Forest Ecology and Management 289 (2013) 7889

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Forest Ecology and Management

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Organic, elemental, and geochemical contributions to lake sediment deposits

during severe spruce beetle (Dendroctonus rupennis) disturbances
Jesse L. Morris a,, Peter C. le Roux a, Anthony N. Macharia b, Andrea Brunelle b, Elizabeth G. Hebertson c,
Zachary J. Lundeen b,d
a

Department of Geosciences and Geography, University of Helsinki, Gustaf Hllstrmin katu 2a, Helsinki 00014, Finland
Department of Geography, University of Utah, 260 S. Central Campus Dr., Salt Lake City, UT 841112, United States
USDA Forest Service, Forest Health ProtectionOgden Field Ofce, 4746 South 1900 East, Ogden, UT 84403, United States
d
Rio Mesa Center, University of Utah, 201 S. Presidents Circle Room 210, Salt Lake City, UT 84112, United States
b
c

a r t i c l e

i n f o

Article history:
Received 15 June 2012
Received in revised form 25 September 2012
Accepted 5 October 2012

Keywords:
C/N ratio
Spruce beetle
Dendroctonus rupennis
GLMM
Disturbance
Lake sediments

a b s t r a c t
Recent outbreaks of native bark beetles are unprecedented during the historical period. The aim of this
manuscript is to develop a proxy-based methodology to infer past bark beetle outbreaks using lake sediments to provide long-term context for recent outbreaks. We test three hypotheses to determine how
the ecological impacts of severe spruce beetle (Dendroctonus rupennis Kirby) disturbances are recorded
in lake sediment deposits. The resulting mortality and defoliation of Engelmann spruce is hypothesized
to: (1) decrease the ratio of spruce to r pollen; (2) reduce canopy interception of precipitation leading to
an increase in soil erosion and/or enhanced mobilization of terrestrial carbon; and (3) leach foliar nitrogen and enhance algal productivity resulting in increased nitrogen values in lake sediments. To test these
hypotheses, we analyzed sediment cores from six spruce beetle-affected basins in Utah for spruce/r pollen ratio (hypothesis 1), loss-on-ignition, magnetic susceptibility of sediments (hypothesis 2), and
d13CBOM, d15NTN, elemental C and N, and the C/N ratio of bulk organic material (hypotheses 2 and 3).
The dataset was statistically tested using general linear mixed models (GLMMs) to determine if the
response variables differed signicantly between outbreak and non-outbreak period. The spruce/r pollen ratio responded signicantly to outbreaks at all sites suggesting that this metric may be the most suitable for identifying past spruce beetle outbreaks. For our second hypothesis we found little support for an
inux of terrestrial C due to strongly individualist responses of the basins. For our third hypotheses we
found little support for increased sedimentary nitrogen, likely due to alterations to nutrient cycling from
human activities. Therefore the host/non-host pollen ratio provides the most promising metric for detecting past outbreaks.
2012 Elsevier B.V. All rights reserved.

1. Introduction
Spruce beetles (Dendroctonus rupennis Kirby) are native to
western North America (WNA) and are considered important disturbance agents (Jenkins et al., 2008; Raffa et al., 2008). The ecological impacts of these insect outbreaks are profound (Baker and
Veblen, 1990; Logan and Powell, 2001; Amin et al., 2012). In Utah
and Colorado recent outbreaks of spruce beetle in mature Engelmann spruce (Picea engelmannii Parry ex Engelm.) have been particularly severe (Mielke, 1950; Dymerski et al., 2001; Kulakowski
and Veblen, 2006; DeRose and Long, 2007; Hebertson and Jenkins,
2008; Morris and Brunelle, 2012). Generally, increasing spruce
beetle populations result from temperature-driven accelerations
of their reproductive cycle, leading to exponential population
Corresponding author.
E-mail address: jesse.morris@helsinki. (J.L. Morris).
0378-1127/$ - see front matter 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.foreco.2012.10.004

growth (Schmid and Frye, 1977; Hansen et al., 2001a,b). Pervasive

warm conditions during the mid-20th century and 1990s CE, concomitant with landscapes composed of abundant suitable-sized
hosts, were favorable for severe spruce beetle outbreaks (Schmid
and Frye, 1977; Dymerski et al., 2001; DeRose and Long, 2012).
Spruce beetles are important catalysts in promoting forest
regeneration (Fettig et al., 2007). For subalpine forests in Utah
and Colorado, tree ring reconstructions estimate the return interval
of stand-replacing spruce beetle disturbances to be ca. 120 years
(Veblen et al. 1991, 1994; DeRose and Long, 2007). Tree ring records in this region extend back in time to the Little Ice Age
(1300 to 1850 CE). In a general sense, the central Rocky Mountains
were cool and dry during the Little Ice Age (Petersen, 1994; Piechota et al., 2004; Knight et al., 2010; Cook et al., 2011). After
1850 CE, the climate warmed and subalpine forests advanced upslope and stand density increased (Munroe, 2003; Carrara, 2011).
Also at ca. 1850 CE Utah was settled by Euro-Americans which

J.L. Morris et al. / Forest Ecology and Management 289 (2013) 7889

resulted in timber harvesting and livestock grazing in subalpine

landscapes (Gill, 2007; Hall, 2001). To mitigate and/or improve adversely impacted rangelands in Utah and elsewhere in the western
US, federally-funded land stewardship agencies were created in
the early 1900s CE (Hall, 2001). However, during the mid and later
20th century, wildre exclusion policies, continued grazing, and
non-native sh stocking in high-elevation lakes altered ecosystem
trajectories still further from presumed pre-settlement conditions
(Romme and Despain, 1989; Leavitt et al., 1994; Parker et al.,
2006).
Determining spruce beetle dynamics during climatic periods
prior to the Little Ice Age would provide greater insight into longterm dynamics of these insects. Of particular interest are climatic
periods of the recent geologic past such as the Holocene (last
11,700 years). For example, the mid-Holocene (ca. 6,000 years
ago) was warm and dry in WNA and may provide a relevant analog
for 21st century climates (Bartlein et al., 1998; Wanner et al., 2008).
Tree ring-based disturbance records in subalpine forests do not
commonly extend back in time beyond recent centuries. On the
other hand, lake sediment records from WNA frequently span the
Holocene and occasionally much longer (e.g. Jimnez-Moreno
et al., 2007). Therefore lake sediment-based reconstructions can address longer term climate-bark beetle dynamics that are important
since forest management strategies are placing greater emphasis on
emulation of natural disturbance regimes (Long, 2009). Since little
is presently known about long-term bark beetle dynamics during
warm and dry periods, it is imperative that beetle disturbance
reconstructions be developed that are relevant for the 21st century
(Logan and Powell, 2001; Mitten and Ferrenberg, 2012).
Records of past ecological conditions and disturbance regimes
assessed from lake sediments provide useful datasets to land management agencies that assist in guiding restorative, prescriptive,
and conservation strategies (Froyd and Willis, 2008; Jackson and
Hobbs, 2009; Marlon et al., 2012). Several recent studies suggest
that lake sediment records yield insights into the ecological impacts of bark beetle outbreaks that are instructive for paleoecological reconstructions (Brunelle et al., 2008; Watt, 2008; Anderson
et al., 2010; Morris et al., 2010; Morris and Brunelle, 2012). For
example, preserved mountain pine beetle (Dendroctonus ponderosae Hopkins) remains were recovered from lake sediments corresponding to both historic and early Holocene outbreaks (Brunelle
et al., 2008). However, the processes that result in preservation
of insect chitin in lake environments is not yet fully understood
but is inuenced by lake water chemistry, weather conditions during peak beetle emergence, and bacterial decomposition (Morris
et al., 2010; Beier et al., 2012; Morris and Brunelle, 2012).
On the other hand, pollen preservation is better understood (e.g.
Sepp and Bennett, 2003) and is known to be sensitive to insect
disturbances (Davis, 1981; Morris and Brunelle, 2012). Because
pollen analysis is time and labor intensive, lake sediment records
are analyzed at discontinuous intervals where centennial resolution is typical (e.g. Brunelle et al., 2008). It is currently unknown
what resolution is required to condently reconstruct bark beetle
outbreaks though it is presumable that centennial (or greater) resolution is inadequate. Down-core compression of lake sediments
(i.e. more time per cm) may limit the capability of any lake sediment proxy to record sub-decadal non-re disturbances, particularly in resilient coniferous ecosystems that recover quickly from
even severe events (Minckley et al., 2011).
Regardless of these challenges, a method for reconstructing
bark beetle outbreaks is needed. The goal of this study is to develop
an analytical strategy that might be useful in detecting bark beetle
disturbances using sedimentary records. Based on our literature review, we developed three hypotheses addressing how the ecological impacts of spruce beetle outbreaks are recorded in lake
sediments. Our rst hypothesis states that because spruce beetle

79

outbreaks result in loss of mature spruce across a landscape, then

signicant decreases in the ratio of spruce to r pollen occur. Our
second hypothesis states that because reduced canopy interception
of precipitation results following post-outbreak needlefall, then increases in soil erosion and/or the mobilization of terrestrial carbon
(i.e. woody litter, needles, frass, and boring dust) will be detectable
in lacustrine deposits. Our third hypothesis states that because
leaching of foliar nitrogen and increases in algal productivity occur
after post-outbreak needlefall, then nitrogen values in lake sediments will also increase.
To test these hypotheses we assessed six lake sediment records
which cover one or more spruce beetle outbreaks that occurred
during the 20th century in southern Utah (Fig. 1, panels a and b).
Specically, we analyzed our sedimentary records for the following
parameters: spruce/r pollen ratio (hypothesis 1); magnetic susceptibility (MS); loss-on-ignition (LOI) for organics (%org) and carbonate (CaCO3) (hypothesis 2); stable carbon (d13C) and nitrogen
(d15N) isotopes (hypotheses 2 and 3); and elemental parameters
(%C, %N, C/N ratio) (hypotheses 2 and 3). These variables were
tested with generalized linear mixed models (GLMMs) (e.g.
Aukema et al., 2005) to determine their response to severe spruce
beetle disturbances.
2. Background
As poikilotherms, spruce beetle reproductive cycles are responsive to temperature changes. In cool climates 23 year reproductive cycles are common whereas in warmer climates (or periods)
the species may produce one generation per year (Hansen et al.,
2001a,b). In the Rocky Mountains, mature spruce beetles emerge
to seek host trees when daily maximum temperature reaches
16 C (Dyer, 1969). Once the temperature threshold for beetle
emergence is surpassed, attacking beetles select host trees based
on chemical cues emitted by other colonizing beetles. Upon selection of a suitable host tree, beetles chew through the outer bark to
access phloem tissue. Trees defend against invading beetles by
ushing attack sites with volatile-rich sap resulting in the formation of pitch tubes (Fig. 1, panel c). If a host tree is moisture
stressed, it produces less sap with which to repel invading beetles.
During outbreaks, the number of attacking beetles is generally sufcient to overwhelm even healthy, vigorous trees. In colonization
of host trees, beetles generate large quantities of boring dust and
excrement (Fig. 1, panel c) (Schmid and Frye, 1977).
Needlefall typically occurs within 35 years after tree mortality
(Page and Jenkins, 2007) and increases nitrogen levels in soils and
surface water (Huber 2005; Morehouse et al., 2008). Reduced canopy continuity decreases precipitation interception leading to elevated soil erosion and/or increases in productivity of understory
trees, shrubs, and herbs (Schmid and Hinds, 1974). During landscape-scale outbreaks, decreased water utilization after widespread tree mortality results in increased streamow, rising
groundwater, and earlier-than-average snowmelt due to loss of
canopy shading (Love, 1955; Bethlahmy, 1974,1975; Potts, 1984).
Instances of paludication (i.e. rising of the water table), increased
algal productivity, and eutrophication in surface water have also
been reported following a severe spruce beetle outbreak (Anderson
et al., 2010).
3. Study sites
3.1. Colorado Plateau
The Colorado Plateau is a physiographic and ecological link
among the Great Basin, Rocky Mountain, and Sonoran and Mojave
desert ecosystems (Anderson et al., 2000). The subalpine plateaus

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J.L. Morris et al. / Forest Ecology and Management 289 (2013) 7889

Fig. 1. (A) Map of study area showing locations for lakes on the Wasatch Plateau, Aquarius Plateau, and Markagunt Plateau. (B) Photographs of ghost forests resulting from
spruce beetle-cause mortality during the 1990s. Note absence of needles on standing dead trees. (C) Photographs of bark beetle-attacked trees. Note copious amounts of sap,
frass, and boring dust. Photographs provided by Jesse Morris (B and C). Steve Munson (C).

and tablelands of the Colorado Plateau encompass an area of ca.

337,000 km2 and the uplifted landforms occur in three primary orogenic belts. These features include nine named high plateaus oriented northeastsouthwest, separated by deep valleys. The
complex topography of this region yields steep moisture and temperature gradients. The precipitation regime is bimodal and is dominated by a late winter/early spring peak from Pacic frontal storms
modulated by El Nio-Southern Oscillation and a late summer peak
from convective storms derived from the North American Monsoon
(Tang and Reiter, 1984; Mock, 1996; Adams and Comrie, 1997).
3.2. Wasatch Plateau
The Wasatch Plateau (Wasatch hereinafter) is the northernmost
of the study sites, is oriented north/south, and covers an area of

2477 km2 with elevations averaging 3300 m. The subalpine zone

of the Wasatch is dominated by Flagstaff limestone causing surface
water to be alkaline (pH 9+) (Klemmedson and Tiedemann, 1998;
Morris et al., 2010). Following Euro-American settlement, the Wasatch was extensively logged and grazed by sheep (Ellison, 1954;
Hall, 2001). Historically the Wasatch has been covered by dense
stands of Engelmann spruce and subalpine r (Abies lasiocarpa
Hook. (Nutt.)). Quaking aspen (Populus tremuloides Michx.), limber
pine (Pinus exilis James), and blue spruce (Picea pungens Engelm.),
a less-preferred host for spruce beetle, can also be found throughout the subalpine forest zone. Beginning in the late 1980s a spruce
beetle epidemic (1990s Wasatch outbreak) began that resulted in
>90% mortality of mature Engelmann spruce (Dymerski et al.,
2001). Hopkins (1909) reported an outbreak in the early 1900s
near Emerald Lake (1900s Emerald outbreak). To investigate the

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81

impacts of these spruce beetle outbreaks two cirque lakes were

cored. Blue Lake (BL) (3930 20.3300 N, 111300 17.4300 W) occurs at
3129 m, has a surface area of 3.2 ha, and water depth of 8 m. Emerald Lake (EL) (3940 26.7200 N, 111290 50.96400 W) occurs at 3090 m
elevation, has a surface area of 3.3 ha, and water depth of 9 m.
3.3. Aquarius Plateau
The Aquarius Plateau (Aquarius hereinafter) is the highest elevation landform in the study area (mean elevation of 3355 m, area
of 2330 km2). The rolling topography of the Aquarius is composed
of andesitic basalt that originated during the Oligocene Marysvale
Volcanic episode (Flint and Denny, 1958). The Aquarius was covered by a ca. 200 m thick ice cap during the Pleistocene yielding
a cover of thin, poorly developed soils that are neutral to weakly
acidic (Osborn and Bevis, 2001; Marchetti et al., 2005). The Aquarius is dominated by spruce/r forests and the highest elevations
consist of pure Engelmann spruce stands interspersed with grasslands (Poaceae spp.). Other arboreal species include subalpine r,
limber pine, aspen, blue spruce, and Great Basin bristlecone pine
(Pinus longaeva Bailey). A spruce beetle epidemic, beginning
around 19161918, persisted into the late 1930s, and killed >80%
of mature Engelmann spruce (1930s Aquarius outbreak) (Dixon,
1935; Mielke, 1950). Two kettle lakes were cored in areas known
to be affected during the 1930s outbreak (Morris and Brunelle,
2012). Banana Lake (BaL) (3840 0.2900 N, 111350 12.2100 W) occurs
at 3,128 m, has a surface area of 10.6 ha, and water depth of 5 m.
Purple Lake (PL) (3840 28.3300 N, 111340 16.4700 W) occurs at
3226 m, has a surface area of 6.2 ha, and water depth of 5 m.
3.4. Markagunt Plateau
The Markagunt Plateau (Markagunt hereinafter) trends north
south and covers an area of 2100 km2 with elevations averaging
3320 m. An ice sheet occupied the summit of the Markagunt during the Pleistocene and soils are generally thin with occasional evidence of till and moraine deposits (Osborn and Bevis, 2001). The
parent bedrock is predominantly composed of Flagstaff limestone
and soils are alkaline (Wilson and Thomas, 1964). Historically the
Markagunt has been covered by dense forests of Engelmann spruce
and subalpine r. Limber pine, quaking aspen, and Great Basin bristlecone pine also occur. The Markagunt experienced a severe
spruce beetle outbreak beginning in the 1990s that caused mortality in >98% of canopy Engelmann spruce in surveyed stands (1990s
Markagunt outbreak) (DeRose and Long, 2007). Two small ponds
were cored to investigate the ecological effects of the 1990s outbreak. Alpine Pond (AP) (37380 11.2200 N, 112490 26.7500 W) occurs
at 3172 m elevation, has a surface area of 0.1 ha, and a water depth
of 2 m. Morris Pond (MP) (37400 25.4800 N, 112460 49.7500 W) occurs
at 3125 m, has a surface area of 1 ha, and a water depth of 2 m.

Fig. 2. Summary of age-depth relationships for the six subalpine lake basins
discussed in this study based on 210Pb/137Cs dating analysis. Full laboratory
analytical results presented in Morris and Brunelle (2012).

in Denver, CO for analysis. The 210Pb prole was interpreted using

the Constant Rate of Supply Model (Appleby et al., 1979). The 1963
CE peak in 137Cs associated with the climax of above-ground nuclear testing was also used to constrain the chronologies (Morris and
Brunelle, 2012). Core top samples were assigned to the year of core
collection. Final age-depth assignments were made by Dr. Budahn.
Though the dated sediment records extend to the 19th century,
only data from the 20th century to the year of coring are presented.
4.2. Pollen ratios
Pollen was isolated from the six sediment cores discussed here
following methods presented by Faegri et al. (1989). Morris and
Brunelle (2012) identied over 75 unique pollen types though they
emphasized that the ratio of spruce to r pollen was useful in diagnosing spruce beetle disturbances. The formula used to calculate
the pollen ratio is (a  b)/(a + b) where a is assigned to spruce
and b to r (i.e. spruce/r ratio). Ratio values are presented in standard units (SUs).
4.3. Magnetic susceptibility (MS)
MS data were collected for every contiguous cm to assess ferromagnetic mineral content of the sediments. Peaks in MS are known
to be associated with increased runoff and erosion from landscape
disturbances that remove vegetative cover such as logging, canopy
defoliation, and re (Gedye et al., 2000). MS properties of the sediments were determined using 10 cc cups analyzed with a Bartington coil sensor. MS data are presented in standard increments
(SIs).
4.4. Loss-on-ignition (LOI)

4. Methods
4.1. Chronology
Chronologies for the six cores discussed here were established
through 210Pb/137Cs analysis (Fig. 2). The upper 24 cm of each sediment core was subsampled in 2-cm intervals. For example, sediments from 2 to 4 cm were homogenized yielding one subsample
(5 cc). Therefore 12 unique subsamples for each core were submitted for dating analysis, with the exception of BL, which was subsampled at 1-cm intervals (5 cc) for the upper 20 cm (Morris and
Brunelle, 2012). Subsamples were weighed and dried in a mufe
furnace at 100 C to remove water. Dehydrated samples were submitted to Dr. James Budahn at the US Geological Survey Laboratory

LOI analysis was performed on 1 cc subsamples collected from

every contiguous cm of each of the six cores presented here. Organic (%org) and carbonate (%CaCO3) content of the sediments
were determined by ignitions at 550 C and 900 C, respectively,
for 2 h (Dean, 1974). LOI data are presented in percentages. Carbonate variability in lake sediments can result from both evaporation and dissolution of parent bedrock (Shuman, 2003).
4.5. Isotopes
One cc sediment subsamples were collected from every contiguous cm of each of the six sediment cores for isotopic and elemental analysis. For each subsample, an aliquot of 300 mg was placed

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J.L. Morris et al. / Forest Ecology and Management 289 (2013) 7889

Fig. 3. Time-series plots of nine response variables for the 20th century for six subalpine lakes in Utah. Note differences in scale of y-axes among sites. The approximate
temporal window of spruce beetle (Dendroctonus rupennis) outbreaks are delineated by dashed rectangles.

into a 50 ml beaker and then treated with excess 0.1 N HCl to remove carbonates and allowed to react for 48 h. Subsample residues
were then transferred into 1.7 ml vials, placed into a centrifuge,
and spun at 4000 rpm for 5 min after which the supernatant was
decanted. Residual acid was rinsed from the sediments by adding
distilled water, centrifuging, and decanting until the pH became
neutral (pH  7.0). The sediment residues were dried at 60 C for
48 h. The subsamples were combusted in a Costech 4010 Elemental Analyzer at 1650 C and inlet to a Deltaplus Isotope Ratio Mass
Spectrometry in continuous ow mode at the Stable Isotope Facility for Environmental Research (SIRFER) Laboratory at the University of Utah. Isotope values are calculated as dX
() = 1000(Rsample/Rstandard  1) where X is either 15N or 13C
and R is 15N/14N or 13C/12C respectively. dX is expressed in per
mil () relative to internationally agreed standards; V-PDB for organic carbon and atmosphere (AIR) for nitrogen. Sediment subsamples were analyzed together with internal standards (PLRM-1,
PLRM-2, and SLRM) calibrated to VPDB standard. The sediment
masses analyzed ranged from 2.5 to 10 mg for BL, 2 to
5.5 mg for EL, 2 mg for AP, 2.5 to 4.5 mg for MP, 1 to
2.5 mg for BaL, and 4 to 10.5 mg for PL. The standard deviations (1r) of isotope measurements of d13C and d15N were 60.2.
The d13C values of bulk organic matter (hereinafter d13CBOM) are
expected to reect the contribution of terrestrial organic matter
relative to organic matter derived from lacustrine primary productivity (Meyers and Lallier-Verges, 1999). The d15N values from sediments (total nitrogen, hereinafter d15NTN) are expected to vary
with changes in total nitrogen cycling, landscape disturbance,
and changes in algal productivity (Robinson, 2001).
4.6. Statistical analysis
The inuence of beetle population status (factor: endemic vs.
outbreak) on the seven environmental parameters was examined
using generalized linear mixed models (GLMMs), adding site as a
random effect to account for multiple measurements being taken
from the same sediment core from each lake (Bolker et al., 2009;
Zuur et al., 2009). Analyses were performed using the glmmPQL
function in the MASS package (Venables and Ripley, 2002) in R statistical software (R Development Core Team, 2011), assuming a

Gaussian distribution of errors and applying an identity link function. Model adequacy was conrmed by examination of residuals,
which were approximately normally distributed. Levels (95% condence levels) of the seven environmental variables under endemic and outbreak conditions were subsequently predicted from
the GLMMs (following Zuur et al., 2009).
5. Results
5.1. Wasatch Plateau
5.1.1. Blue Lake (BL)
The spruce/r pollen ratio declines during the 1990s Wasatch
outbreak (Fig. 3). MS exhibits a long-term decreasing trend over
the 20th century which continues during the 1990s Wasatch outbreak. Carbonate and %org values are generally stable but decrease
during the 1990s Wasatch outbreak. The d13CBOM versus C/N ratio
scatter plot suggests that BL sediments are dominated by organic
matter of algal origin (Fig. 4). Linear regression plots suggest an
inorganic nitrogen component (Fig. 5) and d15NTN values of this
lake range from 0 to +2.1 (Fig. 3). The d13CBOM increases
while d15NTN decreases during the 1990s Wasatch outbreak
(Fig. 3). The C/N ratio, %C, and %N generally decrease over the latter
20th century (Fig. 3).
5.1.2. Emerald Lake (EL)
The spruce/r pollen ratio declines with both the 1990s Wasatch and 1900s Emerald outbreaks (Fig. 3). A long-term declining
trend in MS is evident over the 20th century which decreases
through both outbreaks. From LOI, carbonate decreases during
the 1900s outbreak though does not respond to the 1990s Wasatch
outbreak. The %org increases during the 1990s Wasatch outbreak.
The d13CBOM versus C/N ratio scatter plot indicates that the organic
matter composition is lacustrine algae as well as land plant contributions (Fig. 4). Linear regression plots suggest an inorganic nitrogen component (Fig. 5) and d15NTN values of this lake range from
0 to +3 (Fig. 3). The d13CBOM and d15NTN do not respond to
either the 1990s Wasatch or 1900s Emerald outbreaks. The %C
and %N increase during the 1990s outbreak. The C/N ratio declines

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83

Fig. 4. Scatterplots of d13CBOM, versus C/N ratio for Blue Lake and Emerald Lake (Wasatch Plateau); Banana Lake and Purple Lake (Aquarius Plateau); Alpine Pond and Morris
Pond (Markagunt Plateau). The expected values for lacustrine algae, C3-, and C4-derived organic matter (end-member values) are indicated by polygons (modied after
Meyers and Lallier-Verges (1999)).

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J.L. Morris et al. / Forest Ecology and Management 289 (2013) 7889

over the 20th century before increasing during the 1990s Wasatch
outbreak and then again decreasing at the core top.
5.2. Aquarius Plateau
5.2.1. Banana Lake (BaL)
During the 1930s Aquarius outbreak the spruce/r pollen ratio
declines at BaL (Fig. 3). The MS trend generally increases towards
modern, with a conspicuous increase during the outbreak. There
are visually detectable peaks in MS (e.g. 1905) but not during the
1930s Aquarius outbreak. Carbonate is essentially stable and does
not respond to the 1930s Aquarius outbreak. Towards present, carbonate increases slightly before decreasing steeply ca. 2000. The
d13CBOM versus C/N ratio scatter plot conrms dominance of algal
material with a terrestrial component (Fig. 4). Linear regression
plots suggest an inorganic nitrogen component (Fig. 5) and
d15NTN values of this lake range from 2 to +2 (Fig. 5).
The d13CBOM, d15NTN, and %org are unresponsive to the outbreak
(Fig. 3). The %C is generally stable and %N is unresponsive to the
1930s Aquarius outbreak. The C/N ratio is variable over the 20th
century; however during the 1930s Aquarius outbreak it is stable.
5.2.2. Purple Lake (PL)
The spruce/r pollen ratio decline occurs during the 1940s at PL,
lagging the 1930s Aquarius outbreak (Fig. 3). During the 1930s
Aquarius outbreak MS and carbonate are essentially stable. Carbonate exhibits little variability and generally exhibits a decreasing
trend over the record. The %org is unresponsive during the 1930s
Aquarius outbreak and initiates an increasing trend ca. 1970. The
d13CBOM versus C/N ratio scatter plot conrms organic matter composed of lacustrine algae and C3 plant material (Fig. 4). Linear
regression plots suggest an inorganic nitrogen component (Fig. 5)
and d15NTN values of this lake range from 0 to +3 (Fig. 3).
The C/N ratio, d15NTN, and d13CBOM do not respond to the 1930s
Aquarius outbreak (Fig. 3). The %C is generally stable through the
outbreak with a subtle decrease between 1960 and 1970 while
%N increases slightly ca. 1960. The C/N ratio is stable during the
1930s Aquarius outbreak.
5.3. Markagunt Plateau
5.3.1. Alpine Pond (AP)
The spruce/r pollen ratio decreases coincident with the 1990s
Markagunt outbreak (Fig. 3). MS is variable throughout the record
and decreases during the 1990s Markagunt outbreak. Carbonate
increases slightly during the 1990s Markagunt outbreak. The
%org is variable over the 20th century though decreases during
the outbreak (Fig. 4). The d13CBOM versus C/N ratio scatter plot suggests sediments composed of lacustrine algae (Fig. 5). Linear
regression plots suggest an inorganic nitrogen component (Fig. 5)
and d15NTN values of this lake range from 1 to +2
(Fig. 3). The d13CBOM, d15NTN, %C, %N, and C/N ratio are variable over
the 20th century though all parameters decrease during the 1990s
Markagunt outbreak (Fig. 3).
5.3.2. Morris Pond (MP)
Beginning around 1980, the spruce/r pollen ratio begins a
decreasing trend before decreasing conspicuously during the outbreak (Fig. 3). The MS trend is variable over the 20th century with
no apparent response to the 1990s Markagunt outbreak (Fig. 3).
Carbonate exhibits some variability over 20th century with an increase evident during the 1990s outbreak. The %org increases towards modern with a steep increase during the outbreak. The
d13CBOM versus C/N ratio scatter plot suggests that organic matter
is composed of algal and terrestrial sources (Fig. 4). Linear regression plots suggest an inorganic nitrogen component (Fig. 5) and

d15NTN values range from 1 to +1 (Fig. 3). The d13CBOM
and d15NTN trends are variable with no obvious response during
the outbreak (Fig. 3). The %C, C/N ratio, and %N are variable over
the 20th century and decrease during the 1990s Markagunt
outbreak.
5.4. Statistical analyses
Seven response variables were tested using GLMMs. We elected
to test %N because of its relevance for our third hypothesis which
states that a pulse of nitrogen after an outbreak should cause signicant changes in nitrogen values of lake sediments. The variability existing among the six sites (Fig. 6) is quantied by the random
effects values provided in Table 1. Of the seven response variables,
three parameters differed signicantly under outbreak conditions
relative to the non-outbreak period: spruce/r ratio, MS, and
carbonate (Table 1). The spruce/r pollen ratio responded most
clearly across all six sites (p < 0.001). For the entire dataset, the
pollen ratio decreased by a factor of 2:1 between non-outbreak
and outbreak years after controlling for site effects (Fig. 7; Table 1).
Two parameters (%C and %org), were not tested because they vary
stoichiometrically with %N and are therefore strongly collinear.
6. Discussion
6.1. Sedimentary pollen ratio
Our rst hypothesis states that because spruce beetle outbreaks
result in loss of mature spruce across a landscape, then signicant
decreases in the ratio of spruce to r pollen should occur. Such
changes would be a useful proxy for detecting past outbreaks. This
hypothesis is based on qualitative observations of pollen shifts presented by Anderson et al. (2010), Morris et al. (2010), and Morris
and Brunelle (2012) but until now has not been statistically tested.
Visual inspection of the ratio data indicates that the spruce/r ratio
decreases contemporaneous with spruce beetle outbreaks (Figs. 3
and 6). Statistical analysis indicates support (p > 0.001) for our rst
hypothesis (Table 1). When all outbreaks are considered across all
sites, the spruce/r pollen decreases by a factor of 2:1 following the
onset of an outbreak (Fig. 7).
6.2. Sedimentary mineral, organic, and carbonate content
Our second hypothesis states that because reduced canopy
interception of precipitation results following post-outbreak needlefall, then increases in soil erosion and/or the mobilization of terrestrial carbon (i.e. woody litter, needles, frass, and boring dust)
will be detectable in lacustrine deposits. This is because lakes are
sensitive to terrestrial mineral and organic input resulting from
landscape disturbances (Gedye et al., 2000; Heiri et al., 2001;
Shuman, 2003). The second hypothesis is based on studies documenting post-outbreak increases in streamow, sediment runoff,
and accumulations of ne and coarse organic debris in surface
water and on the forest oor (Love, 1955; Bethlahmy, 1974,1975;
Potts, 1984; DeRose and Long, 2007; Klutsch et al., 2009). Our
results suggest that contributions of terrestrial organic material
(non-pollen) are not signicant in the sediments of these six basins
during outbreaks relative to non-outbreak periods. While the
erosion signal at some lakes appeared to initially support our
second hypothesis, for example increasing MS at BaL (Fig. 3), when
analyzed for the entire dataset overall MS decreased signicantly
during outbreaks (Table 1). This could be due at least three factors.
The rst is that four of the six records we examined correspond to
spruce beetle outbreaks that occurred during the 1990s (Wasatch
and Markagunt outbreaks). Core top samples are often occulent

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85

Fig. 5. Linear regression plots for %N and %C for the six basin in our study. If the regression line passes close to the origin (0, 0), then inorganic nitrogen is only a small
component of total nitrogen (Mller and Mathesius, 1999). All basins in our study appear to have considerable inorganic nitrogen since the regression does not pass through
the origin.

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J.L. Morris et al. / Forest Ecology and Management 289 (2013) 7889

and poorly-consolidated and could potentially be low in mineral

content. Second, decreased MS could result from increases in lake
productivity. Third, erosion is dependent on summer precipitation
(i.e. rainfall) and climate variables are not considered in our study.
Sedimentary carbonate in response to spruce beetle outbreaks
suggests that climate-driven hydrologic controls may be more
important than terrestrial landscape conditions. Even though proximal lakes presumably receive comparable precipitation, differences in carbonate accumulations were observed in nearby
basins (e.g. BL and EL). Carbonate in lake sediments is controlled
by lake water evaporation and also dissolution of parent bedrock.
The net decrease in carbonate observed during bark beetle outbreaks (Table 1) could be due in part to increasing dilution in these
basins from an increase in surface water ow into the lakes. Interpreting these results across basins is problematic due to differences in parent bedrock on these landforms where limestonedominates the Wasatch and Markagunt and basalt the Aquarius.
These two rock types have considerably different pH properties
that inuence soil, ground-, and surface-water reservoirs. Interactions between terrestrial organics inux and soil and water pH
could potentially alter pH conditions which would inuence
carbonate dissolution. Evaporation from lakes is also known to

inuence carbonate content in lake sediments, but could not be

accounted for here as climate variables are not considered in this
study.
6.3. Carbon and nitrogen uxes
Our third hypothesis states that because leaching of foliar nitrogen and increases in algal productivity occurs after post-outbreak
needlefall, then nitrogen values in lake sediments will also increase. Based on the work of Morehouse et al. (2008), we expected
the C/N ratio to decrease during all outbreaks from post-needlefall
leaching of nitrogen. Our results indicate that in general, d15NTN,
%N, and C/N ratio do not differ at a statistically signicant level between non-outbreak (0) and outbreak (1) statuses (Table 1). While
the C/N ratio did decrease at some sites, e.g. BL (Fig. 3), decreases
are not consistently observed across sites and generally did not exceed the range of 20th century variability (Fig. 6; Table 1). The C/N
ratio as an indicator of beetle disturbance is problematic for several
reasons. First these lakes are inuenced by inorganic nitrogen contributions (Fig. 5) that may be related to atmospheric saturation
from anthropogenic activities such as fossil fuel combustion (Wolfe
et al., 2003). Second, terrestrial carbon-rich material resulting from

Fig. 6. Plots of nine response variables examined for this study reporting median (central line), upper/lower quartile (boxes), maximum/minimum excluding outliers
(whiskers), and outliers (open circles). Samples from each lake were assigned to non-outbreak years (0) and outbreak years (1).

Table 1
Results of GLMM analyses examining the effects of spruce beetle population status (xed effect) and site (random effect). All intercepts are signicantly different from zero.
Response variable

Spruce/r ratio
MS
Carbonate (CaCO3)
%N
d15NTN
C/N ratio
d13CBOM

Fixed effects

Random effect

Intercept (Estimate SE)

Beetle status (Estimate SE)

0.50 0.10
1.34 0.58
10.91 4.37
1.30 0.15
0.87 0.26
12.12 1.10
18.25 5.22

0.45 0.06
0.52 0.17
0.88 0.42
0.11 0.06
0.18 0.11
0.36 0.34
0.23 0.33

<0.001
0.002
0.036
0.071
0.106
0.295
0.476

0.23
1.40
10.60
0.36
0.62
2.64
12.66

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87

no conspicuous response. In lakes with apparent increases in nitrogen during outbreaks relative to pre-outbreak samples, these nitrogen values did not differ signicantly from the range of variability
evident in pre-outbreak samples (Fig. 6). One potential explanation
is that the nitrogen signal could be saturated by inorganic nitrogen
deposition from the atmosphere related to human activities. Wolfe
et al. (2003) found that decreases in the C/N ratio and d15N correspond temporally to increases in anthropogenic activity in Colorado. Similar trends to those presented by Wolfe et al. (2003) are
apparent in examining the C/N ratio and d15N timeseries plots
(Fig. 3 Blue, Emerald, Purple and Morris). It is therefore conceivable
that the nitrogen signal may be receiving enrichment from atmospheric deposition of anthropogenic sources. Exploring the nitrogen signal prior to the 20th century and/or analytical
methodologies that isolate the inorganic nitrogen fraction may
be useful for assessing spruce beetle outbreaks and requires further study.
7. Summary and conclusions

Fig. 7. Spruce/r pollen ratios (mean 95% condence interval) for the endemic
and outbreak phases of the spruce beetle, predicted by generalized linear mixed
modeling for the populations of lakes sampled.

an outbreak (e.g. boring dust, needle fragments) is simultaneously

inuencing the C/N ratio. Third, Huber (2005) found that detecting
elevated nitrogen in surface water after outbreaks is confounded
by dilution. Increased surface water contributions to lakes after
outbreaks may complicate detection of episodic terrestrial nutrient
uxes in sediments. Fourth, Morehouse et al. (2008) notes that
elevated nitrogen levels in terrestrial soils are detectable for
only 12 years. This aspect is particularly problematic in lake
sediment records because sub-decadal resolution is rare in many
reconstructions (e.g. Brunelle et al., 2008), with the exception of
varved records where sediments accumulate in annual layers
(e.g. Appleby et al., 1979).
Our third hypothesis also stated that following an outbreak, we
expected to detect increased algal productivity in lake sediments.
Increases in algal productivity are known to increase nitrogen values in lake sediments (Robinson, 2001). Anderson et al. (2010) observed conspicuous increases in aquatic algal spore abundance in
lake sediments contemporaneous with the 1940s spruce beetle
outbreak on the White River Plateau in Colorado. However, Wolfe
et al. (2003) found increases in algal productivity in alpine and
subalpine lakes in Colorado beginning ca. 1930s that they attributed to the introduction of non-native salmonid sh. Salmonid
introduction (i.e. sh stocking) is also common in subalpine and alpine lakes throughout our study area in Utah, which is known to
affect nutrient cycling in high-elevation and high-latitude lakes
(Leavitt et al., 1994; Wolfe et al., 2003). Introduction of non-native
trout, in this case rainbow trout (Oncorhynchus mykiss), occurred in
the Wasatch and Aquarius lakes, though not in the Markagunt
ponds (Utah Department of Wildlife Resources, 2012). Fish introductions and annual stocking programs complicate interpreting
how nitrogen pools may reect terrestrial disturbances. Further,
it is known that sh introductions alone may trigger increases in
algal productivity (Leavitt et al., 1994).
The sediments in this study are dominated by lacustrine algae
(Fig. 4) though any increases in algae that may have occurred during outbreaks are not statistically signicant (Table 1). For example, d15NTN and %N values increased relative to pre-outbreak
samples at BL and EL while other records, e.g. BaL and PL, exhibited

Bark beetle outbreaks equal (Baker and Veblen, 1990) or exceed

(Logan and Powell, 2001) the ecological impacts of wildre, yet
surprising little is known about the recurrence and ecological role
of these insects prior to recent centuries. This is because, unlike re
disturbances, bark beetle outbreaks do not leave direct evidence in
sedimentary deposits (e.g. charcoal produced by re). It is therefore imperative that a methodology utilizing sedimentary proxies
be developed to assist in inferring past outbreaks. In this study
we contribute to a growing body of literature seeking to develop
a methodology for reconstructing spruce beetle disturbances
(Anderson et al., 2010; Morris et al., 2010; Morris and Brunelle,
2012). We tested three hypotheses based on observations of 20th
century outbreaks to determine which response variables may be
useful in paleoenvironmental reconstructions of past spruce beetle
outbreaks. To our knowledge this study is a novel application of
stable carbon and nitrogen isotopes for analyzing the outcomes
of bark beetle disturbances in lake sediments. Observations of ecological effects resulting from spruce beetle damage include reorganization of the terrestrial nutrient pool, relocation of organic
material, and increased surface and groundwater availability (e.g.
Morehouse et al., 2008). We expected to see evidence of similar
changes recorded in elemental, organic, and mineral constituents
in the lake sediment deposits. However, our analysis suggests that
basin-specic controls and anthropogenic activity confound the
geochemical and elemental indicators, despite similar forest composition and spruce mortality during outbreaks across sites.
The ratio of spruce to r pollen (host to non-host) responded
most clearly and consistently to spruce beetle disturbances in
our study and provide a framework for reconstructing past outbreaks. However, a high resolution sampling strategy for pollen
is required to detect spruce beetle disturbance. A pollen-based approach would greatly benet from supporting lines of evidence,
such as ancient DNA, biomarkers, and/or preserved insect remains.
Success using pollen analysis may be limited to ecosystems where
a canopy co-dominant host/non-host relationship exists. Because
tree-ring studies have successfully reconstructed spruce beetle disturbances prior to the historic period (e.g. Sherriff et al., 2011),
overlapping high-resolution pollen analysis with tree ring studies
may offer more temporally extensive datasets that would facilitate
rigorous statistical testing of pollen time series data.
Acknowledgements
This research was funded by awards from the Geological Society
of America, Association of American Geographers, and the National

88

J.L. Morris et al. / Forest Ecology and Management 289 (2013) 7889

Science Foundation (1032099) to Jesse Morris and by a grant from

the Joint Fire Science Program (063131) to Andrea Brunelle. We
thank Jennifer Watt for benecial discussions and A. Steve Munson
for sharing photographs. We extend our gratitude to Brad Erkkila
at SIRFER Lab (University of Utah) for consultation on stable
isotope analyses. This manuscript benetted from discussions with
John Marshall and Steve Perakis at the Paleo Reconstructions of
Biogeochemical Environments (PROBE) Workshop at Kansas State
University in Manhattan, Kansas (April 1921, 2012). We are
grateful to Hubert Sterba and two anonymous reviewers for
providing comments and suggestions that greatly improved our
manuscript.

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