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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.

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Effects of N Deposition Individual Altered morphology Changes in reproduction, survivorship

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Effects of N Deposition Individual Altered morphology Changes in reproduction, survivorship Population Increased long-term extinction risk Changes in short-term dynamics

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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

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Effects of N Deposition on Carnivorous Plants Life History Effects on Individuals Effects on Populations Effects on Communities The Role of Ecologists

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Effects of N Deposition on Carnivorous Plants Life History Effects on Individuals Effects on Populations Effects on Communities The Role of Ecologists

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Carnivorous plants: well- known, but poorly studied

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Carnivory in plants Phylogenetically diverse Morphological, chemical adaptations for attracting, capturing, digesting arthropods Common in low N habitats Poor competitors for light, nutrients

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Family Sarraceniaceae GenusCommon Name Number of Species Distribution DarlingtoniaCobra Lilly1Northwest USA HeliamphoraSun Pitchers5North-central South America SarraceniaPitcher Plants8Eastern USA, Canada

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Genus Sarracenia 8 described species Center of diversity in southeastern US Many subvarieties Extensive hybridization Sarracenia purpurea (New Jersey- Canada)

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The Northern Pitcher Plant Sarracenia purpurea Perennial plant of low-N peatlands Lifespan 30-50 y Arthropod prey capture in water- filled pitchers Diverse inquiline community in pitchers

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The Inquilines Wyeomyia smithii Metriocnemus knabiHabrotrocha rosa Blaesoxipha fletcheri Sarraceniopus gibsoni

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Inquiline food web

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Phyllodia Flat leaves No prey capture High concentration of chlorophyll, stomates Photosynthetically more efficient than pitchers

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Flowering Stalks Single stalk per rosette Flowering after 3 to 5 years Bumblebee, fly pollinated Short-distance dispersal of seeds

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Leaf Senescence End-of-season die off Production of new leaves in following spring Annual increase in rosette diameter

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Effects of N Deposition on Carnivorous Plants Life History Effects on Individuals Effects on Populations Effects on Communities The Role of Ecologists

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Nutrient Treatments Distilled H 2 0 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: NH 4 Cl P: NaH 2 PO 4

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Anthropogenic N additions alter growth and morphology

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Increasing N

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Effects of Anthropogenic N additions Increased production of phyllodia Phenotypic shift from carnivory to photosynthesis Increased probability of flowering

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Contrasting effects of anthropogenic N vs. N derived from prey

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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

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Food additions do not alter growth and morphology Increasing prey

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N uptake increases with food level

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P uptake increases with food level

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N:P ratio decreases with increasing food supply

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Altered N:P ratios suggest P limitation under ambient conditions P limitation (Koerselman & Meuleman 1996, Olde Venternik et al. in press) Ambient

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Food additions do not alter growth and morphology Increasing prey

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Anthropogenic N additions alter growth and morphology Increasing N

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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

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Effects of N Deposition on Carnivorous Plants Life History Effects on Individuals Effects on Populations Effects on Communities The Role of Ecologists

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Study Sites

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Demography survey 100 adult, juvenile plants tagged at each site Plants censused and measured each year Seed plantings to estimate recruitment functions

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Recruits Juveniles Adults Flowering Adults Sarracenia matrix model

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Recruits Juveniles Adults Flowering Adults Hawley Bog Transitions 0.10 4.00 0.04 0.09 0.18 0.83 0.950.70 0.17

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Recruits Juveniles Adults Flowering Adults Molly Bog Transitions 0.10 4.00 0.13 0.17 0.10 0.66 0.850.71 0.31

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Matrix Transition Model (stationary) n t+1 = An t Population vector at time (t + 1) Transition matrix Population vector at time (t)

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Population Projections Siter individuals/individualyear Doubling Time Hawley Bog0.00456152 y Molly Bog0.00554125 y

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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

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Matrix Transition Model (stochastic) n t+1 = A t n t Population vector at time (t + 1) Random transition matrix at time (t) Population vector at time (t)

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Stochastic Model: Results Cannot reject H 0 (r = 0.0) Environmental variation can lead to a substantial risk of long-term extinction (0.3 < p(ext) < 0.6)

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How do N and P concentrations affect population growth of Sarracenia?

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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

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Nutrient Treatments Distilled H 2 0 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: NH 4 Cl P: NaH 2 PO 4

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Effects of N additions Increased production of phyllodia Increased probability of flowering

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Effects of N additions Increased production of phyllodia Increased probability of flowering Decreased juvenile survivorship

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L L M H H

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H M L H L

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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

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Modeling Long-term Environmental Change Observed N Deposition Long-term Forecast N(t) Transition Matrix (t) Population Structure (t) Time Series Modeling Transition Function Population Time Series Extinction Risk Time to Extinction Matrix Multiplication

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Modeling Long-term Environmental Change Observed N Deposition Long-term Forecast N(t) Transition Matrix (t) Population Structure (t) Time Series Modeling Transition Function Population Time Series Extinction Risk Time to Extinction Matrix Multiplication

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N monitoring National Atmospheric Deposition Program NH 4, NO 3 measured as mg/l/yr Annual data 1984-1998 Monitoring sites Shelburne, VT Quabbin, MA

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Quabbin, MA Shelburne, VT NH 4 N0 3

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Quabbin, MA Shelburne, VT NH 4 N0 3

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Regression Models Ordinary Least Squares (OLS) N t = a + bt + e First-order auto- regressive (AR-1) N t = a +bN t-1 + e

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Modeling Long-term Environmental Change Observed N Deposition Long-term Forecast N(t) Transition Matrix (t) Population Structure (t) Time Series Modeling Transition Function Population Time Series Extinction Risk Time to Extinction Matrix Multiplication

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Establishing Transition Functions Linear interpolation between observed data points (n = 3) Asymptotic transitions at extreme levels of nitrogen: p ij = observed p ij if [N] < 0.01 mg/l/yr p ij = 0.0 if [N] > 10.0 mg/l/yr Logarithmic response curve

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Modeling Demographic Transitions as a Function of Nitrogen

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Modeling Long-term Environmental Change Observed N Deposition Long-term Forecast N(t) Transition Matrix (t) Population Structure (t) Time Series Modeling Transition Function Population Time Series Extinction Risk Time to Extinction Matrix Multiplication

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Matrix Transition Model (changing environment) n t+1 = A t n t Population vector at time (t + 1) Sequentially changing transition matrix at time (t) Population vector at time (t)

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Estimated population size at Hawley bog StageNumber of individuals Recruits1500 Juveniles23,500 Non-flowering Adults1400 Flowering Adults500

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Quabbin Exponential Forecast Models (AR-1) ScenarioAnnual % Change P (ext) at 100 y Time to ext (p = 0.95) Best case-4.7%0.00> 10,000 y No change0.0%0.038650 y Small increase 1%0.378290 y Worst case4.7%0.99670 y

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Shelburne Exponential Forecast Models (AR-1) ScenarioAnnual % Change P (ext) at 100 y Time to ext (p = 0.95) Best case-2.2%0.158> 10,000 y No change0.0%0.510230 y Small increase 1.0%0.694200 y Worst case2.2%0.838140 y

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Shelburne Nitrogen Forecast Model

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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

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Effects of N Deposition on Carnivorous Plants Life History Effects on Individuals Effects on Populations Effects on Communities The Role of Ecologists

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Sarracenia Nutrient Feedback Loop Pitcher Nutrient Pool [N,P] Inquiline Community Arthropod Prey Plant Growth Atmospheric Deposition

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Sarracenia Nutrient Feedback Loop Pitcher Nutrient Pool [N,P] Inquiline Community Arthropod Prey Plant Growth Atmospheric Deposition

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Sarracenia Nutrient Feedback Loop Pitcher Nutrient Pool [N,P] Inquiline Community Arthropod Prey Plant Growth Atmospheric Deposition

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Sarracenia Nutrient Feedback Loop Pitcher Nutrient Pool [N,P] Inquiline Community Arthropod Prey Plant Growth Atmospheric Deposition

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Nutrients → Inquilines Manipulate [N], [P] in leaves Orthogonal “regression” design Maintain [] in a “press” experiment

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Response Surface Experimenal Design

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Effects of [N,P] on Inquiline Abundance

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Sarracenia Nutrient Feedback Loop Pitcher Nutrient Pool [N,P] Inquiline Community Arthropod Prey Plant Growth Atmospheric Deposition

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Inquilines → Nutrients Manipulate [N], [P] in leaves Orthogonal “regression” design Establish initial [] in a “pulse” experiment

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Response Surface Experimenal Design

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Null Hypothesis

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Community Regulation of Nutrients

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Sarracenia Nutrient Feedback Loop Pitcher Nutrient Pool [N,P] Inquiline Community Arthropod Prey Plant Growth Atmospheric Deposition

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Nutrients ↔ Inquilines

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Effects of N Deposition on Carnivorous Plants Life History Effects on Individuals Effects on Populations Effects on Communities The Role of Ecologists

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Ecology ≠ Environmental Science

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Reasons for Studying Ecology

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Natural History

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Reasons for Studying Ecology Natural History Field Studies & Experiments

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Reasons for Studying Ecology Natural History Field Studies & Experiments Statistics & Data Analysis

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Reasons for Studying Ecology Natural History Field Studies & Experiments Statistics & Data Analysis Modeling

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Pitcher Nutrient Pool [N,P] Inquiline Community Arthropod Prey Plant Growth Atmospheric Deposition

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Reasons for Studying Ecology Natural History Field Studies & Experiments Statistics & Data Analysis Modeling Collaboration

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Aaron M. Ellison Harvard Forest

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Conclusions Anthropogenic deposition of N is a major ecological challenge

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Conclusions Anthropogenic deposition of N is a major ecological challenge Carnivorous plants in ombrotrophic bogs are a model system

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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

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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

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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

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