This document summarizes a study that examined the photosynthetic efficiency of sapling trees across four common species in a disturbed northern Michigan forest. Light response curves and measurements of apparent quantum yield and maximum photosynthetic rate (Amax) were taken for 117 saplings across a disturbance gradient caused by girdling over 6700 trees. Amax was found to significantly increase over the disturbance gradient for red oak and American beech saplings. This suggests these species have a strong capacity to take advantage of canopy gaps, which may impact future forest composition. The physiological responses observed could help refine parameters in earth systems models regarding forest response to disturbance.

1. Leaf
physiology
response
across
a
disturbance
gradient
in
a
temperate
deciduous
forest:
Implications
for
earth
systems
modeling
Rick
Beckel1,
Chris
Vogel2
Abstract
Light
response
curves
were
constructed
in
situ
for
117
sapling
trees
(between
1
and
7
m
in
height)
of
four
common
tree
species
in
a
disturbed
northern
Michigan
deciduous
forest.
Saplings
were
examined
in
a
manipulated
area
(University
of
Michigan
Biological
Station’s
“Forest
Accelerated
Succession
Experiment)
in
which
>6700
Populus
(aspen)
and
Betula
(birch)
trees
were
stem-­‐girdled
within
a
39-­‐ha
area
to
identify
mechanisms
responsible
for
sustaining
C
uptake
through
partial
canopy
defoliation.
In
this
study,
physiological
parameters
of
apparent
quantum
yield
and
Amax
–
measures
of
photosynthetic
efficiency
–
were
examined
across
a
disturbance
gradient
that
could
help
explain
maintenance
of
carbon
uptake
rates
of
the
manipulated
area.
Amax
was
significantly
different
across
species,
and
Amax
increased
significantly
over
a
disturbance
gradient
(modeled
by
fraction
basal
area
senesced)
considering
all
species
in
aggregate
(p
<
.1).
Examining
this
trend
at
the
species
level
revealed
significance
in
red
oak
and
American
beech,
and
was
nearly
significant
for
white
pine
(p
<
.15).
Red
oak
had
a
slightly
but
significantly
lower
apparent
quantum
yield
than
the
other
species,
but
this
parameter
did
not
vary
over
a
disturbance
gradient
for
any
species.
The
strong
physiological
response
of
white
pine
and
particularly
red
oak
suggests
a
strong
capacity
to
take
advantage
of
canopy
gaps
created
by
successional
patterns
or
climate-­‐related
disturbance
events,
and
may
improve
chances
of
sapling
success
and
allow
for
greater
representation
in
future
forest
composition
in
the
area.
The
trends
suggested
by
the
data
may
be
of
use
to
earth
systems
modelers
interested
refining
the
physiological
parameters
of
their
models
in
response
to
disturbance.
Introduction
Forests
worldwide
represent
a
significant
terrestrial
carbon
sink,
absorbing
a
substantial
fraction
of
carbon
dioxide
and
thereby
moderating
the
extent
of
global
climate
change
(Nemani
et
al.
2003,
Dixon
et
al.
1994,
Purves
and
Pacala
2008).
However,
the
1
Macalester
College
2
University
of
Michigan
Biological
Station

2. future
trajectory
of
this
carbon
sink
is
uncertain
in
an
era
of
increasing
disturbances
directly
and
indirectly
related
to
global
change:
alterations
in
temperature
and
precipitation
patterns
may
render
habitat
unsuitable
for
current
residents,
and
increases
in
severe
weather
patterns
will
lead
to
changes
at
the
landscape
and
local
levels
through
drought,
wildfire,
and
wind
damage.
Changing
climactic
conditions
may
also
alter
and/or
extend
the
range
of
pathogens
or
other
pests
that
target
specific
tree
species
or
entire
forests
(Dale
et
al.
2001).
Emergent
dynamic
global
vegetation
models
seek
to
emulate
biogeochemical
trends
of
forests
worldwide
to
elucidate
how
forest
behavior
may
affect
earth’s
response
to
climate
change.
However,
model
predictions
are
highly
uncertain
and
frequently
contradictory,
and
better
parameters
of
disturbance
and
physiology
are
needed
to
forecast
forest
ecosystems’
interactions
with
a
changing
climate
(Purves
and
Pacala
2008).
The
future
contribution
of
forests
in
the
upper
Midwest
to
the
global
carbon
cycle
is
particularly
uncertain
compared
to
other
older
forests
worldwide.
In
most
areas
across
the
globe,
forests
are
in
a
relatively
stable
state
of
production
due
to
their
age,
whereas
forests
in
the
upper
Midwest
are
undergoing
dynamic
succession,
due
to
their
unique
ecological
history.
Forests
of
the
upper
Midwest,
which
was
widely
impacted
by
clearcuts
and
fires
in
the
late
19th
and
early
20th
centuries,
are
rapidy
changing
where
early
successional
species
across
the
region
are
beginning
to
senesce
(Hardiman
et
al.
2013,
Gough
et
al.
2010).
Though
forests
of
the
upper
Midwest
have
acted
as
a
net
assimilator
of
CO2
in
the
past
century
and
remain
so
today,
their
status
as
a
sink
or
source
is
uncertain
during
and
after
these
expected
successional
changes
(Hardiman
et
al.
2013,
Gough
et
al.
in
preparation).
The
trajectory
and
magnitude
of
this
area’s
potential
as
a
carbon
sink
is
increasingly
important
to
understand
in
an
era
of
considerable
emissions
of
carbon
dioxide,
the
nascent
interest
in
carbon
trading
schemes
both
nationally
and
internationally,
and
building
more
accurate
climate
and
earth
systems
models.
Our
understanding
of
forest
carbon
sequestration
potential
is
mostly
understood
in
terms
of
disturbance
and
succession.
Classical
models
suggest
that
early
successional
forests
have
the
highest
rates
of
net
ecosystem
production,
and
that
as
earlier
successional
trees
decline
and
die,
a
steady
state
old
growth
forest
develops
which
ceases
to
accumulate
carbon,
and
may
even
become
a
carbon
source
(Luyssaert
2008).
However,
this
model
may

3. not
be
applicable
worldwide,
and
there
is
evidence
to
suggest
that
current
successional
trends
in
mixed
deciduous
forests
of
the
upper
Midwest
may
actually
be
increasing
net
ecosystem
production
beyond
its
early
successional
capacity
(Luyssaert
2008,
Gough
et
al.,
in
preparation).
Additional
uncertainty
is
created
because
our
knowledge
of
how
production
responds
to
disturbance
is
mostly
limited
to
severe
disturbance;
less
is
known
about
moderate
disturbance
that
targets
a
subset
of
trees
in
the
forest,
either
by
disease,
severe
weather,
or
successional-­‐related
senescence
(Goodrich-­‐Stuart
et
al.
2014).
Further
study
is
needed
on
these
types
of
impacts
as
we
move
away
from
direct
anthropogenic
disturbance
from
logging
and
associated
fires
into
an
era
of
primarily
moderate
disturbances
resulting
from
natural
processes
and
human-­‐induced
climate
change.
In
the
FASET
(Forest
Accelerated
Succession
ExperiemenT)
study,
~35%
of
total
LAI
and
basal
area
was
removed
by
stem
girdling
all
early
successional
trees
(>6,700
individuals
in
a
39
area)
in
a
northern
Michigan
forest
to
evaluate
the
impacts
of
moderate
disturbances
on
carbon
storage
potential.
Researchers
hypothesized
that
NEP
would
decrease
immediately
and
temporarily
after
moderate
disturbance
and
consequently
rise
above
earlier
levels
of
production
as
later
successional
species
developed
due
to
the
forest’s
increased
structural
complexity.
However,
an
insignificant
dip
in
production
after
the
disturbance
was
observed,
and
subsequent
research
has
suggested
that
both
the
upper
canopy
and
subcanopy
can
sustain
production
following
low
to
moderate
levels
of
disturbance
(Nave
et
al.
2011,
Gough
et
al.
2013,
Goodrich-­‐Stuart
et
al.
2014)
Investigators
are
currently
studying
mechanisms
for
how
forests
sustain
production
immediately
following
disturbance.
Increased
canopy
complexity
is
thought
to
be
a
driver
in
continuously
growing
production
in
older
forests,
but
it
is
unlikely
that
complexity
will
increase
immediately
following
disturbance
to
compensate
for
production
losses
from
early
successional
canopy
trees
(Hardiman
et
al.
2011,
Hardiman
et
al.
2013).
Increased
nitrogen
availability
due
to
reduced
competition
by
recently
deceased
trees
also
had
an
impact
on
sustained
carbon
uptake
(Nave
et
al.
2011).
But
the
major
reason
for
this
maintenance
may
be
due
to
the
creation
of
canopy
gaps
following
senescence,
which
may
allow
for
two
mechanisms
for
sustaining
production:
better
light
distribution
to
other
canopy
strata
due
to
changing
canopy
structure,
or
favorable
physiological
changes
in
response
to
disturbance.
This
study
focuses
in
particular
on
the
physiological
changes
that

4. may
be
occurring
at
the
leaf
level
to
compensate
for
upper
canopy
losses.
Light
dynamics
in
canopy
gap
areas
are
important
to
explore
because
it
is
uncertain
to
what
extent
disturbances
in
the
canopy
level
influence
physiology
and
morphology
at
the
leaf
level,
but
studies
suggest
that
light
harvesting
improves
with
mortality
driven
canopy
disturbances
(Hardiman
et
al.
2011)
and
that
leaf-­‐level
adjustments
are
proportional
to
the
level
of
change
in
the
local
light
environment
from
upper
canopy
gap
formation
(Goodrich-­‐Stuart
et
al.
2014).
The
latter
study
found
that
maximum
photosynthesis
potential
increases
as
gap
size
increased;
all
dominant
species
displayed
a
direct
positive
relationship
of
light
saturated
net
CO2
assimilation
(Amax)
to
disturbance
severity.
However,
it
is
unclear
how
quantum
yield
(α)
–
a
metric
of
photosynthetic
efficiency
that
illustrates
how
quickly
a
tree
can
reach
its
photosynthetic
capacity
–
changes
across
a
gradient
of
canopy
gap
sizes
or
disturbance
levels.
Species
with
higher
quantum
yield
values
could
develop
more
successfully
in
disturbed
areas
and
eventually
become
canopy
dominant
species.
This
study
thus
seeks
to
explore
how
differential
structural
changes
in
the
forest
canopy
impact
trees
at
a
physiological
level,
and
how
these
physiological
changes
may
feedback
to
influence
future
forest
structure
and
composition.
We
explored
how
a
gradient
of
disturbance
impacts
two
important
physiological
parameters
(Amax
and
apparent
quantum
yield)
for
several
common
species
in
the
area,
and
use
our
findings
to
make
suggestions
explaining
why
certain
species
may
outcompete
others
in
this
ecosystem
post-­‐disturbance.
Performing
our
study
in
a
manipulated
area
with
a
gradient
of
disturbance
severity,
we
sought
to
test
the
following
hypotheses:
1)
That
gap
size
and
disturbance
level
would
correlate
positively
with
Amax
2)
that
as
gap
size
increased,
red
oak
would
exhibit
a
relatively
smaller
decrease
in
quantum
yield
compared
to
red
maple
due
to
its
generally
stronger
physiological
performance
(Sullivan
et
al.
1996).
Materials
and
Methods
Study
Site
This
study
took
place
in
a
mixed
deciduous
forest
in
Northern
Lower
Michigan
(45°
35’
N
84°
43’
W).
The
mean
annual
temperature
is
5.58°
C
and
mean
annual
precipitation
is
817
mm
(1942–2003)
(Gough
et
al
2013).
Following
massive
disturbances
(clearcuts
and

5. forest
fires)
in
the
past
two
centuries,
this
region
has
become
primarily
dominated
by
early
the
successional
species
bigtooth
aspen
(Populus
grandidentata),
trembling
aspen
(Populus
tremuloides)
and
paper
birch
(Betula
papyrifa).
Other
canopy
species
include
red
oak
(Quercus
rubra),
red
maple
(Acer
rubrum),
sugar
maple
(Acer
saccharum),
eastern
white
pine
(Pinus
Strobus),
and
American
beech
(Fagus
grandifolia).
Stem
density
of
trees
≥8
cm
dbh
is
700–
800
individuals/ha,
basal
area
is
25
m2/ha,
and
leaf
area
index
(LAI)
averages
3.5.
Red
maple,
red
oak,
eastern
white
pine,
and
American
beech
are
the
prominent
species
composing
the
subcanopy;
they
are
joined
by
other
shade
tolerant
species
such
as
sugar
maple,
red
pine
(Pinus
resinosa),
striped
maple
(Acer
pensylvanicum),
American
hophornbeam
(Ostrya
virginiana),
and
serviceberry
(Amelanchier
arborea).
The
early
successional
species
defined
above
are
in
decline
as
they
reach
the
end
of
their
lifespan,
leaving
room
for
other
species
to
gain
prominence
in
the
canopy.
To
evaluate
the
effects
of
disturbance
and
successional
changes
on
carbon
pools
and
fluxes
in
this
ecosystem
type,
the
University
of
Michigan
Biological
Station
implemented
the
FASET
program
in
2008.
This
large-­‐scale
manipulation
has
hastened
the
development
of
a
forest
composition
that
will
dominate
the
region
in
the
coming
decades
as
succession
proceeds
naturally
(Gough
et
al.
2013,
Nave
et
al.
2011).
To
better
understand
the
implications
of
canopy
gaps
left
by
senescing
early
successional
species,
this
study
examines
trees
across
a
gradient
of
disturbance
levels
in
FASET.
We
chose
10
out
of
21
permanent
0.08
ha
circular
plots
based
on
pre-­‐disturbance
production
and
species
composition
in
order
to
minimize
confounding
variables
(Goodrich-­‐
Stuart
et
al.
2014).
Plots
ranged
in
disturbance
severity
from
.09
to
.64
fraction
basal
area
senesced,
a
range
representative
of
the
differential
early
successional
die-­‐off
expected
in
the
region.
Four
non-­‐overlapping
5
m
radius
subplots
were
established
on
the
cardinal
axis
of
each
plot.
We
sampled
three
saplings
in
each
plot
to
measure
apparent
quantum
yield
and
Amax.
Leaf
Physiology
Analysis
To
establish
the
impact
of
canopy
openness
on
leaf
physiology,
we
constructed
a
light
response
curve
for
three
species
within
each
subplot,
measuring
carbon
dioxide
assimilation
rates
at
a
range
of
irradiance
levels.
We
studied
common
saplings
species
that

6. had
the
potential
to
eventually
extend
into
the
canopy.
Eligible
saplings
were
between
1
and
6.5
m
tall
and
under
3
cm
dbh;
their
size
suggests
that
these
trees
were
in
the
subcanopy
prior
to
the
stem-­‐girdling
disturbance.
Three
saplings
were
randomly
selected
in
each
subplot
for
measurement
with
descending
priority
of
oak,
maple,
pine
and
beach..
A
leaf
at
the
top
of
each
sapling
was
selected
for
measuring
photosynthesislight
response
curves
using
a
LiCor
LI-­‐6400
Portable
Photosynthesis
System
(model
LI-­‐6400,
LI-­‐
COR,
Lincoln,
NE,
USA).
Leaves
were
subjected
to
varying
irradiance
levels
(1500,
750,
500,
250,
75,
50,
30,
10,
0
μmol
photons/m2/s)
using
a
6400-­‐02
red-­‐blue
LED
light
source
(LI-­‐
COR,
Lincoln,
NE,
USA)
–
special
emphasis
was
placed
on
the
initial
slope
of
the
light
response
curve
(i.e.
5
points
under
100
μmol
photons/m2/s)
to
allow
for
precise
computation
of
apparent
quantum
yield.
For
each
broadleaf,
a
2
by
3
cm
area
was
enclosed
in
the
LiCor-­‐6400
chamber
to
monitor
its
carbon
assimilation
rate
at
a
constant
area.
For
examination
of
Pinus
strobus,
we
used
three
five-­‐needle
fascicles
from
the
previous
year's
growth,
laid
across
the
cuvette
in
a
non-­‐overlapping
manner.
Pine
photosynthesis
measurements
were
post-­‐processed
to
correct
for
area
since
15
needles
never
completely
filled
the
cuvette.
We
controlled
immediate
environmental
conditions
in
the
chamber
by
setting
the
LiCor-­‐6400’s
CO2
mixer
to
380
ppm,
and
made
an
effort
to
stabilize
relative
humidity
of
the
sample
between
60
and
70%
and
maintain
a
leaf
temperature
of
24
+/-­‐
1.5
degrees
C.
IRGAs
were
matched
and
conditions
were
allowed
to
stabilize
in
the
chamber
before
photosynthesis
readings
were
taken
at
each
light
level
(minimum
2
minute
stabilization
period).
Data
processing
and
statistical
analysis
Light
curves
were
constructed
using
the
physiology
data
collected
using
the
rectangular
hyperbolic
function::
P
=
(α*Amax*I)/
(Amax
+
α*I)
(adapted
from
Gough
et
al.
2013).
Where
P
is
photosynthesis
(µmol
CO2·m-­‐2·s-­‐1,
α
is
apparent
quantum
yield
(mol
CO2/mol
quanta)
and
I
is
the
irradiance
level
(µmol
quanta·m-­‐2·s-­‐1).
Apparent
quantum
yield
is
the

7. 0
0.02
0.04
0.06
0.08
0.1
Red
Maple
American
Beech
White
Pine
Red
Oak
Apparent
Quantum
Yield
(µmol
CO2/m2/s)
0
2
4
6
8
10
12
Red
Maple
American
Beech
White
Pine
Red
Oak
Amax
(µmol
CO2/m2/s)
Figure
2:
A
max
by
species.
Different
letters
denote
significance
at
p
<
.1.
Error
bars
represent
+/-­‐
1
standard
error
Figure
3:
Quantum
yield
by
species.
Different
letters
denote
significance
at
p
<
.1.
Error
bars
represent
+/-­‐
1
standard
error
b
ab
a
ab
a
b
b
a b
a
ab
a
b
parameter
describing
the
initial
slope
of
the
rectangular
hyperbolic
function,
and
Amax
is
where
the
function
plateaus.
Regression
analysis
was
used
to
determine
relationships
of
α
and
Amax
across
disturbance
gradients
and
analysis
of
variance
with
Tukey’s
HSD
test
to
determine
differences
between
species
(SAS
Institute
2012).
Results
118
saplings
were
sampled
in
the
field,
117
viable
light
response
curves
were
used
in
the
following
analysis.
Although
prioritized
during
field
tests,
there
was
a
dearth
of
oak
saplings
in
the
plots
sampled,
and
total
sample
size
across
the
40
subplots
was
16.
White
pine
was
sampled
most
frequently
at
n
=
37,
followed
by
red
maple
(n
=
37)
and
American
beech
(n
=
22).
When
examining
the
average
light
response
curves
for
each
species,
we
found
red
oak
to
have
significantly
higher
Amax
values
than
beech
and
red
maple
(p
<
.1),
although
not
significantly
higher
than
white
pine
(figure
2).
Red
oak
had
a
significantly
lower
quantum
yield
than
all
species
except
beech.
Figure
1:
Average
light
response
curves
across
all
disturbance
levels
for
the
four
species
of
saplings
sampled
in
the
study
area.
-­‐2
0
2
4
6
8
10
12
0
500
1000
1500
Photo
(µmol
CO2/m2/s)
Irradiance
(µmol
photons/m2/s)
Red
Oak
Red
Maple
White
Pine
American
Beech

8. R²
=
0.0086
0
5
10
15
20
0
0.2
0.4
0.6
0.8
Fraction
Basal
Area
Senesced
Red
Maple
R²
=
0.32156
0
5
10
15
20
0
0.2
0.4
0.6
0.8
American
Beech**
R²
=
0.13859
0
5
10
15
20
0
0.2
0.4
0.6
0.8
Amax
(µmol
CO2/m2/s)
Fraction
Basal
Area
Senesced
White
Pine*
R²
=
0.19529
0
5
10
15
20
0
0.2
0.4
0.6
0.8
Amax
(µmol
CO2/m2/s)
Red
Oak**
Fig.
4:
Regression
analysis
of
A
max
versus
fraction
basal
area
senesced.
Regressions
for
red
oak
and
American
beech
were
significant
at
p
<
.1;
white
pine
was
significant
at
p
<
.15
Examining
these
parameters
across
the
disturbance
gradient
yielded
interesting
results.
According
to
a
regression
analysis,
there
was
significant
positive
relationship
between
Amax
versus
fraction
of
basal
area
senesced
for
all
species
(p
<
.1,
R2
=
.205).
This
positive
relationship
–
increasing
Amax
values
with
increasing
disturbance
–
held
across
all
species
but
red
maple
to
a
significant
degree
(p
<
.1
for
red
oak
and
American
Beech,
p
<
.15
for
white
pine,
see
figure
4).
Regression
analysis
indicated
no
significant
trend
between
α
versus
fraction
of
basal
area
senesced
(figure
5).

9. R²
=
0.0815
0
0.02
0.04
0.06
0.08
0.1
0.12
0
0.2
0.4
0.6
0.8
Quantum
Yield
(µmol
CO2/m2/s)
Red
Oak
R²
=
0.17119
0
0.02
0.04
0.06
0.08
0.1
0.12
0
0.2
0.4
0.6
0.8
American
Beech
R²
=
0.02045
0
0.02
0.04
0.06
0.08
0.1
0.12
0
0.2
0.4
0.6
0.8
Quantum
Yield
(µmol
CO2/m2/s)
Fraction
Basal
Area
Senesced
White
Pine
R²
=
0.067
0
0.02
0.04
0.06
0.08
0.1
0.12
0
0.2
0.4
0.6
0.8
Fraction
Basal
Area
Senesced
Red
Maple
Fig.
5:
Regression
analysis
of
quantum
yield
versus
fraction
basal
area
senesced.
Regressions
were
not
significant
(p
>
.15)
Discussion
Investigators
at
this
site
have
noted
that
production
has
been
sustained
despite
the
loss
of
all
canopy-­‐dominant
early
successional
species
(Nave
et
al.
2011,
Gough
et
al.
2013)
and
the
purpose
of
this
study
was
to
explore
possible
physiological
mechanisms
driving
this
trend.
The
physiological
response
to
disturbance
has
implications
for
the
viability
of
individual
species
as
the
ecosystem
develops
into
a
later
successional
forest,
as
well
as
the
overall
trend
of
the
forest
as
a
carbon
sink
or
source.
Trees
species
with
physiologies
better
adapted
to
taking
advantage
of
canopy
gaps
are
at
a
competitive
advantage
relative
to
other
species.
Areas
of
the
forest
that
are
affected
by
gap-­‐forming
disturbance
experience
an
influx
of
light,
and
those
species
that
are
best
able
to
harvest
this
incoming
light
will
be
most
successful
in
the
gap,
growing
from
saplings
to
canopy
trees
as
the
forest
ages.
This
study
suggests
that
Red
Oak
may
be
at
a

10. comparative
advantage
over
other
major
subcanopy
trees.
Red
Oak
had
a
significantly
higher
Amax
and
lower
quantum
yield
than
other
species.
This
combination
is
illustrative
of
a
typical
sun-­‐adapted
leaf,
and
similar
relationships
between
high
Amax
and
low
apparent
quantum
yield
(and
vice
versa)
have
been
well
documented
(Muraoka
et
al.
2003,
Kubiske
and
Pregitzer
1996).
Even
in
areas
where
the
seedling
is
not
in
a
large
canopy
gap,
high
A-­‐
max
values
allow
the
leaf
to
assimilate
large
amounts
of
carbon
during
sunflecks
(Muraoka
et
al.
2003).
This
physiological
capability
of
oak
may
allow
the
species
to
take
advantage
of
canopy
gaps
most
effectively.
The
claim
that
red
oaks
may
be
most
poised
to
take
advantage
of
disturbance
may
seem
inconsistent
with
the
sampling
done
in
this
study,
since
only
16
eligible
saplings
were
found
out
of
117
total
trees.
The
reason
for
this
discrepancy
is
that
all
of
the
saplings
studied
were
alive
at
the
time
of
the
manipulation
in
2008;
the
distribution
and
abundance
of
trees
eligible
for
study
(1-­‐6.5
m
tall)
was
not
impacted
by
the
disturbance.
It
remains
to
be
seen
how
younger
trees
–
not
yet
sprouted
at
the
time
of
disturbance
–
respond
to
the
treatment.
This
study
suggests
that
oaks
may
be
most
successful
in
harvesting
the
light
made
available
by
formation
of
canopy
gaps.
Species
that
are
less
adept
at
attaining
a
higher
Amax
–
such
as
red
maple,
whose
Amax
was
relatively
flat
across
the
disturbance
gradient
–
will
be
at
a
disadvantage
during
disturbance.
Considering
all
the
trees
studied
in
aggregate,
Amax
increased
significantly
across
the
disturbance
gradient,
which
suggests
that
this
parameter
adjusts
to
differing
light
levels
in
the
subcanopy.
This
corroborates
other
recent
studies
at
this
location
suggesting
a
direct
positive
relationship
between
disturbance
level
and
Amax
(Goodrich-­‐Stuart
et
al.
2014).
Although
Amax
changes
in
response
to
disturbance
(becoming
more
like
sun-­‐leaves)
to
assimilate
more
carbon
dioxide
from
the
atmosphere,
the
other
physiological
parameter
examined,
apparent
quantum
yield,
showed
no
relationship
with
fraction
of
basal
area
senesced.
This
lack
of
response
to
disturbance
suggests
that
this
parameter
does
not
help
to
explain
the
maintenance
of
production
post-­‐disturbance.
Since
quantum
yield
did
not
respond
to
disturbance
and
Amax
does
not
explain
all
of
the
variation
found
in
photosynthesis
rates
at
the
leaf
level,
other
factors
must
explain
the
overall
compensation
for
production
losses
due
to
disturbance.
Much
of
this
can
likely
be
attributed
to
structural
and
light
distribution
patterns,
rather
than
physiological
changes.
Light
that
is
primarily
captured
by
the
top
layers
of
the
canopy
is
used
inefficiently
because
many
of
the
leaves

11. receiving
direct
sunlight
are
unable
to
assimilate
more
CO2
than
is
allowed
by
their
saturation
level
(Amax).
As
individuals
composing
the
canopy
senesce,
canopy
gaps
are
created
which
allow
light
to
penetrate
the
forest
in
novel
ways
and
reach
formerly
light
limited
strata
(Gough
et
al.
2010).
Shade-­‐adapted
leaves
in
lower
levels
of
the
canopy
are
able
to
take
advantage
of
these
small
increases
in
light
levels
and
move
along
their
response
curves
toward
their
Amax,
which
causes
an
overall
increase
in
carbon
dioxide
assimilated
by
the
forest.
Discussion
of
the
future
trajectory
of
growth
and
carbon
storages
of
forests
in
the
upper
Midwest
may
be
of
interest
to
earth
systems
modelers,
forest
managers,
and
policymakers.
Earth
systems
modelers
are
interested
in
refining
their
models
to
better
predict
the
behaviors
of
carbon
fluxes
and
pools,
so
it
is
therefore
important
to
investigate
parameters
and
ecosystems
that
present
uncertainty
in
their
models.
Disturbances
in
the
upper
Midwest
due
to
dynamic
succession
may
lead
to
changes
in
forest
physiology
and
structure,
which
in
turn
impact
rates
of
CO2
uptake.
Establishing
the
extent
to
which
these
factors
are
changing
is
important
so
modelers
can
decide
whether
or
not
to
incorporate
these
changes
into
already
complex
models.
For
example,
the
Biome-­‐BGC
Terrestrial
Ecosystem
Process
Model,
which
estimates
fluxes
and
storage
of
energy
and
macronutrients
for
terrestrial
ecosystems,
assumes
a
fixed
apparent
quantum
yield
over
the
course
of
forest
development
(Gough,
personal
communication,
August
8,
2014).
The
present
study
suggests
that
this
is
appropriate
since
no
change
in
quantum
yield
was
observed
across
a
disturbance
gradient
for
any
species.
This
same
model,
however,
predicted
a
decline
of
production
in
FASET,
so
the
model
is
not
complete
–
there
are
mechanisms
yet
to
be
explained,
and
further
study
of
physiological
and
structural
changes
of
forests
are
necessary
to
forecast
an
accurate
global
trajectory
of
atmospheric
CO2.

12. Acknowledgements
I
would
first
and
foremost
like
to
thank
the
National
Science
Foundation
for
the
funding
of
this
project
through
the
“Biosphere-­‐Atmosphere-­‐Hydrosphere
Interactions
in
a
Changing
Global
Environment”
Research
Experience
for
Undergraduates
program.
Special
thanks
to
Dave
Karowe
and
Mary
Anne
Carroll
for
directing
this
program
and
offering
advice
on
experimental
design.
Chris
Vogel
acted
as
the
mentor
for
this
REU
experience,
with
Chris
Gough
also
playing
an
important
advisor
role.
Thanks
to
Jason
Tallant
and
Adam
Levick
for
their
help
with
data
processing.
Thanks
to
the
staff
at
University
of
Michigan
Biological
station
for
providing
the
resources
and
facilities
that
made
this
research
possible.
Thanks
to
the
eight
other
undergraduates
that
make
up
the
REU
cohort
at
UMBS
who
offered
support
throughout
the
project.
Literature
Cited
Dale,
V.H.,
L.A.
Joyce,
S.
McNulty,
R.P.
Neilson,
M.P.
Ayres,
M.D.
Flannigan,
P.J.
Hanson,
et
al.
2001.
Climate
Change
And
Forest
Disturbances.
Bioscience,
51:
723-­‐734.
Dixon,
R.K.,
A.M.
Solomon,
S.
Brown,
R.A.
Houghton,
M.C.
Trexier,
J.
Wisniewski.
1994.
Carbon
pools
and
flux
of
global
forest
ecosystems.
Science,
263,
5144,
185-­‐90.
Goodrich-­‐Stuart,
E,
P.S.
Curtis,
R.T.
Fahey,
C.S.
Vogel,
C.M.
Gough.
2014.
Forest
net
primary
production
resistance
across
a
gradient
of
moderate
disturbance.
Masters
Thesis,
Virginia
Commonwealth
University.
Paper
627.
Gough,
C.M.,
B.S.
Hardiman,
L.E.
Nave,
G.
Bohrer,
K.D.
Maurer,
C.S.
Vogel,
K.J.
Nadelhoffer,
P.S.
Curtis.
2013.
Sustained
carbon
uptake
and
storage
following
moderate
disturbance
in
a
Great
Lakes
forest.
Ecological
Applications,
23:
12012-­‐1215.
Gough,
C.M.,
B.S.
Hardiman,
P.S.
Curtis.
2010. Wood
net
primary
production
resilience
in
an
unmanaged
forest
transitioning
from
early
to
middle
succession.
Forest
Ecology
and
Management,
260:
36-­‐41.
Gough,
C.M.,
P.S.
Curtis,
B.S.
Hardiman,
C.M.
Scheuermann.
Carbon
storage
across
stand
development
in
North
America’s
temperate
deciduous
forests:
shifting
paradigms
and
management
options.
Frontiers
in
Ecology
and
the
Environment,
in
preparation.
Hardiman,
B.S.,
G.
Bohrer,
C.M
Gough,
C.S.
Vogel,
P.S.
Curtis.
2011.
The
role
of
canopy
structural
complexity
in
wood
net
primary
production
of
a
maturing
northern
deciduous
forest.
Ecology,
92:
1818-­‐1827.
Hardiman,
B.S.,
C.M.
Gough,
B.
Halperin.
2013.
Maintaining
high
rates
of
carbon
storage

13. in
old
forests:
A
mechanism
linking
canopy
structure
to
forest
function.
Forest
Ecology
and
Management,
298:
111-­‐119.
Kubiske,
M.E.
and
K.S.
Pregitzer.
1996.
Effects
of
elevated
CO2
and
light
availability
on
the
photosynthetic
light
response
of
trees
of
contrasting
shade
tolerance.
Tree
Physiology,
16:
351-­‐358.
Luyssaert,
S.,
E.D.
Schulze,
A.
Börner,
A.
Knohl,
D.
Hessenmöller,
B.
E.
Law,
P.
Ciais,
and
J.
Grace.
2008.
Old
growth
forests
as
global
carbon
sinks,
Nature,
455:
213–215.
Muraoka,
H,
H.
Koizumi,
R.W.
Pearcy.
2003.
Leaf
display
and
photosynthesis
of
tree
seedlings
in
a
cool
temperate
deciduous
broadleaf
forest
understorey.
Oecologica,
135:
500-­‐509.
Nave,
L.
E.,
et
al.
2011.
Disturbance
and
the
resilience
of
coupled
carbon
and
nitrogen
cycling
in
a
north
temperate
forest.
Journal
of
Geophysical
Research:
Biogeosciences
116.
Nemani,
R.
R.,
C.D.
Keeling,
H.
Hashimoto,
W.M.
Jolly,
S.C.
Piper,
C.J.
Tucker,
R.B.
Myneni,
S.W.
Running.
2003.
Climate-­‐driven
increases
in
global
terrestrial
net
primary
production
from
1982
to
1999.
Science,
300:
1560-­‐3.
Purves,
D.,
and
S.
Pacala.
2008.
Predictive
Models
of
Forest
Dynamics.
Science,
320:
1452-­‐
1453.
Sullivan,
N.H.,
P.V
Bolstad,
J.M.
Vose.
1996.
Estimates
of
net
photosynthetic
parameters
for
twelve
tree
species
in
mature
forests
of
the
southern
Appalachians.
Tree
Physiology,
16:
397-­‐406.