetation changes from the same peat records (Magnan et al., 2018). We hypothesized that testate amoeba assemblages responded to three particular periods of environmental change, which were 1) the LIA cooling, associated with permafrost development in some peatlands of the region (Magnan et al., 2018; Vitt, Halsey, & Zoltai, 2000b), 2) the 20th century warming and 3) the presence of anthropogenic activity, causing elevated emissions of mineral dust in the ABS sites. The use of multiple records, located at variable distance to industrial activity, allowed us to estimate the relative importance of these three events, and to identify the nature of forcing factors.
Study region
Peat cores were collected from five ombrotrophic peatlands, three of which are part of the ABS region near Fort McMurray: McKay (McK), JPH4 and Mildred (MIL). Anzac 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160
(ANZ) is located 45 km southeast of Fort McMurray, while Utikuma (UTK) bog is located 264 km southwest of this region (Figure 1). All peatlands are Sphagnum-P. mariana bogs with a high presence of ericaceous shrubs, including Chamaedaphne calyculata (L.) Moench and Rhododendron groenlandicum (Oeder) Kron & Judd.
Fort McMurray has a continental climate with a mean annual temperature of 1.0°C, ranging from −17.4°C in January to 17.1°C in July and a mean annual precipitation of 419 mm, of which 32% falls as snow (1981-2010 data; Environment Canada, 2015). UTK bog has a mean annual temperature of ~2.0°C (-13.5°C to 16.2°C) and ~480 mm of precipitation annually (Slave Lake weather station; Environment Canada, 2015). The ABS region is located at the transition from the region of localized permafrost to the region of discontinuous permafrost (Beilman, Vitt, & Halsey, 2001; Vitt, Halsey, & Zoltai, 1994). A regional increase in mean summer temperature (MST) of ~2.0°C since 1950 CE (Adjusted and Homogenized Canadian Climate Data; Vincent et al., 2012, downloaded from Environment and Climate Change Canada) contributed to a gradual permafrost degradation, the extent of which was estimated at 26-50% of the permafrost extent having disappeared by 2000 CE (Vitt, Halsey, & Zoltai, 2000b). Remaining permafrost is prone to ongoing thawing as climate warming continues in the decades to come (Beilman, Vitt, & Halsey, 2001; Vitt, Halsey, & Zoltai, 2000b).
Permafrost conditions developed during the LIA (Halsey, Vitt, & Zoltai, 1995) and were identified specifically in ANZ and UTK cores by Magnan et al. (2018), based on a typical succession of highly decomposed, dense ligneous peat, often with abundant Picea
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needles, overlain by Sphagnum riparium and sedge peat, reflecting the formation of an internal lawn (Turetsky, 2004), and finally Sphagnum angustifolium and Sphagnum fuscum (Vitt, Halsey, & Zoltai, 1994). When permafrost conditions persist over decades to centuries, palsa and permafrost plateaus may develop. These features are often
associated with a very slow accumulation of peat overlying the frozen section (Lamarre, Garneau, & Asnong, 2012; Robinson & Moore, 2000).
Materials and methods
Sampling
Peat monoliths (100⨯15⨯15 cm) were retrieved using a modified Wardenaar sampler (Wardenaar, 1987) from permafrost-free locations. All cores were sampled from Sphagnum-dominated lawns, at intermediate elevation within the ecosystem’s
microtopographical range. The cores were wrapped in polyethylene cling film and packed into wooden boxes in the field. In the laboratory, cores were frozen at -18°C before being cut into ~1-cm slices using a stainless-steel band saw and polypropylene cutting table. The edges (~1 cm) were trimmed away from each slice.
Chronologies
Peat core chronologies were constructed using data from three techniques: AMS 14C dates, 210Pb profiles, and a cryptotephra isochron from a 20th century eruption. These three 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206
methods were compared to identify any chronological offsets and combined to produce a final Bayesian age-depth model with increased precision. Full details on sample selection strategies and modelling can be found in Davies et al. (accepted).
A total of 51 AMS 14C dates (9-11 dates per core) were measured from identified plant macrofossils, including samples dated using the atmospheric bomb-pulse curve. The unknown 14C ages were calibrated using Bomb13NH1 (Hua, Barbetti, & Rakowski, 2013) and IntCal13 (Reimer et al., 2013) calibration curves as appropriate with Oxcal v4.2 (Bronk Ramsey, 2009). 210Pb profiles were constructed using measurements from each sample of the upper-core segments (~20-50 cm depth). Ages were calculated using the Constant Rate of Supply Model (Appleby & Oldfield, 1978) and validated where possible using peaks in artificial radionuclides for the 1963 CE depth (137Cs, 241Am). Composite Bayesian age-depth models for each core were produced in OxCal v4.2 using the Poisson process model (P_Sequence; Bronk Ramsey, 2008; Bronk Ramsey, 2009). These models include boundaries at depths where potential significant changes in peat accumulation or preservation are identified from supporting environmental proxies (e.g. peatland succession, local fire and burning of organic matter or permafrost development; Magnan et al., 2018). The boundaries allow a change in modelled peat accumulation rates if it best fits the data surrounding the specified boundary depth and produce more realistic results where peat accumulation and preservation is not uniform.
Testate amoeba analysis 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228
Testate amoeba sample preparation roughly followed the protocol described by Booth, Lamentowicz, & Charman (2010). All preparations were performed on 1-cm3
subsamples, which were brought to a gentle boil in water and sieved over 212-m and 15-m mesh to eliminate a maximum amount of organic matter while keeping most, if not all, tests. Tests were identified and counted using a transmitted light microscope at ⨯400 magnification to a minimum count of 100 specimens (Payne & Mitchell, 2008). To identify taxa, the key developed by Charman, Hendon, & Woodland (2000) was
primarily used, but adaptations by Booth (2008) were followed as well. Centropyxis ecornis and Centropyixs laevigata were regrouped as C. orbicularis type and Centropyxis cassis was merged with C. aerophila type according to Mitchell (2002). Taxon
abundance was expressed as a percentage of the total count. Species richness was quantified by the number of species using rarefaction curves, standardized to 100
specimens to account for small differences in count totals, using the Vegan 2.2-1 package (Oksanen et al., 2015) in R 3.3.2 (R Core Team, 2016). Three cores, MIL, UTK and McK were analyzed at 1-cm intervals, while ANZ and JPH4 were generally analyzed at 2-cm intervals, except for some sections which had contiguous analyses because of lower apparent rates of peat accumulation.
Reconstructions based on testate amoebae
Constrained hierarchical clustering was applied to each core separately to identify distinct testate amoeba assemblages, with clusters constrained by sample order, using the chclust function of the rioja package (Juggins, 2015) in R 3.3.2 (R Core Team, 2016). Prior to 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251
these analyses, testate amoeba assemblages were logarithmically transformed. A testate amoeba transfer function for inferring water-table levels is not available for the ABS region, hence a transfer function from eastern Canada, which included samples from a permafrost (palsa) peatland, was applied to the assemblages (Lamarre, Magnan, Garneau, & Boucher, 2013), hereafter referred to as ECTF. Many testate amoeba taxa show similar water-table optima in transfer functions from different regions and continents which may justify the use of transfer functions trained on surface data from relatively remote regions (Amesbury et al., 2016). For instance, common taxa such as A. flavum and Difflugia globulosa type are generally hydrophilous, while Assulina muscorum and Trigonopyxis arcula are xerophilous according to various transfer functions (Amesbury et al., 2016; Booth, 2008; Charman, Blundell, & Accrotelm members, 2007; Lamarre, Magnan, Garneau, & Boucher, 2013; Lamentowicz & Mitchell, 2005). Following recent recommendations (Amesbury et al., 2016; Swindles et al., 2015a; Turner, Swindles, Charman, & Blundell, 2013), variability in reconstructed water-table depth (WTD) was quantified as anomalies, relative to the most recent quantified value, with high, positive numbers indicating deeper water tables and negative numbers representing shallower water tables.
In addition to inferences from a transfer function, we quantified two functional traits of testate amoebae which may provide additional information on how dust fluxes may have affected these communities. These traits included mineral matter presence on tests, quantified as either presence or absence, and the ability to feed through mixotrophy. These traits were quantified for each taxon and the weighted average for each functional 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274
trait was calculated for each sample based on the relative abundance (%) of each taxon within that sample and expressed as community-weighted means (CWMs) (Ricotta & Moretti, 2011).
Non-metric multidimensional scaling (NMDS) was performed on testate amoeba assemblages to explore assemblage composition among cores and their subsections. NMDS was performed using the Bray–Curtis dissimilarity index on pooled data and cores separately, with Canoco 5 software (Ter Braak & Šmilauer, 2012). Partial
redundancy analyses were used to identify potential effects of environmental variables on testate amoeba assemblages. Permutation tests allowed to verify significance of canonical axes, based on 9999 permutations. Finally, multiple regression, using environmental variables as predictors, was performed on each core to identify potential combined effects on past WTD anomalies directly.
Bulk density and acid-insoluble ash
Bulk density (g cm-3) was measured on contiguous 1-cm3 subsamples in each core after drying overnight at 105°C (Chambers, Beilman, & Yu, 2010). Ash content (%) was measured after the dried peat samples were combusted at 550C for 16 hours in a muffle furnace (Andrejko, Fiene, & Cohen, 1983). Acid-insoluble ash (AIA) was used as a proxy for dust deposition and was determined quantitatively after reaction of ash samples in 1M HCl for 15 minutes, followed by filtering under vacuum to recover the insoluble 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296
fraction (Mullan-Boudreau et al., 2017b). The AIA flux (g m-2 yr-1) was quantified using the peat accumulation rates as obtained from the age-depth modelling.
Results
Age-depth models were obtained by combining AMS 14C dates, 210Pb profiles, and a cryptotephra layer. The models showed an apparent increase in accumulation rates at the top section of each core, which is mainly the result of incomplete decay of the oxic layer (Figures S1-S5). Downcore variability in vertical accumulation rates were observed, which were mainly associated with shifts in local vegetation (Magnan et al., 2018). For instance, the plateau in the core from ANZ (Figure S4) was associated with the local development of permafrost during the LIA. Further details on the chronologies can be found in Davies et al. (accepted).
Testate amoeba records
All testate amoeba records covered the period 1700-2013 CE with McK extending back to 920 CE. The 211 samples from five cores contained a total of 58 different taxa from 22 genera. After rarefaction to 100 specimens, mean species richness for each core varied between 10 (UTK) and 16 (JPH4). The most frequently observed taxa were D. pristis type (11.8%), A. flavum (10.3%) and A. muscorum (9.3%).
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McK core
Testate amoeba assemblages for this core, subdivided in seven zones and covering the period 920-2013 CE, were characterized by important variability (Figure 2). Water tables were relatively high between 920 CE and 1860 CE, with assemblages dominated by A. flavum, Arcella catinus type and D. pristis type. After 1860 CE, a rapid succession of Phryganella acropodia, D. pristis type, Nebela militaris, T. arcula, Trigonopyxis minuta and A. muscorum was reconstructed and water tables fluctuated until the second half of the 20th century followed by a marked apparent drop, i.e. relative to the surface, in the early 1990s. A strong increase in AIA flux, from <2 g m-2 yr-1 in 1976 CE up to 10-12 g m-2 yr-1 in the 21st century (Mullan-Boudreau et al., 2017b), characterized the top of the sequence. The increase in AIA flux did not have the hypothesized effect on testate amoeba assemblages as mineral matter CWMs decreased around 1960 CE and
mixotrophic taxa were virtually absent since the start of the 20th century.
JPH4 core
The deeper section of the JPH4 core (1360-1490 CE) showed relatively high water tables, inferred by the dominance of P. acropodia (Figure 2). A dry phase (1490-1630 CE) with T. arcula as most abundant taxon was followed by an increase in water-table levels as D. pristis type became dominant. As in the other cores, major shifts in assemblages occurred at the top of the core, with a slight dry shift during the 20th century. N. militaris became 320 321 322 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342
the most abundant taxon, while AIA fluxes culminated at the top of the sequence at 19 g m-2 yr-1 in 2006 CE. Mixotrophic taxa were very rare throughout the sequence and mineral matter CWMs decreased as AIA fluxes increased towards the top of the core.
MIL core
As McK, the MIL record is characterized by a high diversity in testate amoeba taxa (Figure 2). The lower 12 cm of the core, representing the period between 1700 and 1916 CE, showed high bulk density at >0.1 g cm-3, which suggests, in combination with a low AIA flux, the presence of highly decomposed peat. Dominant testate amoebae are Trigonopyxis spp., A. catinus type, D. pristis type, Centropyxis platystoma type and A. muscorum. After 1994 CE, A. muscorum became dominant, indicating a sharp drop in water-table levels, with a minor presence of C. orbicularis type. The top section of the core showed the greatest variability in taxa and among the highest AIA fluxes of all the sequences studied here, with a maximum AIA flux of 38 g m-2 yr-1 in 2003 CE. As in McK, however, an effect on mineral matter CWMs was not detected as mineral matter CWMs remained stable during this period. Mineral matter CWMs were also higher in the last millennium, when AIA fluxes were well below 5 g m-2 yr-1. Mixotrophic taxa were very rare throughout the core.
ANZ core 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365
The core from ANZ showed an initial dominance of A. flavum with Diffugia lucida type and D. pristis type (Figure 2) between 990 and 1700 CE. Between 1700 and 1989 CE, important shifts in assemblages and high rates of change were observed, with an alternance of D. pristis type, Arcella discoides, A. muscorum, T. arcula and A. flavum dominance, followed by a lowering of the water table. Past permafrost levels, dated between 1700 and 1956 CE, were characterized by dominance of D. pristis type and A. catinus type. Although the relative abundance of mineral matter CWMs increased strongly under permafrost conditions, there was no apparent linkage with AIA flux, which remained stable but reached its maximum in 1960 CE. Mixotrophic taxa, which were general in the entire sequence, disappeared when permafrost developed. The return of high accumulation rates after 1960 CE coincided with a return of mixotrophic A. flavum and the appearance of H. papilio, N. militaris and Hyalosphenia elegans. From 1977 CE onwards, the water table started lowering, attaining greatest depth during the last decade.
UTK core
The assemblages at the base of UTK were dominated by D. lucida type between 1240 and 1960 CE. Between 1840 and 1960 CE, D. pristis type and D. pulex became equally dominant, coinciding with local permafrost conditions (Magnan et al., 2018). Inferred water tables did not suggest important drying associated with permafrost development. The greatest AIA fluxes were registered between 1983 and 1992 CE, but these were modest (2-4 g m-2 yr-1) when compared with the flux values obtained from the other peat 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388
cores. After permafrost degradation, around 1970 CE, mixotrophy CWMs increased rapidly and remained high until 1989 CE. This period was followed by a dominance of A. muscorum and Trigonopyxis spp., which suggests an important drying trend since the 1990s. No near-surface increase in AIA flux was registered at UTK.
Spatial and temporal trends
NMDS of the entire dataset was performed to explore spatial and temporal trends in amoeba assemblages. NMDS axis 1 showed a separation of xerophilous taxa of the order Euglyphida, including Trinema, Corythion and Euglypha, Assulina spp., Hyalosphenia minuta and Trigonopyxis spp. at the positive end, and relatively hydrophilous taxa, such as A. flavum, at the negative end (Figure 3). Taxon assemblages show important overlap among sites, but distinct differences in assemblages were evident when samples,
identified by period, were plotted in the same space. The separation of assemblages pre- and post-1960 CE showed that the major variability in assemblages was temporal, rather than spatial (Figure 3). Even though permafrost-associated assemblages were relatively well-grouped within the ordination, they did not show a markedly different composition than non-permafrost assemblages.
Major changes in testate amoeba assemblages occurred during the second half of the 20th century. In addition to a clear shift in testate amoeba assemblages, clear trends in amoeba functional trait CWMs were found with lower mineral matter CWMs during the second 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411
half of the 20th century in all cores, and decreasing mixotrophy CWMs in McK and JPH4 but increasing numbers of mixotrophs in ANZ and UTK (Figure 4). Inferred WTD show a general apparent drop in water tables after 1960 CE in all cores, except ANZ, possibly because this period coincided with permafrost thawing in ANZ. Both ANZ and UTK showed a significant increase in species richness post-1960, whereas McK, MIL and JPH4 had a higher AIA flux.
Overall, UTK and ANZ had lower AIA fluxes and bulk density values and less mineral particle-agglutinating, but more mixotrophic taxa, which may be interpreted as typical undisturbed ombrotrophic peatland conditions; these are likely characterized by limited availability of nutrient elements and low rates of organic matter decay. The peat cores from MIL, JPH4 and McK yielded greater fluxes of AIA and harboured more mineral-agglutinating and very few, if any, mixotrophic taxa. After 1960 CE, differences between sites decreased, with MIL, JPH4 and McK switching towards a contemporary vegetation dominated by Sphagnum section Acutifolia (mainly S. fuscum), which is typical for ombrotrophic conditions as found in the bogs of the region today (Magnan et al., 2018).
Discussion
Peatland development before the 20th century 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433
The five sites followed different pathways towards their present state of ombrotrophic peatlands (Magnan et al., 2018). Throughout its history until the late-20th century, MIL evolved as a treed, minerotrophic fen, JPH4 became an ombrotrophic bog around 1530 CE and McK showed a sequence that accumulated under dry, ombrotrophic conditions after 1790 CE. The coring sites of ANZ and UTK, both located south of the Fort McMurray region, developed under ombrotrophic conditions during the last millennium. No clear, common trend in testate amoeba assemblages or inferred water-table levels between cores, e.g. as forced by climate change, was identified before the second half of the 20th century. This may be explained by the differences in ecosystem state prior to the 20th century, which caused differences in ecosystem sensitivity to external forcing.
The effect of LIA cooling, and related permafrost development, was identified in the cores from ANZ and UTK, mainly by the analysis of plant macrofossils and peat composition (Magnan et al., 2018). The sections corresponding to past permafrost conditions were dominated by D. pristis type, which has an intermediate position along the range in water-table optima of the ECTF (Lamarre, Magnan, Garneau, & Boucher, 2013), and the disappearance of mixotrophs (Figure 2). The abundance of D. pristis type and the absence of typical xerophilous taxa suggest that water tables did not drop
importantly relative to the surface when permafrost established, possibly reflecting a limited intensity of freezing and uplift. The absence of an apparent drop in water tables may also be explained by very low vertical accumulation rates during this period (Figure S2). Thawing of permafrost, dated around 1965 CE in both sites, coincided with the most 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454 455 456
important shifts in testate amoeba assemblages of the last millennium. Both sites showed a shift from mineral matter-agglutinating taxa towards mixotrophs while AIA fluxes peaked in ANZ. This increase in AIA flux may be explained by a re-mobilization of dust from frozen layers after thawing. The establishment of S. s. Acutifolia after thawing in both sites (Magnan et al., 2018) may have positively influenced the presence of
mixotrophic taxa, especially A. flavum, which appears to thrive under increasingly acidic and ombrotrophic conditions (Fournier, Lara, Jassey, & Mitchell, 2015). However, permafrost thawing per se was not a driving factor for this change as McK and MIL, which did not show signs of past permafrost, recorded important shifts during the mid-20th century as well.
20th century environmental change
Our data show important environmental change at the regional scale around the mid-20th century. NMDS ordinations suggested that the main shift in testate amoeba assemblages was associated with an increasing dominance of mainly xerophilous Euglyphida, as opposed to Arcellinida and Amphitremida. Euglyphida are dominant in successional stages (Laggoun-Défarge et al., 2008), they may be considered r-strategists (Beyens, Ledeganck, Graae, & Nijs, 2009) and they may be better adapted to unstable conditions as they dominate through rapid recolonization (Fournier, Malysheva, Mazei, Moretti, & Mitchell, 2012). Euglyphida may also benefit from an abundance of bacteria, as they are generally bacterivorous (Gilbert, Amblard, Bourdier, André-Jean, & Mitchell, 2000; 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479
Lara, Heger, Mitchell, Meisterfeld, & Ekelund, 2007). Many of these taxa (Assulina, Trinema and some Euglypha) are xerophilous and the relative abundance of bacteria under dry conditions in temperate, ombrotrophic peatlands (Fenner, Freeman, &
Reynolds, 2005) may explain their dominance here. All sites showed a lowering of water tables, on average ~15 cm (σ = 6 cm) since 1960 CE (Figure 5).
To verify the validity of the WTD reconstructions we applied a second transfer function to the data, which was trained on samples from subarctic Sweden, including permafrost sites (Swindles et al., 2015c), hereafter referred to as STF. WTD reconstructions obtained using the ECTF (Lamarre, Magnan, Garneau, & Boucher, 2013) correlated reasonably well with those from the STF (Swindles et al., 2015c), with a Spearman's rank correlation coefficient rs of 0.67 (p < 0.0001) for the pooled, raw data (Figure S6). Correlation
coefficients varied between 0.34 and 0.90 and were significant (p < 0.05) for all cores except JPH4 (p = 0.13) and highest in UTK core (rs = 0.81) (Figures S7-S11). Both
transfer functions associate D. pristis type, which appeared characteristic for permafrost-affected levels in northern Alberta, with intermediate WTD. Discrepancies in WTD optima were notably found for A. discoides, which had wetter optima according to STF compared to ECTF, while a high abundance of D. lucida type and P. acropodia in samples resulted in drier reconstructions according to STF. Major differences were obtained for the ANZ core during the mid-20th century, which were much drier according to ECTF when compared to the STF reconstruction. Plant macrofossils, showing a presence of ligneous peat, high bulk density and C:N ratios of <80 (Magnan et al., 2018) indicated these levels were likely much drier than the ones overlying them, which 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494 495 496 497 498 499 500 501 502
demonstrates that the ECTF may be more appropriate for WTD reconstructions in the northern Alberta peatlands. The timing and intensity of the recent apparent lowering of water tables was replicated by the STF for all cores, except the JPH4 core.
After 1960 CE, the various peatland types, including a forested minerotrophic fen (MIL), poor fens and ombrotrophic bogs with past permafrost (ANZ and UTK), all converged towards ombrotrophic conditions, dominated by S. s. Acutifolia (often S. fuscum). The apparent drying trend coincided with important climatic warming: an increase in mean summer temperature (MST) on the order of ~2.0°C was registered in the region since 1950 CE (Adjusted and Homogenized Canadian Climate Data; Vincent et al., 2012, downloaded from Environment and Climate Change Canada). In addition, all cores showed low AIA fluxes in the first half of the 20th century (< 8 g m-2 yr-1) but strongly increasing values in the peat cores from the ABS sites (McK, JPH4 and MIL) after 1960 CE (Figure 4). Given the location and the timing of the increase, there is little doubt that this trend in AIA flux is linked with the industrial activity of the ABS (Mullan-Boudreau et al., 2017a; Mullan-Boudreau et al., 2017b). This attribution of dust sources is
supported as well by elevated thorium (Th) concentrations, reflecting the abundance of insoluble mineral particles, attaining 0.40 mg kg-1 in JPH4, 0.38 mg kg-1 in McK and 0.34 mg kg-1 in MIL. Much lower concentrations were found at ANZ (0.07) and UTK (0.09), which are located further from industrial sources of dust (Shotyk et al., 2017). Finally, environmental change was also reflected by a shift in local vegetation: all sites showed an increasing presence of S. s. Acutifolia (mainly S. fuscum) during the 20th century, with the main shifts occurring between 1950 and 1990 CE (Magnan et al., 2018). All these
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changes, as well as interactions between potential forcings, need to be taken into account to elucidate the changes in testate amoeba assemblages.
The nearly-annual resolution of our reconstructions for the last 80 years allows for correlations with instrumental climate data to verify possible linkages between climate variables, vegetation and water-table dynamics. We performed partial redundancy analyses, including MST, mean summer precipitation (MSP), a reconstruction of the summer (May-September) Palmer Drought Severity Index (s-PDSI) and S. s. Acutifolia presence (%) on testate amoeba assemblages, as well as multiple regression analyses on inferred WTD using the same predictors. The PDSI is a standardized measure of surface moisture conditions, based on both precipitation and surface air temperature. The s-PDSI reconstruction was calculated based on monthly self-calibrated PDSI using Penman-Monteith PE (Dai, 2011; data downloaded from ftp://aspen.atmos.albany.edu/DaiPDSI/). Given the fact that testate amoeba samples each represent one up to several years of water-table dynamics (Booth, 2010), the climate variable averages and s-PDSI values to be used in the analyses were calculated taking into account the age span of each sample, as obtained from the age-depth model. The AIA flux could not be included in the analyses, because data on these fluxes was too sparse. Partial redundancy analyses showed that S. s. Acutifolia was the only significant predictor of variations in testate amoeba assemblages in the records from ANZ and UTK (Table 1). MST and MSP were never significant predictors for individual sites when the effect of S. s. Acutifolia was taken into account.
526 527 528 529 530 531 532 533 534 535 536 537 538 539 540 541 542 543 544 545 546 547 548
In a second step, we tested the effects of MST, MSP, s-PDSI and S. s. Acutifolia presence (%) on the WTD anomalies (cm) using multiple regression and forward selection of variables using a stepwise approach (Table 2). For the entire dataset, i.e. all sites combined, S. s. Acutifolia presence was the only significant predictor (p < 0.05), which explained 14% of the variability in WTD. As expected, S. s. Acutifolia was positively correlated with WTD, i.e. lower water tables were associated with higher presence of S. s. Acutifolia. When the sites of the ABS (McK, JPH4 and MIL) were excluded, S. s.
Acutifolia explained best the variability in WTD, at 18%. In the ABS sites, MST was a poor, but significant predictor, but best predictors were different for the cores from McK (s-PDSI, R2 = 0.27) and MIL (S. s. Acutifolia, R2 = 0.51). No significant predictors were
identified for JPH4, which may be due to the low number of observations.
The results of partial redundancy analyses and multiple regression show that, for the 1930-2013 period, the testate amoeba assemblages were most strongly linked to local vegetation in the cores from ANZ and UTK, located farthest away from the ABS region, and in MIL. At the ABS sites, the drying trend was slightly better predicted by MST than by S. s. Acutifolia presence, but predictors were either not or weakly significant. Thus, in the ABS region, changes in amoeba assemblages were not clearly linked to trends in either climate or vegetation. Increasing AIA fluxes would be an alternative explanation for the identified shifts in amoeba assemblages in the ABS area. Potential influence of increasing AIA fluxes on testate amoeba assemblages and associated WTD
reconstructions could only be estimated visually, because AIA flux reconstructions were 549 550 551 552 553 554 555 556 557 558 559 560 561 562 563 564 565 566 567 568 569 570 571
sparse and did not always correspond to the levels for which testate amoebae were analyzed. In the core from MIL, S. s. Acutifolia abundance increased in the 1950s, before the development of the ABS and well before AIA flux culminated around 2000 CE. Similarly, in the core from McK, S. s. Acutifolia became dominant during the 1970s, while the local AIA flux remained below 5 g m-2 yr-1 until 2000 CE. These trends, and the fact that S. s. Acutifolia established in a similar way in ANZ and UTK, which were both not subjected to elevated dust fluxes, suggest that both S. s. Acutifolia establishment and the drop in water tables were independent of the increases in AIA flux. Instead, these were likely driven by a common variable, acting at a wider spatial scale, such as the increase in summer temperature (Figure 5). However, S. s. Acutifolia and the apparent drop in water tables may be mutually related as well. Increasing summer temperatures may have facilitated the establishment and expansion of S. fuscum since 1960 CE by relieving a cold stress on productivity (Gunnarsson, 2005; Loisel, Gallego-Sala, & Yu, 2012), in addition to enhanced primary productivity which may be linked with permafrost thaw at ANZ and UTK (Camill, Lynch, Clark, Adams, & Jordan, 2001). A hypothesized increase in plant productivity would likely have contributed to the observed apparent lowering of water tables: enhanced litter production results in an acceleration of peat accumulation, attaining a rate which may exceed the potential rate of water-table rise, thus causing the apparent drying trend. WTD may remain stable for some time as hydraulic conductivity, and therefore lateral drainage potential, remains high, yet this mechanism is also strongly linked to the surface topography (Belyea & Clymo, 2001). Only after the state of decay of the peat at the bottom of the oxic layer increases, may the water tables rise relative to the surface. Although we hypothesize that climate was the 572 573 574 575 576 577 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594
dominant factor for both S. s. Acutifolia expansion and the apparent lowering of water tables, we do not exclude the possibility that the enhanced AIA flux contributed to Sphagnum productivity in the three ABS sites. Wieder et al. (2016) found S. fuscum productivity and vertical growth was greater between 2009 and 2014 CE at sites in proximity of the ABS, possibly related to enhanced mineral deposition. However, the relative contributions of enhanced N, P, Ca and Mg deposition to this trend remained unclear. Wieder et al. (2016) found no significant relationship between temperature and Sphagnum productivity, possibly because productivity was limited by a moisture deficit, causing a desiccation stress between 2009 and 2014 CE.
Testate amoeba traits and environmental conditions
Unlike previous findings (e. g. Fiałkiewicz-Kozieł et al., 2015), our results do not support a relationship between dust (AIA) flux and the presence of mineral-agglutinating testate amoebae. Mineral matter CWMs were significantly greater at all sites during the pre-1960 CE period, while AIA flux was significantly greater in the three sites closest to the ABS activity after 1960 CE (Figure 4). Recent inputs of mineral dusts from open pit mines, tailings and roads may have supplied the bogs with mineral particles in size ranges that are unsuitable for test construction: the most common particle sizes incorporated by testate amoebae are on the order of 5-10 µm in diameter (Armynot du Châtelet, Bernard, Delaine, Potdevin, & Gilbert, 2015), whereas the dust being generated in the ABS region is dominated by coarse-grained beach and dune sands (Mullan-Boudreau et al., 2017a). Nevertheless, the decrease in the abundance of mineral-agglutinating taxa post-1960 CE 595 596 597 598 599 600 601 602 603 604 605 606 607 608 609 610 611 612 613 614 615 616 617
was also evident in the remote sites and therefore this trend cannot be strictly linked to changes in dust deposition. The shift in mineral matter CWMs is related with the
colonization by A. muscorum, Trinema spp., Corythion dubium and N. militaris, which do not use mineral matter in test construction. Trinema spp. and C. dubium, as most
Euglyphida, rely mainly on bacterivory. These testate amoebae are relatively small and are often preyed upon by taller taxa (Gilbert, Amblard, Bourdier, André-Jean, & Mitchell, 2000). Given their limited size, they may also be too small to effectively use and benefit from the availability of mineral particles. As data on bacteria abundance are lacking for our sites, we hypothesize the abundance of Euglyphida may be partly
explained by a possible increase in available bacteria, by the absence of other predators, or as discussed above, by morphological advantages that allow them to dominate in successional stages. A more detailed characterization of the size and mineral composition of the dust may allow a better understanding of the impacts of dust deposition on testate amoeba assemblages in this region.
Mixotrophic amoebae were generally absent when the AIA flux exceeded 5 g m-2 yr-1 and were much more abundant in the peat cores from ANZ and UTK. The establishment of permafrost conditions in the core from ANZ coincided with the disappearance of mixotrophs. During this period, accumulation of peat was extremely reduced, and the relatively constant input of dust, as reflected by the AIA flux (Figure 2c), on this stable surface may have increased the amount of nutrients available for microbial life to
develop. Heterotrophic testate amoebae may then have been able to feed on increasingly available prey, thus outcompeting the mixotrophs. These trends confirm the prevalence of mixotrophic amoebae in nutrient-poor, acidic conditions, characterized by low rates of 618 619 620 621 622 623 624 625 626 627 628 629 630 631 632 633 634 635 636 637 638 639 640
dust deposition which may allow mixotrophs to outcompete heterotrophs by relying on photosynthesis when prey is scarce.
Climate change and perspectives on carbon balance
To our knowledge, no other detailed peatland water-table reconstructions are available for this region, but model hindcasts suggested late-20th century warming was a driver for drying in wetlands in southeastern Alberta and southern Saskatchewan (Werner, Johnson, & Guntenspergen, 2013). In addition, three lake level records from east-central Alberta, obtained from lakes varying in size between 5 and 7 km2, show levels have declined ~4 m in depth in a very uniform trend since the mid-1970s (Donahue, 2006; van der Kamp, Keir, & Evans, 2008). Donahue (2006) ascribed the change observed in Muriel Lake to a likely combination of climatic change and land-use changes.
Our results suggest that the 20th century represented the most important regional-scale shift in peatland hydrology and ecology of the last millennium in the Fort McMurray region. Enhanced warming, causing an increase in the length and the intensity of the growing season, may have relieved constraints on Sphagnum primary productivity thus enhancing peat accumulation (Gunnarsson, 2005; Loisel, Gallego-Sala, & Yu, 2012). A similar, positive relationship between peat accumulation and temperature-related variables was reconstructed from other northern regions at centennial to millennial timescales (Charman et al., 2013; Gallego-Sala et al., in review; Garneau et al., 2014; van 641 642 643 644 645 646 647 648 649 650 651 652 653 654 655 656 657 658 659 660 661 662 663
Bellen et al., 2013). Northern Alberta is currently characterized by low amounts of precipitation which situates the region at the dry-warm limit of the global northern peatland distribution when plotted on a temperature-precipitation ‘climate-space’ (Yu, Beilman, & Jones, 2009). The reported absence of an annual-scale relationship between temperature and Sphagnum productivity in the region may indicate plant growth had become limited by drought stress between 2009 and 2014 CE (Wieder et al., 2016), and possibly earlier. Limited Sphagnum productivity at sub-decadal timescales could not be validated using our age-depth models, given the error associated with the model and the possible effect of ongoing decay.
The presence of Sphagnum may be beneficial to carbon sequestration, even if
accompanied by deeper water tables (Camill, Lynch, Clark, Adams, & Jordan, 2001; Tolonen & Turunen, 1996). S. fuscum exhibits an efficient retention of moisture, due to its dense growth form, and therefore microforms dominated by these species may be less vulnerable to drying and deep burning than other Sphagnum species (Benscoter & Wieder, 2003). Combining species distribution models and climate projections, Oke & Hager (2017) showed S. fuscum growth potential may remain stable in northern Alberta until 2050 CE. Other studies suggested persisting large-scale drying of peatlands of this region during the 21st century may eventually cause an increase in net CO2 emissions (Cai, Flanagan, & Syed, 2010) and this effect may become stronger in case Sphagnum is replaced by shrubs (Munir, Xu, Perkins, & Strack, 2014), a trend which was observed in the upper sections of JPH4 and ANZ (Magnan et al., 2018). Even more important in this region may be the contribution from fire-related CO2 emissions as fire frequencies 664 665 666 667 668 669 670 671 672 673 674 675 676 677 678 679 680 681 682 683 684 685 686
increase (Turetsky, Wieder, Halsey, & Vitt, 2002). Boreal peatlands of western Canada are highly sensitive to fire because of the dry climate and high tree density which sustains the spread of fire. Enhanced warming and drying during the 21st century will result in more intense regional fire regimes (de Groot, Flannigan, & Cantin, 2013). No fires were registered in the studied peatlands between 1970 and 2013 CE, when most cores were sampled, but MIL and ANZ were affected by the Fort McMurray fires of 2016 CE. Severe and more frequent burning in the near future may release carbon from deep peat layers that has been stored for centuries. An ongoing apparent lowering of water tables in these peatlands, combined with a possible future expansion of tree and shrub cover, may further promote emissions of CO2.
Acknowledgements
Funding was provided by Alberta Innovates (special thanks to John Zhou, Brett Purdy, and Dallas Johnson). The University of Alberta, the Faculty of Agricultural, Life and Environmental Sciences, and Alberta Environment and Parks provided munificent start-up sstart-upport for the SWAMP laboratory, and the Canada Foundation for Innovation offered a generous equipment grant and matching funds from Alberta Enterprise and Advanced Education. Sarah Gooding, Tracy Gartner, Claudia Sabrina Soto Farfan, Melanie Bolstler, and Karen Lund provided administrative support. We thank Lucas Arantes Garcia, and Brittney Wipf for their help in the laboratory as well as Pedro Henrique Simões and Cara Albright for their help in the field. Special thanks to Melanie Vile, Kelman Wieder and Kevin Devito, who introduced us to the beautiful peatlands of 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 703 704 705 706 707 708 709
northern Alberta. We finally thank Graeme Swindles and an anonymous reviewer for their reviews of an earlier version, and Matthew Amesbury for help with the application of the permafrost transfer function.
References
Amesbury, M. J., Swindles, G. T., Bobrov, A., Charman, D. J., Holden, J., Lamentowicz, M., . . . Warner, B. G. (2016). Development of a new pan-European testate amoeba transfer function for reconstructing peatland palaeohydrology.
Quaternary Science Reviews, 152, 132-151.
http://dx.doi.org/10.1016/j.quascirev.2016.09.024.
Andrejko, M. J., Fiene, F., & Cohen, A. D. (1983). Comparison of ashing techniques for determination of the inorganic content of peats. In: Testing of peats and organic soils. (ed Jarrett PM) pp Page., ASTM International.
Aoki, Y., Hoshino, M., & Matsubara, T. (2007). Silica and testate amoebae in a soil
under pine–oak forest. Geoderma, 142, 29-35.
https://doi.org/10.1016/j.geoderma.2007.07.009.
Appleby, P. G., & Oldfield, F. (1978). The calculation of lead-210 dates assuming a constant rate of supply of unsupported 210Pb to the sediment. Catena, 5, 1-8. 10.1016/s0341-8162(78)80002-2.
Armynot du Châtelet, E., Bernard, N., Delaine, M., Potdevin, J.-L., & Gilbert, D. (2015). The mineral composition of the tests of ‘testate amoebae’ (Amoebozoa, Arcellinida): The relative importance of grain availability and grain selection. 710 711 712 713 714 715 716 717 718 719 720 721 722 723 724 725 726 727 728 729 730 731 732
Revue de Micropaléontologie, 58, 141-154. http://dx.doi.org/10.1016/j.revmic.2015.05.001.
Beilman, D. W., Vitt, D. H., & Halsey, L. A. (2001). Localized permafrost peatlands in western Canada: definition, distributions, and degradation. Arctic, Antarctic, and Alpine Research, 33, 70-77.
Belland, R. J., & Vitt, D. H. (1995). Bryophyte vegetation patterns along environmental gradients in continental bogs. Ecoscience, 2, 395-407.
Belyea, L. R., & Clymo, R. S. (2001). Feedback control of the rate of peat formation. Proceedings of the Royal Society B: Biological Sciences, 268, 1315-1321.
Benscoter, B. W., & Wieder, R. K. (2003). Variability in organic matter lost by combustion in a boreal bog during the 2001 Chisholm fire. Canadian Journal of Forest Research, 33, 2509-2513.
Beyens, L., Ledeganck, P., Graae, B. J., & Nijs, I. (2009). Are soil biota buffered against climatic extremes? An experimental test on testate amoebae in arctic tundra (Qeqertarsuaq, West Greenland). Polar Biology, 32, 453-462. 10.1007/s00300-008-0540-y.
Booth, R. K. (2008). Testate amoebae as proxies for mean annual water-table depth in Sphagnum-dominated peatlands of North America. Journal of Quaternary Science, 23, 43-57.
Booth, R. K., Lamentowicz, M., & Charman, D. J. (2010). Preparation and analysis of testate amoebae in peatland palaeoenvironmental studies. Mires and Peat, 7, 1-7. Bronk Ramsey, C. (2008). Deposition models for chronological records. Quaternary
Science Reviews, 27, 42-60. 733 734 735 736 737 738 739 740 741 742 743 744 745 746 747 748 749 750 751 752 753 754 755
Bronk Ramsey, C. (2009). Bayesian analysis of radiocarbon dates. Radiocarbon, 51, 337-360.
Cai, T., Flanagan, L. B., & Syed, K. H. (2010). Warmer and drier conditions stimulate respiration more than photosynthesis in a boreal peatland ecosystem: Analysis of automatic chambers and eddy covariance measurements. Plant, Cell & Environment, 33, 394-407. 10.1111/j.1365-3040.2009.02089.x.
Camill, P. (2005). Permafrost Thaw Accelerates in Boreal Peatlands During Late-20th Century Climate Warming. Climatic Change, 68, 135-152. 10.1007/s10584-005-4785-y.
Camill, P., Lynch, J. A., Clark, J. S., Adams, J. B., & Jordan, B. (2001). Changes in biomass, aboveground net primary production, and peat accumulation following permafrost thaw in the boreal peatlands of Manitoba, Canada. Ecosystems, 4, 461-478. 10.1007/s10021-001-0022-3.
Canada, E. (2015). Canadian Climate Normals 1981-2010 Station Data. pp Page, Environment Canada.
Chambers, F. M., Beilman, D. W., & Yu, Z. (2010). Methods for determining peat humification and for quantifying peat bulk density, organic matter and carbon content for palaeostudies of climate and peatland carbon dynamics. Mires and Peat, 7.
Charman, D. J., Beilman, D. W., Blaauw, M., Booth, R. K., Brewer, S., Chambers, F. M., . . . Zhao, Y. (2013). Climate-related changes in peatland carbon accumulation during the last millennium. Biogeosciences, 10, 929-944. 10.5194/bg-10-929-2013. 756 757 758 759 760 761 762 763 764 765 766 767 768 769 770 771 772 773 774 775 776 777 778
Charman, D. J., Blundell, A., & Members, A. (2007). A new European testate amoebae transfer function for palaeohydrological reconstruction on ombrotrophic peatlands. Journal of Quaternary Science, 22, 209-221.
Charman, D. J., Hendon, D., & Woodland, W. A. (2000). The identification of testate amoebae (Protozoa: Rhizopoda) in peats, London, Quaternary Research Association.
Charman, D. J., & Warner, B. G. (1992). Relationship between testate amoebae (Protozoa: Rhizopoda) and microenvironmental parameters on a forested peatland in northeastern Ontario. Canadian Journal of Zoology, 70, 2474-2482. 10.1139/z92-331.
Charman, D. J., & Warner, B. G. (1997). The ecology of testate amoebae (Protozoa: Rhizopoda) in oceanic peatlands in Newfoundland, Canada: modelling hydrological relationships for paleoenvironmental reconstruction. Ecoscience, 4, 555-562.
Dai, A. (2011). Characteristics and trends in various forms of the Palmer Drought Severity Index during 1900–2008. Journal of Geophysical Research: Atmospheres, 116.
Davies, L. J., Shannon, B., Jensen, B., Zaccone, C., Froese, D. G., Magnan, G., . . . Shotyk, W. (accepted). High-resolution age modelling of ombrotrophic peat bog profiles from northern Alberta, Canada, using pre- and post-bomb 14C, 210Pb and historical tephra. Quaternary Geochronology.
779 780 781 782 783 784 785 786 787 788 789 790 791 792 793 794 795 796 797 798 799
de Groot, W. J., Flannigan, M. D., & Cantin, A. S. (2013). Climate change impacts on future boreal fire regimes. Forest Ecology and Management, 294, 35-44. http://dx.doi.org/10.1016/j.foreco.2012.09.027.
Donahue, W. F. (2006). Historical interpretation of water supply to Muriel Lake in the 20th century. pp Page, Edmonton, AB, Freshwater Research Ltd.
Fenner, N., Freeman, C., & Reynolds, B. (2005). Hydrological effects on the diversity of phenolic degrading bacteria in a peatland: implications for carbon cycling. Soil
Biology and Biochemistry, 37, 1277-1287.
http://dx.doi.org/10.1016/j.soilbio.2004.11.024.
Fiałkiewicz-Kozieł, B., Smieja-Król, B., Ostrovnaya, T. M., Frontasyeva, M., Siemińska, A., & Lamentowicz, M. (2015). Peatland microbial communities as indicators of the extreme atmospheric dust deposition. Water, Air, & Soil Pollution, 226, 1-7. 10.1007/s11270-015-2338-1.
Finlay, B. J., Esteban, G. F., Clarke, K. J., & Olmo, J. L. (2001). Biodiversity of terrestrial protozoa appears homogeneous across local and global spatial scales. Protist, 152, 355-366.
Foissner, W. (2006). Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozoologica, 45, 111-136.
Fournier, B., Lara, E., Jassey, V. E., & Mitchell, E. A. (2015). Functional traits as a new approach for interpreting testate amoeba palaeo-records in peatlands and assessing the causes and consequences of past changes in species composition. The Holocene, 25, 1375-1383. 10.1177/0959683615585842. 800 801 802 803 804 805 806 807 808 809 810 811 812 813 814 815 816 817 818 819 820 821
Fournier, B., Malysheva, E., Mazei, Y., Moretti, M., & Mitchell, E. A. D. (2012). Toward the use of testate amoeba functional traits as indicator of floodplain restoration success. European Journal of Soil Biology, 49, 85-91. http://dx.doi.org/10.1016/j.ejsobi.2011.05.008.
Gallego-Sala, A., Charman, D. J., Brewer, S., Page, S., Prentice, I. C., Friedlingstein, P., . . . Zhao, Y. (in review). Latitudinal limits to the predicted increase of the peatland carbon sink with warming.
Garneau, M., van Bellen, S., Magnan, G., Beaulieu-Audy, V., Lamarre, A., & Asnong, H. (2014). Holocene carbon dynamics of boreal and subarctic peatlands from Québec, Canada. The Holocene, 24, 1043-1053. 10.1177/0959683614538076. Gilbert, D., Amblard, C., Bourdier, G., André-Jean, F., & Mitchell, E. A. D. (2000). Le
régime alimentaire des Thécamoebiens (Protista, Sarcodina). L’Année Biologique, 39, 57-68. https://doi.org/10.1016/S0003-5017(00)80001-X.
Gunnarsson, U. (2005). Global patterns of Sphagnum productivity. Journal of Bryology, 27, 269-279. 10.1179/174328205X70029.
Halsey, L. A., Vitt, D. H., & Zoltai, S. C. (1995). Disequilibrium response of permafrost in boreal continental western Canada to climate change. Climatic Change, 30, 57-73. 10.1007/BF01093225.
Heal, O. W. (1962). The Abundance and Micro-Distribution of Testate Amoebae (Rhizopoda:Testacea) in Sphagnum. Oikos, 13, 35-47. 10.2307/3565062.
Hua, Q., Barbetti, M., & Rakowski, A. Z. (2013). Atmospheric radiocarbon for the period 1950–2010. Radiocarbon, 55, 2059-2072. 822 823 824 825 826 827 828 829 830 831 832 833 834 835 836 837 838 839 840 841 842 843
Jassey, V. E., Signarbieux, C., Hättenschwiler, S., Bragazza, L., Buttler, A., Delarue, F., . . . Lara, E. (2015). An unexpected role for mixotrophs in the response of peatland carbon cycling to climate warming. Scientific Reports, 5.
Jassey, V. E. J., Meyer, C., Dupuy, C., Bernard, N., Mitchell, E. A. D., Toussaint, M. L., . . . Gilbert, D. (2013). To what extent do food preferences explain the trophic position of heterotrophic and mixotrophic microbial consumers in a Sphagnum peatland? Microbial Ecology, 66, 571-580.
Juggins, S. (2015). rioja: Analysis of Quaternary Science Data. In: R package version 0.9-7. pp Page, http://cran.r-project.org/package=rioja.
Laggoun-Défarge, F., Mitchell, E., Gilbert, D., Disnar, J.-R., Comont, L., Warner, B. G., & Buttler, A. (2008). Cut-over peatland regeneration assessment using organic matter and microbial indicators (bacteria and testate amoebae). Journal of Applied Ecology, 45, 716-727. 10.1111/j.1365-2664.2007.01436.x.
Lamarre, A., Garneau, M., & Asnong, H. (2012). Holocene paleohydrological reconstruction and carbon accumulation of a permafrost peatland using testate amoeba and macrofossil analyses, Kuujjuarapik, subarctic Québec, Canada. Review of Palaeobotany and Palynology, 186, 131-141.
Lamarre, A., Magnan, G., Garneau, M., & Boucher, É. (2013). A testate amoeba-based transfer function for paleohydrological reconstruction from boreal and subarctic peatlands in northeastern Canada. Quaternary International, 306, 88-96. http://dx.doi.org/10.1016/j.quaint.2013.05.054.
Lamentowicz, M., Balwierz, Z., Forysiak, J., Płóciennik, M., Kittel, P., Kloss, M., . . . Pawlyta, J. (2009). Multiproxy study of anthropogenic and climatic changes in the 844 845 846 847 848 849 850 851 852 853 854 855 856 857 858 859 860 861 862 863 864 865 866
last two millennia from a small mire in central Poland. Hydrobiologia, 631, 213-230. 10.1007/s10750-009-9812-y.
Lamentowicz, M., & Mitchell, E. A. (2005). The ecology of testate amoebae (Protists) in Sphagnum in north-western Poland in relation to peatland ecology. Microbial Ecology, 50, 48-63.
Lara, E., Heger, T. J., Mitchell, E. A. D., Meisterfeld, R., & Ekelund, F. (2007). SSU rRNA Reveals a Sequential Increase in Shell Complexity Among the Euglyphid Testate Amoebae (Rhizaria: Euglyphida). Protist, 158, 229-237. http://dx.doi.org/10.1016/j.protis.2006.11.006.
Loisel, J., Gallego-Sala, A. V., & Yu, Z. (2012). Global-scale pattern of peatland Sphagnum growth driven by photosynthetically active radiation and growing season length. Biogeosciences, 9, 2737-2746.
Magnan, G., van Bellen, S., Shotyk, W., Zaccone, C., Mullan-Boudreau, G., Froese, D., . . . Garneau, M. (2018). Impact of the Little Ice Age cooling and 20th century climate change on peatland vegetation dynamics in northern Alberta using a multi-proxy approach and high-resolution peat chronologies. Quaternary Science Reviews. 10.1016/j.quascirev.2018.01.015.
Marcisz, K., Colombaroli, D., Jassey, V. E. J., Tinner, W., Kołaczek, P., Gałka, M., . . . Lamentowicz, M. (2016). A novel testate amoebae trait-based approach to infer environmental disturbance in Sphagnum peatlands. Scientific Reports, 6, 33907. 10.1038/srep33907.
Marcisz, K., Lamentowicz, Ł., Słowińska, S., Słowiński, M., Muszak, W., & Lamentowicz, M. (2014). Seasonal changes in Sphagnum peatland testate amoeba 867 868 869 870 871 872 873 874 875 876 877 878 879 880 881 882 883 884 885 886 887 888 889
communities along a hydrological gradient. European Journal of Protistology, 50, 445-455.
Marcisz, K., Tinner, W., Colombaroli, D., Kołaczek, P., Słowiński, M., Fiałkiewicz-Kozieł, B., . . . Lamentowicz, M. (2015). Long-term hydrological dynamics and fire history over the last 2000 years in CE Europe reconstructed from a high-resolution peat archive. Quaternary Science Reviews, 112, 138-152. http://dx.doi.org/10.1016/j.quascirev.2015.01.019.
Mitchell, E., Charman, D., & Warner, B. (2008). Testate amoebae analysis in ecological and paleoecological studies of wetlands: past, present and future. Biodiversity and Conservation, 17, 2115-2137.
Mitchell, E. A. D. (2002). The identification of Centropyxis, Cyclopyxis, Trigonopyxis and similar Phryganella species living in Sphagnum. pp Page, http://istar.wikidot.com/id-keys.
Mullan-Boudreau, G., Belland, R., Devito, K., Noernberg, T., Pelletier, R., & Shotyk, W. (2017a). Sphagnum Moss as an Indicator of Contemporary Rates of Atmospheric Dust Deposition in the Athabasca Bituminous Sands Region. Environmental Science & Technology, 51, 7422-7431. 10.1021/acs.est.6b06195.
Mullan-Boudreau, G., Davies, L., Devito, K., Froese, D., Noernberg, T., Pelletier, R., & Shotyk, W. (2017b). Reconstructing past rates of atmospheric dust deposition in the Athabasca bituminous sands region using peat cores from bogs. Land Degradation and Development, 28, 2468–2481. 10.1002/ldr.2782.
Munir, T. M., Xu, B., Perkins, M., & Strack, M. (2014). Responses of carbon dioxide flux and plant biomass to water table drawdown in a treed peatland in northern 890 891 892 893 894 895 896 897 898 899 900 901 902 903 904 905 906 907 908 909 910 911 912
Alberta: a climate change perspective. Biogeosciences, 11, 807-820. 10.5194/bg-11-807-2014.
Oke, T. A., & Hager, H. A. (2017). Assessing environmental attributes and effects of climate change on Sphagnum peatland distributions in North America using single- and multi-species models. PLoS ONE, 12, e0175978. 10.1371/journal.pone.0175978.
Oksanen, J., Guillaume Blanchet, F., Kindt, R., Legendre, P., O'Hara, R. B., Simpson, G. L., . . . Wagner, H. (2015). Vegan: Community Ecology Package. pp Page. Payne, R. J. (2012). Volcanic impacts on peatland microbial communities: A
tephropalaeoecological hypothesis-test. Quaternary International, 268, 98-110. Payne, R. J., & Mitchell, E. A. D. (2008). How many is enough? Determining optimal
count totals for ecological and palaeoecological studies of testate amoebae. Journal of Paleolimnology, 42, 483-495.
R Core Team. (2016). R: A language and environment for statistical computing. pp Page, Vienna, Austria, R Foundation for Statistical Computing.
Reimer, P. J., Bard, E., Bayliss, A., Beck, J. W., Blackwell, P. G., Ramsey, C. B., . . . van der Plicht, J. (2013). IntCal13 and Marine13 Radiocarbon Age Calibration Curves 0–50,000 Years cal BP. Radiocarbon, 55, 1869-1887. 10.2458/azu_js_rc.55.16947.
Ricotta, C., & Moretti, M. (2011). CWM and Rao’s quadratic diversity: a unified framework for functional ecology. Oecologia, 167, 181-188. 10.1007/s00442-011-1965-5. 913 914 915 916 917 918 919 920 921 922 923 924 925 926 927 928 929 930 931 932 933 934
