Article

Carbon and Nutrient Stoichiometric Relationships in the
Soil–Plant Systems of Disturbed Boreal Forest Peatlands within
Athabasca Oil Sands Region, Canada
Felix Nwaishi 1,2, * , Matthew Morison 1 , Janina Plach 1 , Merrin Macrae 1 and Richard Petrone 1
1

2

*

Citation: Nwaishi, F.; Morison, M.;
Plach, J.; Macrae, M.; Petrone, R.
Carbon and Nutrient Stoichiometric
Relationships in the Soil–Plant
Systems of Disturbed Boreal Forest
Peatlands within Athabasca Oil
Sands Region, Canada. Forests 2022,
13, 865. https://doi.org/10.3390/
f13060865
Academic Editors: Kerong Zhang
and Xiaoli Cheng
Received: 30 April 2022
Accepted: 17 May 2022
Published: 31 May 2022

Department of Geography & Environmental Management, University of Waterloo,
Waterloo, ON N2L 3G1, Canada; mmorison@uwaterloo.ca (M.M.); jplach@uwaterloo.ca (J.P.);
mmacrae@uwaterloo.ca (M.M.); rpetrone@uwaterloo.ca (R.P.)
Department of Earth and Environmental Sciences, Mount Royal University, Calgary, AB T3E 6K6, Canada
Correspondence: fnwaishi@mtroyal.ca

Abstract: Peatlands store carbon (C), nitrogen (N), and phosphorus (P), and the stoichiometric
relationship among them may be modified by ecosystem disturbances, with major implications for
boreal peatland ecosystem functions. To understand the potential impact of landscape fragmentation
on peatland nutrient stoichiometry, we characterize the stoichiometric ratios of C, N and P in
the soil–plant systems of disturbed boreal forest peatlands and also assessed relationships among
site conditions, nutrient availability, stoichiometric ratios (C:N:P) and C storage in four sites that
represent the forms of disturbed peatlands in the Athabasca oil sands region. Our results showed
that nutrient stoichiometric balance differed across and within these peatlands, among plants, peat,
and groundwater. Ratios of C:N and C:P in peat is a function of nutrient and moisture conditions,
increasing from nutrient-rich (C:N = 28; C:P = 86) to nutrient-poor fens (C:N = 82; C:P = 1061),
and were lower in moist hollows relative to drier hummock microforms. In groundwater, the
drier nutrient-rich fen had higher N:P ratios relative to the nutrient-poor fen, reflecting interactions
between dominant hydrologic conditions and stoichiometric relationships. The N:P ratio of plants
was more similar to those of peat than groundwater pools, especially in the most recently disturbed
nutrient-poor fen, where plant C:N:P ratios were greater compared to older disturbed sites in the
region. These findings suggest that disturbances that modify moisture and nutrient regimes could
potentially upset the C:N:P stoichiometric balance of boreal forest peatlands. It also provides valuable
insights and essential baseline data to inform our understanding of how peatland C:N:P stoichiometry
would respond to disturbance and restoration interventions in a boreal forest region at the tipping
point of environmental change.
Keywords: boreal forest; peatland; C:N:P stoichiometry; disturbance; restoration; Athabasca oil
sands region

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1. Introduction

iations.

Peatlands are major land units in the northern boreal forest region on Canada. These
peatlands support vital ecological functions, which include peat accumulation, nutrient
sequestration, and the provision of unique habitats for biodiversity conservation [1–3].
The ability of peatlands to sustain these ecological functions can be attributed to the
persistence of anoxic conditions, which slows the rate of litter decomposition, consequently
reducing the mineralization rate of organically bound nutrients in the partially decomposed
litter [4–6]. The resulting nutrient conditions support the assemblage of diverse plant
communities, ranging from fast growing vascular species (e.g., sedges) in nutrient-rich
fens to the dominant Sphagnum spp. in nutrient-poor fens [7]. Peatland ecological studies
have shown that aside from hydrologic conditions, the availability of nutrients is a major
control on the capacity of peatlands to accumulate carbon (C) [8,9]. The organic matter that

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Forests 2022, 13, 865. https://doi.org/10.3390/f13060865

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Forests 2022, 13, 865

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forms peat constitutes primary macronutrients such as nitrogen (N), phosphorus (P) and
potassium (K), which are essential for plant C fixation (productivity) and development of
physiological characteristics such as the ability to withstand period stress [10]. The relative
concentrations (ratios) of N and P in organic matter regulate the rate of microbial-mediated
C oxidation during decomposition and mineralization processes [11–13]. Hence, a shift
in the ratio of macronutrient concentrations within the soil–plant system may modify C
cycling dynamics in peatlands.
Ecosystem disturbances that lead to increased availability of essential nutrients can
modify the ratios of macronutrient concentrations within the soil–plant system through
the interaction of peatland vegetation with reactive forms of nutrients available in the
environment. For instance, peatlands in the Athabasca oil sands region (AOSR) of Canada
are threatened by the cumulative impacts of oil sands development such as landscape
fragmentation and modification of peatland hydrology following drainage of development
sites [14]. The region has been described as one of the major hotspots of peatland disturbance due to the large footprint of oil sands extraction [15,16]. Studies from this region
indicate that the construction of semi-permanent roads and well pads on peatlands leads
to a change in site hydrology, oxidation of peat, and subsequent release of mineralised nutrients into the groundwater of surrounding peatlands [17,18]. Atmospheric N deposition
within the vicinity of active mine sites presents another source of exogenous nutrient input
to peatlands in this region, with a reported average of about 4 kg ha−1 year−1 of reactive
forms of N (NO3 –N and NH4 –N), relative to 1 kg ha−1 year−1 background level recorded
in typically N-limited boreal forest sites [19–21]. These exogenous nutrient inputs could
modify the stoichiometric balance of C, N and P in peatland vegetation through increase in
primary productivity and nutrient uptake, subsequently altering the litter chemistry and
biogeochemical functioning of boreal peatlands near industrial development sites [22,23].
Changes in macronutrient balances within peatlands affect C cycling and storage by
altering the C:N:P ratios in plant litter [24,25]. As such, the uncertainties surrounding the
future response of peatland C stock to variable inputs of nutrients from exogenous sources
highlight the need to characterize the stoichiometric ratio of C, N and P in the soil–plant
system of disturbed peatlands located in a region at the tipping point of major ecosystem
change. No recent study has characterized the stoichiometric ratio of macronutrients
in disturbed peatlands within the vicinity of oil sands developments. However, in the
near future, such research data will be essential to inform a mechanistic understanding of
how peatland ecological functions, especially C storage, would respond to the cumulative
impact of anthropogenic and natural disturbance regimes.
To address these knowledge gaps, the objectives of this study were to: (1) evaluate the
chemical characteristics of shallow groundwater across the disturbed peatlands; (2) characterize the patterns of elemental concentrations and nutrient stoichiometric ratios in the
soil–plant systems within microforms (hummock and hollows) across sites; and (3) assess
relationships between nutrient ratios in plants and potential sources of labile nutrients
(i.e., groundwater and peat) relative to site conditions. Consistent with established peatland
stoichiometry literature, we hypothesized that irrespective of the degree of disturbance,
the presence of microtopographic gradients will control soil C stock and nutrient storage in
peatlands [26]. Given the potential for mineral controls (sorption of Fe/Al or Ca) on P mobility [27,28], we hypothesized an increase in N:P ratios within the soil-water system along
the gradient of nutrient-poor to nutrient-rich sites, which may be apparent in plant tissue
as an increase in P limitation (i.e., N:P >16:1). It was also hypothesized that the patterns of
stoichiometric ratios in peatlands would reflect the degree of disturbance across sites.
2. Materials and Methods
2.1. Description of Study Sites
Field research was conducted in four peatland sites that represent the various forms
of disturbed peatlands in this region, leading to some degree of variation in hydrology

2. Materials and Methods
2.1. Description of Study Sites
Forests 2022, 13, 865

3 of 15

Field research was conducted in four peatland sites that represent the various forms
of disturbed peatlands in this region, leading to some degree of variation in hydrology
and water chemistry. The peatlands include a rich, saline and poor fens located within the
and water
chemistry.
The peatlands
include
AOSR
near Fort
McMurray,
AB CA (Figure
1).a rich, saline and poor fens located within the
AOSR near Fort McMurray, AB CA (Figure 1).

Figure 1. Location of the study sites (dark circles) relative to active industrial development hub in
Figure 1. Location of the study sites (dark circles) relative to active industrial development hub in
the Athabasca Oil Sands Region, near Fort McMurray, Alberta, Canada (inset map). The rich fen site
the Athabasca Oil Sands Region, near Fort McMurray, Alberta, Canada (inset map). The rich fen site
is adjacent to industrial development centers to the North whereas the JACOS fen is located within
is adjacent to industrial development centers to the North whereas the JACOS fen is located within
in-situ
disturbance
lease.
an an
in-situ
disturbance
lease.

The nutrient-rich fen site (Rich fen) is located within the larger Poplar Creek Fen, ~7 km
The nutrient-rich fen site (Rich fen) is located within the larger Poplar Creek Fen, ~7
northwest of the active oil sands development hub, near Fort McMurray, CA (56◦ 560 N,
km northwest
of the active oil sands development hub, near Fort McMurray, CA (56°56′
111◦ 330 W). The site sits next to a pipeline right-of-way, that was decommissioned over
N, 111°33′ W). The site sits next to a pipeline right-of-way, that was decommissioned over
12 years ago, leading to a slight modification in site hydrology. A previous study on the
12 years ago, leading to a slight modification in site hydrology. A previous study on the
site reported that the vegetation cover is dominated by Larix laricina (larch), Betula glansite reported that the vegetation cover is dominated by Larix laricina (larch), Betula glandudulosa (dwarf birch), Equisetum fluviatile (swamp horsetail), Smilacena trifolia (three-leaved
losa (dwarf birch), Equisetum fluviatile (swamp horsetail), Smilacena trifolia (three-leaved
Soloman’s-seal), Carex spp. and moss including Polytrichum spp., Tomenthypnum spp. and
Soloman’s-seal),
spp.hyper-saline
and moss including
Polytrichum
spp.,
Tomenthypnum
spp.
and
Sphagnum spp. Carex
[17]. The
fen (Saline
fen) is least
impacted
site, located
approxiSphagnum
spp.
[17].
The
hyper-saline
fen
(Saline
fen)
is
least
impacted
site,
located
ap-by
◦
0
◦
0
mately 40 km south of the industrial hub (56 34 N, 111 16 W). The site is characterized
proximately
40
km
south
of
the
industrial
hub
(56°34′
N,
111°16′
W).
The
site
is
charactera sharp transition from the nutrient-rich saline fen to a nutrient-poor treed fen. Detailed
ized
by a sharphave
transition
from the nutrient-rich
saline Peat
fen toand
a nutrient-poor
treed fen.
descriptions
been previously
reported [28–30].
vegetation samples
from
Detailed
descriptions
have
been
previously
reported
[28–30].
Peat
and
vegetation
samples
this study site were collected in the rich-poor fen transition zone under dominant vascular
from
this study
collectedmaritima
in the rich-poor
transition and
zoneJuncus
underbalticus
dominant
species
cover, site
suchwere
as Triglochin
(Seaside fen
arrowgrass),
in the
vascular
species
cover,
such
as
Triglochin
maritima
(Seaside
arrowgrass),
and
Juncus
baltiSaline portion, Ledum rhododendrum (Labrador tea), Rubus chamaemorus (cloudberry),
and
cusVaccinium
in the Saline
portion,
Ledum rhododendrum
tea),Some
Rubus
(cloud-on
oxycoccos
(cranberry)
in the poor (Labrador
fen portion.
ofchamaemorus
bryophytes found
berry),
and
Vaccinium
oxycoccos
(cranberry)
in the poor
fen portion.
bryophytes
the site
include
Sphagnum
fuscum,
S. capillifolium
and Cladonia
mitis Some
(greenofreindeer
lichen)
(A. Borkenhagen, Unpublished). First nutrient-poor fen (Poor fen) is situated on a local
topographic high (Stony Mountain ~740 masl), about 62 km south of the industrial hub
(56◦ 220 N, 111◦ 140 W). The hydrology of this site was impacted by a road construction that
occurred over 30 years ago. Vegetation cover within the fen is dominated by Sphagnum spp.
(e.g., S. capillifolium, S. agustifolium and S. magellanicum). Additionally, present in abundance
are sedges (e.g., Carex aquatilis and C. limosa) and ericaceous shrubs (Betula glandulosa, Oxy-

Forests 2022, 13, 865

4 of 15

coccus microcarpus, Chamaedaphne calyculata, and Andromeda polifolia), with a discontinuous
tree cover that is dominated by stunted Picea mariana and some Larix laricina [31,32].
The most recent industry-impacted poor fen is within an in-situ oil sands development
lease operated by Japan Canada Oil Sands Company (JACOS). The site is located in Hangingstone, about 50 km south of Fort McMurray (56◦ 190 N, 111◦ 390 W) and was disturbed
through the construction of a semi-permanent road in 2001, which bisected the fen and
restricted water flow along the natural hydrologic gradient [17,18]. Given the hydrological
disturbance and tendency for N and P input to this poor fen from peat oxidation, the
site was specifically selected before the commencement of restoration work to serve as
baseline for future assessment of restoration effects on the nutrient status of peatland soil
and dominant plants. The fen’s vegetation cover comprises mosses (e.g., Sphagnum fuscum),
lichen (e.g., Cladonia stellaris) and ericaceous shrubs (e.g., Rhododendron groenlandicum and
Vaccininium vitis-idaea). A detailed description of the site is presented in [18].
2.2. Sample Collection and Analysis
Sampling for this study was conducted in August 2015, just prior to when some
peatland plants were about to transition from active growth to the senescence phase.
Twelve sampling locations with two microforms (peatlands often comprise undulating
patterns of two microtopographic positions: hummocks-which are elevated, relatively
dry, densely vegetated patches, and hollows–which are lower, sparsely vegetated wet
depressions [26] were randomly selected within each fen. Where present, the living surface
moss layer was removed, and peat was sampled within a 1 × 1 m area using a knife to
cut into a depth of 0 to 10 cm from the surface in each of the two microforms in all of the
12 sampling locations (n = 24). Vegetation samples were collected randomly at six of the
sampling locations at each site. For mosses, capitula of the living moss layer were collected
from the hummock and hollow species, whereas photosynthetically active leaves of three
dominant vascular plants (e.g., Vaccininium vitis-idaea, Chamaedaphne calyculata and/or
Rhododendron groenlandicum) were randomly collected at three of the sampling locations
in each fen. In the lab, peat samples from each sampling point were homogenized in the
original sample bags before removing two subsamples (~5 g dry weight) for bio-available
nutrient extractions.
One of the peat subsamples was shaken for one hour in a solution of 50 mL distilled-deionized
water for the determination of soluble reactive P (SRP), whereas the other peat subsample
was shaken in a solution of 50 mL 2M KCl for nitrate (NO3 − ) and ammonium (NH4 + )
extractions [33]. The extracts were gravity filtered through Whatman No. 42 ashless filter
paper and frozen until analysis. Analysis for determination of SRP, NO3 − -N and NH4 + -N
concentrations were completed using colorimetric techniques (Bran Luebbe AA3, Seal
Analytical, Seattle, WA, USA, Methods G- 102-93 (NH4 + -N), G-109-94 (NO3 − -N + NO2 − N), and G-103-93 (PO4 3− -P (SRP)). Total inorganic N (TIN) was estimated as the sum of
NO3 − -N and NH4 + -N.
Subsamples of peat and vegetation slated for elemental analyses were oven-dried at
60 ◦ C until a constant weight, and ground to a fine powder (60-mesh sieve). Concentrations of C and N were determined by dry combustion on an elemental analyzer (CHNS
Analyzer-EA 1108, Carlo Erba, Milan, Italy). Total Iron (Fe), P, and K were determined on
an Inductively Coupled Plasma Optical Emission Spectrometer (ICP-OES: Optima 8000,
Perkin Elmer LLC, Norwalk, CT, USA), after digestion in concentrated sulphuric acid and
hydrogen peroxide with selenium and lithium sulphate catalysts [34]. Digested samples
were filtered to < 0.45 µm before analysis. The approach by Koerselman and Meuleman [35]
was applied to assess whether plants are classified as either limited by N (mass ratio
N:P < 14:1), P (N:P > 16:1), or co-limited by N:P and some other element (e.g., K, when
14:1 < N:P < 16:1). The ratio of total Fe to total P (Fe:P) concentrations in peat was used as
an indicator of mineral influences on the overall peat P pool across sites.
Samples for groundwater chemistry (pH, conductivity, major ions and nutrients) were
collected from 12 shallow (100 cm depth) PVC wells used for monitoring water table depth

Forests 2022, 13, 865

5 of 15

in the sampling plots within each study site. The wells were purged 24–72 h prior to
sampling, and samples collected were filtered in the field through a 0.45 µm filter, attached
to a hand operated FlipMate filtration system (Delta Scientific Laboratory Products Ltd.,
Canada). The filtrates were frozen until analyses for bioavailable nutrient pools in the
groundwater (i.e., SRP, NO3 − -N and NH4 + -N) using the colorimetric techniques stated
above. Major ions (anions, Cl− , SO4 2− and cations, Ca2+ , Na+, Mg2+ , K+ ) were analyzed
using ion chromatography (DIONEX ICS 3000, IonPac AS18 and CS16 analytical columns).
2.3. Statistical Analysis
All statistical analyses were performed with R [36]. The analyzed variables were
tested for normality prior to any parametric tests, and when necessary, appropriate transformations (log transformation) were implemented for all required data before parametric
analysis. The variability in soil–plant stoichiometric relationships among four sites was
analyzed using linear mixed effects (lme) model in package “nlme” [37], which included
site, microform and interaction between them. Pairwise comparison of significant effects
was carried out by Tukey’s Honestly Significant Differences tests (“TukeyHSD” R Development Core Team, 2013), considered significant at p < 0.05. A standard principal component
analysis (PCA) was employed on logarithmically transformed peat and vegetation chemical data (total C, N, P, K and Fe), using singular value decomposition scaled to have unit
variance (“prcomp” function) [36].
3. Results
3.1. Chemical Characteristics of Shallow Groundwater
The average growing season water table depth varied among the fens, with deeper
water table positions found in the Saline and Rich fens, whereas the JACOS and Poor fens
had shallower water table depths (Table 1). Groundwater chemistry showed a gradient
in the concentration of major ions (e.g., SO4 2− , Ca2+ , Mg2+ , K+ ) among the sites, with the
Poor fen at the lower concentrations margin, Rich fen at the intermediate and Saline at the
upper margin (Table 1). The high concentrations of Cl- and Na+ observed in Saline fen
groundwater were reflected in the electrical conductivity, which was significantly (p < 0.001)
higher than those of the other fens. The inorganic N:P ratio (i.e., TIN: SRP) of groundwater
also showed an increasing gradient from the Poor fen to the Rich fen. Consequently, relative
to all the sites, the N:P ratio of the groundwater pool at the JACOS fen was the lowest,
given the high P concentration in groundwater at this site (Table 1; Figure 2). Across all the
sites, NH4 + was the dominant form of inorganic N in groundwater, whereas NO3 − -N was
available in very low concentration, especially in the Saline fen. The concentration of TIN
was significantly higher (p < 0.05) in the Saline fen than the other fens.
Table 1. Mean (standard deviation) of physicochemical characteristics of shallow groundwater across
the range of natural fen types in the Athabasca Oil Sand Region.
Variables

Saline Fen

Rich Fen

Poor Fen

JACOS

−27 (21)
−36 (33)
−7 (6.1)
−18 (11)
6.3 (0.9)
6.9 (0.4)
4.9 (0.3)
3.5 (0.1)
12,789 (7265)
474 (161)
23 (8)
180 (20)
497 (3890)
288 (232)
161 (137)
440 (254)
14 (8)
150 (160)
45 (74)
75 (31)
511 (410)
438 (282)
199 (171)
515 (285)
21.5 (16.2)
8.18 (5.1)
96.2 (122.0)
126 (77)
22
67
8
9
8.1 (12.4)
1.1 (0.7)
0.6 (0.6)
1.0 (0.1)
156.6 (142.9)
28.5 (8.9)
8.2 (10.5)
7.2 (1.4)
77.9 (71.2)
11.9 (4.6)
2.0 (3.7)
1.8 (0.1)
5471.7 (8683.2)
7.7 (2.5)
2.0 (2.6)
3.8 (0.7)
95.2 (155.0)
12.6 (11.8)
4.2 (10.4)
6.4 (7.8)
5671.0 (7636.0)
2.4 (1.5)
0.7 (1.8)
6.7 (3.4)
WTD: Water table depth; EC: Electrical Conductivity; TIN: Total Inorganic N; SRP: Soluble Reactive Phosphorus.
WTD (cm)
pH
EC (µS/cm)
NH4 -N (µg L−1 )
NO3 -N (µg L−1 )
TIN (µg L−1 )
SRP (µg L−1 )
N: P ratio (mass/mass)
K+ (mg L−1 )
Ca2+ (mg L−1 )
Mg2+ (mg L−1 )
Na2+ (mg L−1 )
SO4 2- (mg L−1 )
Cl− (mg L−1 )

Forests 2022, 13, 865

Ca2+ (mg L−1)
Mg2+ (mg L−1)
Na2+(mg L−1)
SO42- (mg L−1)
Cl− (mg L−1)

156.6 (142.9)
77.9 (71.2)
5471.7 (8683.2)
95.2 (155.0)
5671.0 (7636.0)

28.5 (8.9)
11.9 (4.6)
7.7 (2.5)
12.6 (11.8)
2.4 (1.5)

8.2 (10.5)
2.0 (3.7)
2.0 (2.6)
4.2 (10.4)
0.7 (1.8)

7.2 (1.4)
1.8 (0.1)
3.8 (0.7)
6.4 (7.8)
6.7 (3.4)6 of 15

WTD: Water table depth; EC: Electrical Conductivity; TIN: Total Inorganic N; SRP: Soluble Reactive
Phosphorus.

Figure
Figure2.2.Relationships
Relationshipsbetween
betweennutrient
nutrientlimitation
limitationpatterns
patternsin
inmajor
majorplant
plantfunctional
functionaltypes
types(mosses
(mosses
whitebars
barsand
andshrubs
shrubsin
ingrey
greybars)
bars)and
andN:P
N:Pratios
ratiosof
ofnutrient
nutrientreservoirs
reservoirs(peat
(peatsolution
solutionin
inbrick
brickbars
bars
white
andgroundwater
groundwaterin
indotted
dottedbars)
bars)among
amongall
allthe
thestudy
studysites,
sites,following
followingthe
theapproach
approachofofKoerselman
Koerselman
and
andMeuleman
Meuleman(1996).
(1996).
and

3.2. Elemental Concentration and Stoichiometric Ratios in Soil–Plant System
Inorganic fractions of N in peat were dominated by NH4 + , typically comprising
80–90% of TIN (Table 2) and differed significantly (p < 0.01) among the sites. In sites with
deeper water table positions (i.e., Rich and Saline fens), concentrations of inorganic forms of
N (NO3 − and NH4 + ) were greater (p < 0.01) in drier hummocks than in hollows. Whereas
in the wetter sites (Poor fen and JACOS), only NH4 + -N was significantly higher (p < 0.01)
in hollows, whereas NO3 − -N was not significantly different (p > 0.05) between microforms.
Total inorganic N comprised a very small fraction (<0.5%) of the total N (TN) pool in
peat. Similarly, the bio-available P fraction (i.e., SRP) constituted a very small proportion
of the total P (TP) pool stored in the peat (<1% in all sites). A greater percentage of the
bio-available N and P fraction was estimated for hummocks, especially in the Poor and
JACOS fen sites with higher water table.
Table 2. Mean (standard deviation) of elemental composition and nutrient ratios in peat and vegetation samples across the range of fen types and within site microforms.
PEAT
CHEMISTRY
Ext. NO3 -N (µg/g)
Ext. NH4 -N (µg/g)
TIN (µg/g)
SRP (µg/g)
C (mg/g)
N (mg/g)
P (mg/g)
K (mg/g)
Fe (mg/g)
C:N Ratio
C:P Ratio
N:P Ratio
Fe:P Ratio

SALINE FEN

RICH FEN

POOR FEN

JACOS FEN

Hummock

Hollow

Hummock

Hollow

Hummock

Hollow

Hummock

Hollow

2.25 (0.74)
14.04 (3.65)
16.29 (3.45)
2.51 (0.86)
420.31 (17.0)
18.27 (2.93)
5.57 (0.69)
1.75 (0.12)
0.55 (0.07)
34 (6.5)
96 (15)
3 (2.2)
0.1 (0.03)

2.04 (0.73)
9.73 (1.87)
11.76 (1.87)
2.26 (0.86)
401.03 (5.4)
25.22 (2.58)
6.42 (0.69)
1.66 (0.14)
0.79 (0.09)
22 (6.7)
75 (12)
4 (2.4)
0.1(0.05)

1.64 (0.87)
17.91 (4.51)
19.56 (4.42)
1.43 (0.31)
399.04 (11.3)
10.48 (0.52)
0.79 (0.06)
4.48 (0.41)
2.95 (0.55)
39 (2.5)
537 (40)
14 (3.6)
4 (2.8)

1.50 (0.57)
14.76 (3.98)
16.26 (3.94)
0.88 (0.20)
386.41 (12.0)
11.56 (1.18)
0.90 (0.13)
3.25 (0.40)
2.13 (0.38)
37 (4.4)
528 (73)
13 (2.6)
3 (1.0)

1.54 (0.19)
16.71 (2.34)
18.25 (2.36)
3.63 (1.32)
418.37 (4.0)
7.34 (0.58)
0.92 (0.17)
5.36 (1.12)
1.0 (0.11)
61 (4.4)
616 (99)
8 (2.5)
1 (1.1)

1.39 (0.18)
20.58 (4.64)
21.96 (4.61)
2.13 (0.70)
410.14 (4.2)
9.96 (0.82)
0.85 (0.08)
2.70 (0.37)
0.71 (0.12)
44 (3.4)
539 (61)
11 (2.7)
1 (0.3)

0.83 (0.17)
10.55 (3.44)
11.78 (3.27)
3.24 (1.35)
434.62 (2.1)
4.89 (0.27)
0.40 (0.03)
2.62 (0.22)
0.82 (0.06)
92 (5.3)
1172 (89)
13 (2.4)
2 (0.7)

0.82 (0.08)
12.11 (3.19)
13.02 (3.22)
3.74 (2.84)
431.91 (1.9)
6.95 (0.87)
0.55 (0.08)
2.58 (0.36)
0.85 (0.07)
72 (7.6)
950 (111)
13 (2.9)
2 (0.9)

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Table 2. Cont.
PEAT
CHEMISTRY

SALINE FEN
Hummock

RICH FEN

Hollow

Hummock

POOR FEN

Hollow

Hummock

JACOS FEN
Hollow

Hummock

Hollow

VEGETATION CHEMISTRY
Humoss

Ho-moss

Vascular

C (mg/g)

428 (6.6)

427 (2.8)

484 (25)

N (mg/g)

8.7(0.6)

10 (0.8)

11 (1.0)

P (mg/g)

5.6 (0.7)

5.6 (1.3)

6.0 (0.9)

K (mg/g)

9.3 (1.8)

8.4 (0.7)

13 (5.4)

C:N Ratio

50 (4.0)

42 (3.8)

43 (3.5)

C:P Ratio

79 (9.2)

84 (17)

86 (17)

N:P Ratio

2 (0.5)

2 (0.9)

2 (0.5)

Humoss
445
(2.0)
9.8
(1.1)
6.4
(0.2)
28
(2.2)
47
(5.6)
70
(2.7)
2
(0.2)

Ho-moss
442 (5.4)
11 (1.2)
3.9 (1.5)
24 (4.9)
43 (4.0)
200 (18)
2 (0.6)

Vascular

Humoss

504
(26)
13
(1.5)
3.9
(1.3)
31
(9.9)
39
(5.7)
174
(37)

449
(0.8)
9.7
(0.4)
5.4
(0.5)
24
(8.2)
46
(1.8)
85
(7.7)

5 (4.2)

2 (0.2)

Ho-moss
447 (1.7)
9.2 (0.7)
4.1 (0.9)
30 (2.8)
49 (3.8)
118 (23)
2 (0.5)

Vascular
515
(30)
13
(0.8)
5.1
(1.5)
43
(16)
41
(2.6)
131
(24)
3 (2.4)

Humoss

Ho-moss

Vascular

448 (1.0)

538 (25)

12 (1.2)

12 (1.2)

1.0 (0.1)

1.3 (0.1)

14 (1.4)

13 (0.9)

38 (4.0)

46 (4.1)

771(109)

468 (33)

432 (14)

16
(3.4)

12 (0.7)

10 (0.9)

453
(3.6)
9.2
(0.3)
0.6
(0.1)
13
(1.6)
50
(1.9)

Peat C content was higher in the drier hummock microform relative to the hollow
peat in all the sites (Table 2). In contrast, the total N content of peat was significantly
higher (p < 0.001) in the hollows than hummocks across all sites. Consequently, the C:N
ratio of peat increased along the microtopographic gradient, with significantly lower ratios
(p < 0.001; Table 3) estimated for hollows in all the sites. Similarly, the total P content of
peat was higher (p < 0.05) in hollows than hummocks across all sites, especially in Saline
fen (p < 0.01). Thus, the N:P ratio of Saline fen peat was significantly lower (p < 0.001;
Table 3) than those of all the other fens (Figure 2). The Fe:P ratio estimated for Saline fen
peat was an order of magnitude lower than the ratios of the other fens (Table 2). Using the
product of the mean bulk density measurements for surface peat (0–10 cm depth) from our
sites and the mean concentration of total C, N and P at the same depth, the amount of C, N,
and P stored per unit area across the study sites was estimated (Table 4).
Table 3. Results from the linear mixed effect models for Stoichiometric ratios of peat and vegetation.
Material

Peat

Vegetation

Ratio

Factor

F-Statistic

p-Value

N:P

Site
Microtopography
Microtopography x Site

F3, 23 = 28.462
F1,47 = 1.6483
F3, 47 = 0.2038

<0.001
0.21
0.89

C:N

Site
Microtopography
Microtopography x Site

F3, 23 = 38.1015
F1,47 = 11.1928
F3, 47 = 1.0532

<0.001
<0.001
0.37

C:P

Site
Microtopography
Microtopography x Site

F3, 23 = 52.2549
F1,47 = 3.7309
F3, 47 = 1.2575

<0.001
0.06
0.30

N:P

Site
Microtopography/PFT
Microtopography/PFT x Site

F3, 8 = 48.3075
F2, 11 = 0.1131
F6, 11 = 2.8909

<0.001
0.89
0.03

C:N

Site
Microtopography/PFT
Microtopography/PFT x Site

F3, 8 = 0.299
F2, 11 = 3.1754
F6, 11 = 0.7895

0.83
0.06
0.59

C:P

Site
Microtopography/PFT
Microtopography/PFT x Site

F3, 8 = 27.9797
F2, 11 = 0.2276
F6, 11 = 6.6905

0.01
0.81
0.14

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Table 4. Mean bulk density, carbon, and nutrients concentrations (standard deviation) used in
estimating potential C and nutrients (N and P) stock among the range of peatland in the Athabasca
Oil Sands Region.

Sites

Bulk Density
(0–10 cm)
g/cm3

Carbon and Nutrient Concentrations in Upper Peat
(0–10 cm)
C

N

411.1 (46)
393.3 (40)
413.8 (15)
433.3 (7)

21.6 (10)
11.0 (3)
8.7 (3)
5.9 (2)

Carbon and Nutrients Stored in Upper Peat
(0–10 cm)

P

C Stock

N Stock

6.0 (2.0)
0.8 (0.3)
0.9 (0.4)
0.5 (0.2)

51,382.2 (5773)
23,595.1 (2399)
13,550.7 (482)
12,131.4 (193)

2700.8 (1280)
658.6 (178)
283.7 (92)
165.6 (68)

(g/kg)
SALINE Fen
RICH Fen
POOR Fen
JACOS Fen

0.125 (0.01) 1,2
0.060 (0.03) 3
0.033 (0.03) 3,4,5
0.028 (0.01) 3

P Stock

(kg/ha)
747.3 (304)
50.3 (20)
29.1 (14)
13.2 (6)

1,2 [29,38], 3 [39], 4,5 [32,40].

In the living tissue of plants, C content of vascular species increased significantly
(p < 0.05) along the poor-rich fen gradient and were higher (p < 0.001) than those of
bryophytes (Table 2). There was no significant difference (p > 0.05; Table 3) between
the C and N content of hummock and hollow bryophyte species in all the sites. In contrast,
the N contents of vascular species were significantly higher than (p < 0.001) than those of
bryophyte species, especially the hummock moss species. Hence, the C:N ratios of mosses,
especially the hummock species, were higher than ratios estimated for vascular species.
Relative to the other sites, the P content of living plant tissues in the JACOS fen was low
(p < 0.001). Consequently, the N:P ratios of both bryophytes and vascular plants in JACOS
were significantly higher (p < 0.001; Table 3) than ratios estimated for these plants from the
other sites. Following the characterization of homeostasis [41], vegetation C:N across sites
in both vascular and bryophyte living tissues appear homeostatic, but this is not the case
for N:P and C:P (Figure 3).
A principal component analysis (PC) revealed clear separation in the chemical composition of plants between the JACOS fen (the recently impacted poor fen) and the other older
impacted Poor fen (Figure 4a). The difference between JACOS fen and the other Poor fen is
found almost entirely along the PC1 axis, dominated by variation in total Fe (r = −0.65) and
P (r = −0.45) concentrations. In contrast, the JACOS fen was not distinct from the other sites
in PC space of peat chemical data (Figure 4b), showing overlap with both the Poor
and Rich
Forests 2022, 13, x FOR PEER REVIEW
10 of 17
fens. Instead, the Saline fen was distinct from the three other fens, separated by PC1 values,
which are closely associated with total N (r = −0.61) and P (r = −0.62) concentrations.

Figure 3. Cont.

Forests 2022, 13, 865

Forests 2022, 13, x FOR PEER REVIEW

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Figure 3. Resource and organism stoichiometry in (A) C:N, (B) N:P, and (C) C:P (all as g g−1 ) across
Figure 3. Resource and organism stoichiometry in (A) C:N, (B) N:P, and (C) C:P (all as g g-1) across
thefour
fourstudy
study
sites
(saline
PF; Jacos
and Jacos
fen,C:N,
JF). N:P,
C:N,and
N:P,C:P
and C:P
the
sites
(saline
fen,fen,
SF;SF;
richrich
fen,fen,
RF; RF;
poorpoor
fen, fen,
PF; and
fen, JF).
ratiosdisplay
displayaahomeostatic
homeostatictrend
trendacross
acrossthe
the four
four sites
sites as
as per
and
Elser
(2002),
ratios
per the
the approach
approach of
of Sterner
Sterner
and
Elser
11 of 17
givengiven
that the
of the
relationship
was
not
significant
Points and
(2002),
thatstrengthen
the strengthen
of the
relationship
was
not
significant(p(p>> 0.05
0.05 throughout).
throughout). Points
and
error
mean
standard
deviation
peat
and
9 vegetation
samples
per
error
barsbars
are are
the the
mean
andand
oneone
standard
deviation
of of
24 24
peat
and
9 vegetation
samples
per
site.
site.

Figure 4. Cont.

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Figure 4. Principal components analysis of major element concentrations in (A) all living vegetation
Figure 4. Principal components analysis of major element concentrations in (A) all living
tissues across both plant functional types and (B) all peat material across both microforms across all
vegetation tissues across both plant functional types and (B) all peat material across both
four fen sites, shown with 68% probability ellipses for each site.
microforms across all four fen sites, shown with 68% probability ellipses for each site.

4. Discussions
4.1. Shallow Groundwater Chemistry and Nutrient Availability

4. Discussions

4.1. Shallow Groundwater Chemistry and Nutrient Availability

Our groundwater chemistry results support existing peatland biogeochemistry litera-

Our groundwater chemistry results support existing peatland biogeochemistry literture [18,42], which suggests that nutrient availability in peatlands is strongly influenced by
ature [18,42], which suggests that nutrient availability in peatlands is strongly influenced

site geochemistry and hydrology through groundwater-surface water interactions (water
table fluctuation). With a higher degree of water table fluctuation in the nutrient-rich fens,
we observed greater mineral contributions to the groundwater, as indicated by higher
concentrations of Ca2+ and Mg2+ , as well as greater mineral influences on the availability
of nutrients, especially P. Consistent with previous fen water chemistry studies in central
Alberta and other northern peatlands [43–45], our results show that Ca2+ and SO4 2− are
the predominant peatland cation and anion, respectively, and decrease from the rich to
poor fen types (Table 1). An exception to this trend is observed in the Saline fen, which
shows the predominance of Na+ and Cl− as the major cation and anion, respectively. A
previous hydrogeochemistry study in this fen suggests that the accumulation of Na+ and
Cl− salts in Saline originates from the erosional edge of the underlain Cretaceous Grand
Rapids Formation [46].
Generally, the elemental composition of fen groundwater affects the availability of
nutrients through chemical sorption [47]. For instance, our results show that relative to
the nutrient-rich fens, concentrations of SRP were larger in groundwater and soils of the
nutrient-poor fens, especially the JACOS fen. Lower concentrations of SRP observed in
the Rich fen can be attributed to the high content of mineral elements (e.g., Ca2+ and Fe3+ ),
which binds with mineralized P, limiting the availability and mobility of SRP. Further, there
is a tendency for exacerbated adsorption of P to redox sensitive minerals (e.g., Fe oxides) in
the Rich and Saline fen sites, given deeper water table depths and the higher efficiency of P
adsorption under aerobic conditions [48]. Thus, the higher concentration of SRP observed
in JACOS and Poor fens with shallow water tables (Table 2) is likely because mineralized P
is less readily chelated in low cation peat with limited P sorption potentials [49].

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4.2. Stoichiometric Ratios of C to Macronutrients in the Soil–Plant System among Fens
Our results shows that the C:N and C:P ratios of peat and vegetation vary along a
geochemical gradient, increasing from the Saline fen to the poor JACOS fen, and also along
a microtopographic gradient (decreasing from hummocks to hollows), with the exception
of the C:P ratios of mosses, which were mostly higher in hollow species. The higher C:N
ratios observed in hummock peat and vegetation suggest that the aerobic conditions found
in hummocks support more efficient mineralization of C and N relative to hollows [50,51].
With the exception of the highest C:N ratio observed in peat from JACOS (92:1 and 72:1 for
hummocks and hollows, respectively), the C:N and C: P ratios estimated at our Poor fen
site are within the range reported by [52] for bryophyte dominated ombrotrophic peatland
in eastern Canada. Similarly, the C:N and C: P ratios of sedge peat from Saline fen were
within the range estimated for sedge peats in Minnesota [49] (Table 5) and in the southern
Boreal region of Alberta [45]. These findings suggest that irrespective of past disturbance
regimes, there is a consistent relationship between vegetation community that comprise the
peat litter and the C to macronutrients ratios of peat. Thus, it is apparent that the difference
in stoichiometric ratios among the peatlands in our study reflect the gradients of water
chemistry, hydrologic condition, and vegetation assemblages in these sites.
Table 5. Nutrient stoichiometry of the studied peatlands in the Athabasca Oil Sands Region with
comparable peatland sites, representing entire-core data. Ranges are shown when explicitly available
in paper; otherwise; means of a single or multiple sites are given, indicated by * or ***, respectively.

Study Reference

Peat Stoichiometry
(g g−1 )

Study Years
C:N

N:P

C:P

Verhoeven et al. [4]

1987

19–59

18–37

337–2197

Bridgham et al. [49]

1991

16–38

24–32

526–913

Macrae et al. [53]

2004

16–53

23–57

907–1424

Wang et al. [54] *

2012

37

56

2073

Schillereff et al. [55]

2014

30–47

37–68

1129–3091

Gorham and Janssens [56]

1981-1982

57–81

31–58

2000–4727

Wang et al. [52] ***

1982-1985

23–33

46–60

1190–1360

Hill et al. [57]

2010-2012

24–49

54-163

1506–2438

Present Study

2015

22–92

3–14

75–1172

Study Site
Ten natural and harvested fen and bog sites,
The Netherlands
Three natural bog and fen sites, MN, USA
Paired drained and natural open bog and
poor fen in Quebec, Canada
Mer Bleue Bog, Eastern Canada
Five ombrotrophic blanket mires in a
longitudinal gradient spanning the UK
One bog in northern Minnesota and four
bogs along North American eastern coast
~400 peat profiles across Ontario, Canada,
representing bogs, fens, and swamps
An ombrotrophic bog and a minerotrophic
fen, northern Minnesota, USA
Four fens along a hydrologic gradient, AOSR

The separation between sites within the PC space (Figure 4) provides insights as to
which key elements differentiate the sites in terms of plants and peat chemical composition.
With the JACOS and Saline fens being the most distinct fens in terms of plant and peat
chemical compositions, the PCA results suggest that the Fe and P concentrations of plant
tissue (Figure 4a) and N and P concentration of peat (Figure 4b) may be indicative of
peatland biogeochemical responses to disturbance. This has important implications for
the assessment of both disturbances impacts and ecosystem trajectories in natural and
industry-impacted peatlands.
4.3. Plant Nutrient Ratios and Carbon Storage in Peat Soils of Various Fens
The N:P ratio of dominant PFTs has been widely used as a diagnostic biometric
for detecting the nature of macronutrient limitations in wetlands and other terrestrial
ecosystems [58,59]. Based on the approach of [35], our results suggest that the major
vegetation assemblages found in the older disturbed peatlands of the AOSR are N-limited

Forests 2022, 13, 865

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(N:P < 14:1; Table 2), which is consistent with previous nutrient limitation studies in natural
boreal peatland of Alberta and Ontario [45,59,60]. Conversely, the plant tissue N:P ratios
of mosses and vascular plants in the recently disturbed JACOS fen indicate that the plant
species at this site, especially mosses, are P-limited. This result supports the hypothesis that
peatland disturbance can modify the natural balance of plant tissue nutrient concentration
by reversing the pattern of plant nutrient limitation relative to natural analogues (Figure 2).
Results from our study also show that the TN:TP ratios of peat (Table 2) are not
reflected in either the N:P ratios in bio-available pools or plant tissues in these peatlands
(Figure 2). Indeed, the total P stored in peat represents the various organic and inorganic
forms of P that may be unavailable to plants [45]. This imbalance in N:P ratio between the
bioavailable nutrient pools and the long-term stores in peat supports the hypothesis that
the availability of P is dependent on geochemistry of the site [27,28]. Thus, a disturbance
that modifies the geochemistry of peat could potentially lead to an imbalance in the ratio of
essential plant nutrients.
Although the TN and TP content of peat are not reliable indicators of plant tissue
nutrient conditions, they can be explored in the same way as C stock calculations [61] to
estimate variability in nutrient storage among peatland types, to enable us to quantify the
impact of various forms of disturbance (e.g., wildfire) on peatland’s C and nutrient stock.
The estimates of C storage obtained for our study sites are within the range reported for
northern peatlands [62], where there is still a dearth of information on N and P stocks. With
the highest and lowest stocks of C and nutrients observed in the Saline and the Poor fens,
respectively, our estimate also confirms that more C and nutrients are stored in the upper
peat layer of nutrient-rich fens than their nutrient-poor counterparts (Table 4).
4.4. Potential Impact of Disturbance on Stoichiometry and Carbon Storage of Boreal Fens
Peatlands in the AOSR are highly susceptible to disturbance, and subsequent exogenous input of nutrients given their proximity to an industrial development hub [19].
Evidence from the productivity of Sphagnum fuscum and biogeochemical response of soil
processes to exogenous nutrient inputs suggest that the impact of such disturbance on the
structure and function of peatlands will be more pronounced in poor fens and ombrotrophic
bogs due to the inherent nutrient poor conditions and dependency on precipitation chemistry [21]. Our findings are in agreement with this, as the C to nutrient ratio of acrotelm peat
from the poor fen sites exceeded the critical level for mineralization of organic matter [63].
Thus, any potential shift in C:nutrient ratios of these nutrient poor fens in response to
exogenous nutrient addition will stimulate organic matter mineralization and subsequent
decline in C storage.
Studies have shown that in peatlands receiving exogenous nutrients, the imbalance
between biomass production and decomposition is controlled by availability of P, moisture and soil temperature [64–66]. Our results show that in the short term, hydrological
modification in JACOS was associated with increases in bio-available P, especially within
hollow microforms. Thus, in the absence of P limitation, long-term N addition with a
stable near-surface water table could lead to an increase in peatland C storage. However,
under conditions of P limitation, long-term exogenous N inputs could lead to peatland C
loss [67,68].
5. Conclusions and Implications for Peatland Management under Disturbance
Our study characterized stoichiometric relationships between C and nutrients (N and
P) in the soil–plant systems of peatlands that represent the various degrees of disturbance
in AOSR. We observed that plant chemical composition was distinct between the recently
disturbed peatland and older disturbed sites, which was indicated by total elemental (especially Fe and P) content in living plant tissue. Consistent with stoichiometric relationships
observed in plant tissue of boreal peatland vegetations, our results show that major peatland plant functional types in AOSR are N-limited, except for the recently disturbed site,
where bryophytes, the keystone species in peatlands tend to be P-limited. Our findings

Forests 2022, 13, 865

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suggest that the natural N-limited conditions of boreal peatland plant communities can be
modified by disturbances that alter the hydrology and nutrient regimes of peatlands, with
the potential to shift the stoichiometric balance of C:N:P in the soil–plant system, especially
in the short term. The implications of this stoichiometric shift on the long-term C storage
will depend on dominant vegetation communities, the availability of P, and dominant water
table conditions. Given the gradient of nutrient conditions between the Poor and Rich
fens, it is expected that the impact of disturbances that leads to exogenous nutrient inputs
could be exacerbated in nutrient-poor peatlands, which have the potential to store more C.
Thus, these peatland types should be prioritized in the conservation and management of
peatlands threatened by major environmental disturbances.
Author Contributions: Conceptualization, F.N., J.P. and R.P.; Investigation, F.N., M.M. (Matthew
Morison), M.M. (Merrin Macrae) and J.P.; Data curation, F.N. and M.M. (Matthew Morison); Formal
Analysis, F.N. and M.M. (Matthew Morison); Writing—original draft, F.N., Writing—editing and
review, M.M. (Matthew Morison), J.P., M.M. (Merrin Macrae) and R.P.; Visualization, M.M. (Matthew
Morison) and M.M. (Merrin Macrae); Resources, J.P. and M.M. (Merrin Macrae); Methodology, J.P.,
F.N. and M.M. (Matthew Morison); Funding acquisition, M.M. (Merrin Macrae) and R.P.; Supervision,
M.M. (Matthew Morison), M.M. (Merrin Macrae) and R.P. All authors have read and agreed to the
published version of the manuscript.
Funding: This study was funded by the Natural Sciences and Engineering Research Council of
Canada (NSERC)-Discovery Grant Awarded to R. Petrone and M. Macrae. The authors also acknowledge funding support to R. Petrone from Canada’s Oil Sands Innovation Alliance (COSIA), Suncor
Energy Inc., Shell Canada and the Japan Canada Oil Sands Company. Funders had no role in study
design, data analysis or decision to publish the results.
Data Availability Statement: The datasets generated during and/or analyzed during the current
study are available from the corresponding author on reasonable request.
Acknowledgments: We acknowledge the assistance of Tristian Gingras-Hill and Adam Green with
field sampling for this study.
Conflicts of Interest: The authors declare no conflict of interest.

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