1. 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.

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

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

6. 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

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

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

9. Carnivorous plants: well- known, but poorly studied

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

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

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

13. 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

16. The Inquilines Wyeomyia smithii Metriocnemus knabiHabrotrocha rosa Blaesoxipha fletcheri Sarraceniopus gibsoni

17. Inquiline food web

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

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

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

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

22. 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

23. Anthropogenic N additions alter growth and morphology

25. Increasing N

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

27. Contrasting effects of anthropogenic N vs. N derived from prey

28. 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

29. Food additions do not alter growth and morphology Increasing prey

30. N uptake increases with food level

31. P uptake increases with food level

32. N:P ratio decreases with increasing food supply

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

34. Food additions do not alter growth and morphology Increasing prey

35. Anthropogenic N additions alter growth and morphology Increasing N

36. 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

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

40. Study Sites

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

48. Recruits Juveniles Adults Flowering Adults Sarracenia matrix model

49. 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

50. 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

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

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

53. 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

54. 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)

57. 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)

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

60. 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

62. 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

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

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

65. L L M H H

66. H M L H L

67. 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

68. 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

69. 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

70. 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

71. Quabbin, MA Shelburne, VT NH 4 N0 3

72. Quabbin, MA Shelburne, VT NH 4 N0 3

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

75. 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

76. 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

77. Modeling Demographic Transitions as a Function of Nitrogen

78. 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

79. 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)

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

81. 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

82. 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

83. Shelburne Nitrogen Forecast Model

84. 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

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

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

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

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

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

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

91. Response Surface Experimenal Design

92. Effects of [N,P] on Inquiline Abundance

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

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

95. Response Surface Experimenal Design

96. Null Hypothesis

97. Community Regulation of Nutrients

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

100. Nutrients ↔ Inquilines

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

105. Ecology ≠ Environmental Science

106. Reasons for Studying Ecology

107. Natural History

109. Reasons for Studying Ecology Natural History Field Studies & Experiments

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

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

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

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

116. Aaron M. Ellison Harvard Forest

117. Conclusions Anthropogenic deposition of N is a major ecological challenge

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

119. 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

120. 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

121. 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