Nitrogen deposition and
extinction risk in carnivorous
plants: ecological challenges
for the next century
Nicholas J. Gotelli
Department of Biology
University of Vermont
Burlington, VT 05405
U.S.A.
Teragrams of Nitrogen
200
Total anthropogenic N fixed
150
Natural range
100
50
Fertilizer
0
1900
1920
1940
1960
Year
NOx
1980
2000
Effects of N Deposition
• Individual
Altered morphology
Changes in reproduction, survivorship
Effects of N Deposition
• Individual
Altered morphology
Changes in reproduction, survivorship
• Population
Increased long-term extinction risk
Changes in short-term dynamics
Effects of N Deposition
• Individual
 Altered morphology
 Changes in reproduction, survivorship
• Population
 Increased long-term extinction risk
 Changes in short-term dynamics
• Community
 Changes in abundance and composition
 Altered nutrient transfer and storage
Effects of N Deposition on
Carnivorous Plants
•
•
•
•
•
Life History
Effects on Individuals
Effects on Populations
Effects on Communities
The Role of Ecologists
Effects of N Deposition on
Carnivorous Plants
•
•
•
•
•
Life History
Effects on Individuals
Effects on Populations
Effects on Communities
The Role of Ecologists
Carnivorous plants: wellknown, but poorly studied
Carnivory in plants
• Phylogenetically diverse
• Morphological, chemical adaptations for
attracting, capturing, digesting
arthropods
• Common in low N habitats
• Poor competitors for light, nutrients
Family Sarraceniaceae
Genus
Common
Name
Number of
Species
Distribution
Darlingtonia
Cobra Lilly
1
Northwest USA
Heliamphora
Sun Pitchers
5
North-central
South America
Sarracenia
Pitcher Plants
8
Eastern USA,
Canada
Genus Sarracenia
•
•
•
•
•
8 described species
Center of diversity in southeastern US
Many subvarieties
Extensive hybridization
Sarracenia purpurea (New JerseyCanada)
The Northern Pitcher Plant
Sarracenia purpurea
• Perennial plant of
low-N peatlands
• Lifespan 30-50 y
• Arthropod prey
capture in waterfilled pitchers
• Diverse inquiline
community in
pitchers
Sarraceniopus gibsoni
Wyeomyia smithii
The Inquilines
Blaesoxipha fletcheri
Habrotrocha rosa
Metriocnemus knabi
Inquiline food web
Phyllodia
• Flat leaves
• No prey capture
• High concentration
of chlorophyll,
stomates
• Photosynthetically
more efficient than
pitchers
Flowering Stalks
• Single stalk per
rosette
• Flowering after
3 to 5 years
• Bumblebee, fly
pollinated
• Short-distance
dispersal of seeds
Leaf Senescence
• End-of-season die
off
• Production of new
leaves in following
spring
• Annual increase in
rosette diameter
Effects of N Deposition on
Carnivorous Plants
•
•
•
•
•
Life History
Effects on Individuals
Effects on Populations
Effects on Communities
The Role of Ecologists
Nutrient Treatments
•
•
•
•
•
•
Distilled H20
Micronutrients
Low N (0.1 mg/L)
High N (1.0 mg/L)
Low P (0.025 mg/L)
High P (0.25 mg/L)
• N:P(1) Low N + Low P
• N:P(2) Low N + High P
• N:P(3) High N + Low P
Nutrient Source:
Micronutrients: Hoaglands
N: NH4Cl
P: NaH2PO4
Anthropogenic N additions alter
growth and morphology
Anthropogenic N additions alter
growth and morphology
Increasing N
Effects of Anthropogenic
N additions
• Increased production of phyllodia
Phenotypic shift from carnivory to
photosynthesis
• Increased probability of flowering
Contrasting effects of
anthropogenic N vs. N derived
from prey
Food Addition Experiment
•
•
•
•
Ecological “press” experiment
Food supplemented with house flies
Treatments: 0, 2, 4 ,6, 8,10,12, 14 flies/week
Plants harvested after one field season
Food additions do not alter
growth and morphology
Increasing
prey
N uptake increases with food level
P uptake increases with food level
N:P ratio decreases with
increasing food supply
Altered N:P ratios suggest
P limitation under ambient conditions
Ambient
P limitation (Koerselman &
Meuleman 1996, Olde Venternik et
al. in press)
Food additions do not alter
growth and morphology
Increasing
prey
Anthropogenic N additions alter
growth and morphology
Increasing N
Contrasting effects of anthropogenic
and natural sources of N
Anthropogenic N
Altered N:P ratios
Morphological shift
Reduction in prey uptake
Prey N
Uptake, storage of N & P
No morphological shifts
Continued prey uptake
Effects of N Deposition on
Carnivorous Plants
•
•
•
•
•
Life History
Effects on Individuals
Effects on Populations
Effects on Communities
The Role of Ecologists
Study Sites
Demography survey
• 100 adult, juvenile plants tagged at
each site
• Plants censused and measured each
year
• Seed plantings to estimate recruitment
functions
Recruits
Juveniles
Adults
Flowering
Adults
Sarracenia matrix model
4.00
Recruits
0.10
Juveniles
0.04
Adults
0.09
0.95
0.18
0.83
0.70
Flowering
Adults
0.17
Hawley Bog Transitions
4.00
Recruits
0.10
Juveniles
0.13
Adults
0.17
0.85
0.10
0.66
0.71
Molly Bog Transitions
Flowering
Adults
0.31
Matrix Transition Model
(stationary)
nt+1 = Ant
Population vector
at time (t + 1)
Transition matrix
Population
vector at time (t)
Population Projections
Site
r individuals/individual•year
Hawley Bog
0.00456
Doubling
Time
152 y
Molly Bog
0.00554
125 y
Deterministic Model: Results
• Growth, survivorship, and reproduction
are closely balanced in both sites
• Doubling times > 100 y
• Juvenile, adult persistence contribute
most to population growth rate
• Sexual reproduction, recruitment
relatively unimportant
Matrix Transition Model
(stochastic)
nt+1 = Atnt
Population vector
at time (t + 1)
Random transition
matrix at time (t)
Population
vector at time (t)
(m
ild
)
e)
(s
ev
er
(m
e)
)
ild
st
ic
(s
ev
er
E
ES
E
ES
M
M
in
i
r
D
et
er
m
Hawley Bog
0.30
0.20
0.10
0.00
-0.10
-0.20
-0.30
Hawley Bog
1000
Deterministic
ES (severe)
ES (mild)
800
n 600
400
200
0
5
10
15
Time Step
20
25
Stochastic Model: Results
• Cannot reject H0 (r = 0.0)
• Environmental variation can lead to a
substantial risk of long-term extinction
(0.3 < p(ext) < 0.6)
How do N and P
concentrations affect
population growth of
Sarracenia?
Nutrient Addition Experiment
• 10 juveniles, 10 adults/treatment
• Nutrients added to leaves twice/month
• Nutrient concentrations bracket
observed field values
• Nutrient treatments maintained 1998,
1999
• “Press” experiment
Nutrient Treatments
•
•
•
•
•
•
Distilled H20
Micronutrients
Low N (0.1 mg/L)
High N (1.0 mg/L)
Low P (0.025 mg/L)
High P (0.25 mg/L)
• N:P(1) Low N + Low P
• N:P(2) Low N + High P
• N:P(3) High N + Low P
Nutrient Source:
Micronutrients: Hoaglands
N: NH4Cl
P: NaH2PO4
Effects of N additions
• Increased production of phyllodia
• Increased probability of flowering
Effects of N additions
• Increased production of phyllodia
• Increased probability of flowering
• Decreased juvenile survivorship
Population Growth Rate
(Deterministic)
0.05
0.00
L
L
M
r -0.05
H
-0.10
H
-0.15
Distilled
High N
NP (2)
Micros
Low P
NP (1)
Low N
High P
NP (3)
Population Growth Rate
(Measurement Error)
0.10
0.05
0.00
-0.05
-0.10
L
r -0.15
L
M
-0.20
-0.25
-0.30
H
-0.35
H
D
(3
)
N
P
(1
)
N
P
(2
)
N
P
P
H
ig
h
P
Lo
w
N
H
ig
h
N
Lo
w
is
til
le
d
M
ic
ro
s
-0.40
Effects of Nitrogen on
Demography: Results
• Population growth rates respond to
different N and P regimes
• Population growth rate decreases in
response to increasing N
• Population growth rate decreases in
responses to increasing N:P
Modeling Long-term
Environmental Change
Time Series
Modeling
Observed
N Deposition
Long-term
Forecast
N(t)
Transition
Function
Transition
Matrix (t)
Matrix
Multiplication
Population Time Series
Extinction Risk
Time to Extinction
Population
Structure (t)
Modeling Long-term
Environmental Change
Time Series
Modeling
Observed
N Deposition
Long-term
Forecast
N(t)
Transition
Function
Transition
Matrix (t)
Matrix
Multiplication
Population Time Series
Extinction Risk
Time to Extinction
Population
Structure (t)
N monitoring
• National Atmospheric Deposition
Program
• NH4, NO3 measured as mg/l/yr
• Annual data 1984-1998
• Monitoring sites
Shelburne, VT
Quabbin, MA
Shelburne, VT
Quabbin, MA
0.30
0.30
0.25
0.25
0.20
0.20
0.15
0.15
0.10
0.10
0.05
0.05
0.00
0.00
2.0
2.0
1.5
1.5
1.0
1.0
0.5
0.5
0.0
0.0
19
84
19
86
19
88
19
90
19
92
19
94
19
96
19
98
N03
2.5
19
84
19
86
19
88
19
90
19
92
19
94
19
96
19
98
2.5
19
84
19
86
19
88
19
90
19
92
19
94
19
96
19
98
0.35
19
84
19
86
19
88
19
90
19
92
19
94
19
96
19
98
NH4
0.35
Shelburne, VT
Quabbin, MA
0.30
0.30
0.25
0.25
0.20
0.20
0.15
0.15
0.10
0.10
0.05
0.05
0.00
0.00
2.0
2.0
1.5
1.5
1.0
1.0
0.5
0.5
0.0
0.0
19
84
19
86
19
88
19
90
19
92
19
94
19
96
19
98
N03
2.5
19
84
19
86
19
88
19
90
19
92
19
94
19
96
19
98
2.5
19
84
19
86
19
88
19
90
19
92
19
94
19
96
19
98
0.35
19
84
19
86
19
88
19
90
19
92
19
94
19
96
19
98
NH4
0.35
Regression Models
Ordinary Least
Squares (OLS)
Nt = a + bt + e
First-order autoregressive (AR-1)
Nt = a +bNt-1 + e
Shelburne (AR-1)
Quabbin (AR-1)
10
1
b = 0.947
b = 1.000
0.1
b = 1.053
N (mg/l/y)
N (mg/l/yr)
10
0.01
1
b = 0.978
b = 1.000
b = 1.022
0.1
0.01
1
10
19
28
37
46
1
10
19
Year
37
46
Year
Shelburne (OLS)
Quabbin (OLS)
0.7
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
0.6
b = -0.004
b = 0.000
b = 0.004
N (mg/l/y)
N (mg/l/y)
28
b = -0.001
0.5
b = 0.000
0.4
b = 0.001
0.3
0.2
1
10
19
28
Year
37
46
1
10
19
28
Year
37
46
Modeling Long-term
Environmental Change
Time Series
Modeling
Observed
N Deposition
Long-term
Forecast
N(t)
Transition
Function
Transition
Matrix (t)
Matrix
Multiplication
Population Time Series
Extinction Risk
Time to Extinction
Population
Structure (t)
Establishing Transition
Functions
• Linear interpolation between observed
data points (n = 3)
• Asymptotic transitions at extreme levels
of nitrogen:
pij = observed pij if [N] < 0.01 mg/l/yr
pij = 0.0 if [N] > 10.0 mg/l/yr
• Logarithmic response curve
Modeling Demographic Transitions as a
Function of Nitrogen
Adults → Adults
1
Extrapolated
Observed
0.8
0.6
0.4
0.2
0
-3
-2
-1
0
Log10 [N]
1
2
Modeling Long-term
Environmental Change
Time Series
Modeling
Observed
N Deposition
Long-term
Forecast
N(t)
Transition
Function
Transition
Matrix (t)
Matrix
Multiplication
Population Time Series
Extinction Risk
Time to Extinction
Population
Structure (t)
Matrix Transition Model
(changing environment)
nt+1 = Atnt
Population vector
at time (t + 1)
Sequentially
changing transition
matrix at time (t)
Population
vector at time (t)
Estimated population size at
Hawley bog
Stage
Recruits
Number of
individuals
1500
Juveniles
23,500
Non-flowering Adults
1400
Flowering Adults
500
Quabbin Exponential Forecast
Models (AR-1)
Scenario
P (ext) at
100 y
0.00
Time to ext
(p = 0.95)
> 10,000 y
No change 0.0%
0.038
650 y
Small
1%
increase
Worst case 4.7%
0.378
290 y
0.996
70 y
Best case
Annual %
Change
-4.7%
Shelburne Exponential
Forecast Models (AR-1)
Scenario
P (ext) at
100 y
0.158
Time to ext
(p = 0.95)
> 10,000 y
No change 0.0%
0.510
230 y
Small
1.0%
increase
Worst case 2.2%
0.694
200 y
0.838
140 y
Best case
Annual %
Change
-2.2%
Shelburne Nitrogen
Forecast Model
Population Size
30000
25000
20000
AR
15000
OLS
10000
5000
0
1
10
19
28
Year
37
46
Forecasting Models for
Nitrogen Deposition: Results
• Increasing or stationary models of
Nitrogen deposition drive Sarracenia
populations to extinction
• Extinction risk declines with reduced
nitrogen
• Correlated nitrogen series can induce
cycles and complex population
dynamics
Effects of N Deposition on
Carnivorous Plants
•
•
•
•
•
Life History
Effects on Individuals
Effects on Populations
Effects on Communities
The Role of Ecologists
Sarracenia Nutrient
Feedback Loop
Arthropod
Prey
Atmospheric
Deposition
Inquiline
Community
Pitcher
Nutrient
Pool [N,P]
Plant
Growth
Sarracenia Nutrient
Feedback Loop
Arthropod
Prey
Atmospheric
Deposition
Inquiline
Community
Pitcher
Nutrient
Pool [N,P]
Plant
Growth
Sarracenia Nutrient
Feedback Loop
Arthropod
Prey
Atmospheric
Deposition
Inquiline
Community
Pitcher
Nutrient
Pool [N,P]
Plant
Growth
Sarracenia Nutrient
Feedback Loop
Arthropod
Prey
Atmospheric
Deposition
Inquiline
Community
Pitcher
Nutrient
Pool [N,P]
Plant
Growth
Nutrients → Inquilines
• Manipulate [N], [P] in leaves
• Orthogonal “regression” design
• Maintain [] in a “press” experiment
Response Surface
Experimenal Design
[P]
7
6
5
4
3
2
1
0
0
1
2
3
[N]
4
5
6
7
Effects of [N,P]
on Inquiline Abundance
30
20
10
0
6
5
4
2
3
[N]
2
1
1
0
0
6
]
4
3
5
[P
nce
Rotifer Abunda
40
Sarracenia Nutrient
Feedback Loop
Arthropod
Prey
Atmospheric
Deposition
Inquiline
Community
Pitcher
Nutrient
Pool [N,P]
Plant
Growth
Inquilines → Nutrients
• Manipulate [N], [P] in leaves
• Orthogonal “regression” design
• Establish initial [] in a “pulse”
experiment
Response Surface
Experimenal Design
[P]
7
6
5
4
3
2
1
0
0
1
2
3
[N]
4
5
6
7
Null Hypothesis
[P]
7
6
5
4
3
2
1
0
0
1
2
3
[N]
4
5
6
7
Community Regulation
of Nutrients
[P]
7
6
5
4
3
2
1
0
0
1
2
3
[N]
4
5
6
7
Sarracenia Nutrient
Feedback Loop
Arthropod
Prey
Atmospheric
Deposition
Inquiline
Community
Pitcher
Nutrient
Pool [N,P]
Plant
Growth
Nutrients ↔ Inquilines
dN
 f (N , I , t)
dt
dI
 g (I , N , t)
dt
Effects of N Deposition on
Carnivorous Plants
•
•
•
•
•
Life History
Effects on Individuals
Effects on Populations
Effects on Communities
The Role of Ecologists
Teragrams of Nitrogen
200
Total anthropogenic N fixed
150
Natural range
100
50
Fertilizer
0
1900
1920
1940
1960
Year
NOx
1980
2000
Ecology
≠
Environmental Science
Reasons for Studying Ecology
Reasons for Studying Ecology
• Natural History
Reasons for Studying Ecology
• Natural History
• Field Studies & Experiments
Reasons for Studying Ecology
• Natural History
• Field Studies & Experiments
• Statistics & Data Analysis
Population Growth Rate
(Deterministic)
0.05
0.00
r -0.05
-0.10
-0.15
Micros
Low P
NP (1)
Low N
High P
NP (3)
0.35
0.30
0.25
0.20
0.15
0.10
0.05
0.00
19
84
19
86
19
88
19
90
19
92
19
94
19
96
19
98
Distilled
High N
NP (2)
Reasons for Studying Ecology
•
•
•
•
Natural History
Field Studies & Experiments
Statistics & Data Analysis
Modeling
dN
 f (N , I , t)
dt
dI
 g (I , N , t)
dt
Arthropod
Prey
Atmospheric
Deposition
Inquiline
Community
Pitcher
Nutrient
Pool [N,P]
Population Size
30000
25000
20000
AR
15000
OLS
10000
5000
0
1
10
19
28
Year
37
46
Plant
Growth
Reasons for Studying Ecology
•
•
•
•
•
Natural History
Field Studies & Experiments
Statistics & Data Analysis
Modeling
Collaboration
Aaron M. Ellison
Harvard Forest
Conclusions
• Anthropogenic deposition of N is a major ecological
challenge
Conclusions
• Anthropogenic deposition of N is a major ecological
challenge
• Carnivorous plants in ombrotrophic bogs are a model
system
Conclusions
• Anthropogenic deposition of N is a major ecological
challenge
• Carnivorous plants in ombrotrophic bogs are a model
system
• Individual response
 plants alter morphology and growth in response to N:P ratios
Conclusions
• Anthropogenic deposition of N is a major ecological
challenge
• Carnivorous plants in ombrotrophic bogs are a model
system
• Individual response
 plants alter morphology and growth in response to N:P ratios
• Population response
 N and P environments affect population growth rate
Conclusions
• Anthropogenic deposition of N is a major ecological
challenge
• Carnivorous plants in ombrotrophic bogs are a model
system
• Individual response
 plants alter morphology and growth in response to N:P ratios
• Population response
 N and P environments affect population growth rate
• Community response
 Further study of nutrient ↔ inquiline feedback loop