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The Ecological Impacts Of Nitrogen Deposition: Insights From The Carnivorous Pitcher Plant Sarracenia purpurea Nicholas J. Gotelli Department of Biology University of Vermont Burlington, VT 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 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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Wakefield, A. E., N. J. Gotelli, S. E. Wittman, and A. M. Ellison Prey addition alters nutrient stoichiometry of the carnivorous plant Sarracenia purpurea. Ecology 86:

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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 added food

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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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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 Although Sarracenia has evolved adaptations for low N environments, chronic N deposition may have caused populations to be currently limited by P, not N.

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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

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Recruits Juveniles Adults Flowering Adults Molly Bog Transitions

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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 Bog y Molly Bog 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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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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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 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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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% y Small increase 1% y Worst case4.7% 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% y Small increase 1.0% y Worst case2.2% 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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Four-level Multi-Factorial Experiment Atmospheric N (8 levels) Prey supplement (yes,no) Top predator removal (yes,no)

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Four-level Multi-Factorial Experiment Atmospheric N (8 levels) Prey supplement (yes,no) Top predator removal (yes,no) Nutrient exchange with plant (unmanipulated, isolated, control)

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Quantifying Trophic Structure Food web saturation is our response variable. Each taxon in the food web is given a binary value representing its presence (1xxxx) or absence (0xxxx): TaxonBinary valueDecimal value Metriocnemus11 Habrotrocha102 Sarraceniopus1004 Wyeomyia10008 Fletcherimyia The saturation of the food web in a given pitcher is the sum of the equivalent decimal values of each taxon present. Food webs with higher saturation values have both more trophic levels present and more trophic links present. There are 32 possible food webs that can be assembled with these 5 taxa; the decimal value for each food web ranges from 0 – 31, with increasing numbers indicating more saturated food webs.

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Nutrient exchange with the plant and top predators affect food web structure

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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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