,, . _, o EPA/600/R-05/007
United States Aoril 2007
Environmental Protection aprn^uu/
Agency www.epa.gov
A Summary of NHEERL Ecological Research
on Global Climate Change
Edited by
Peter A. Beedlow
And
David T. Tingey
U.S. Environmental Protection Agency
Office of Research and Development
Washington, DC 20460
-------
Contributing Authors
Author
Christian P. Andersen
Peter A. Beedlow
Michael Cairns
Naomi E. Detenbeck
Robert K. Dixon
William S. Fisher
William Hogsett
Mark G. Johnson
Robert McKane
Leah M. Oliver
David M. Olszyk
Donald Phillips
John E. Rogers
Paul T. Rygiewicz
Debbie L. Santavy
Ray Seidler
Allen M. Solomon
David T. Tingey
Lidia S. Watrud
Address
USEPA National Health and Environmental Effects Research Lab/ORD
Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR 97333-
4902
USEPA National Health and Environmental Effects Research Lab/ORD
Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR 97333-
4902
USEPA National Health and Environmental Effects Research Lab/ORD
Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR 97333-
4902
USEPA Environmental Effects Research Laboratory, Mid-Continent
Ecology, Division/ORD, 6201 Congdon Boulevard, Duluth, MN 55804
(formerly US EPA) Deputy Assistant Secretary, US Department of
Energy, Washington, DC 20585
USEPA Environmental Effects Research Laboratory, Gulf Ecology
Division/ORD, Sabine Island Drive, Gulf Breeze, FL 32561-5299
USEPA National Health and Environmental Effects Research Lab/ORD
Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR 97333-
4902
USEPA National Health and Environmental Effects Research Lab/ORD
Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR 97333-
4902
USEPA National Health and Environmental Effects Research Lab/ORD
Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR 97333-
4902
USEPA Environmental Effects Research Laboratory, Gulf Ecology
Division/ORD, Sabine Island Drive, Gulf Breeze, FL 32561-5299
USEPA National Health and Environmental Effects Research Lab/ORD
Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR 97333-
4902
USEPA National Health and Environmental Effects Research Lab/ORD
Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR 97333-
4902
USEPA Environmental Effects Research Laboratory, Gulf Ecology
Division/ORD, Sabine Island Drive, Gulf Breeze, FL 32561-5299
USEPA National Health and Environmental Effects Research Lab/ORD
Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR 97333-
4902
USEPA Environmental Effects Research Laboratory, Gulf Ecology
Division/ORD, Sabine Island Drive, Gulf Breeze, FL 32561-5299
(ret.) USEPA National Health and Environmental Effects Research
Lab/ORD Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR
97333-4902
USEPA National Health and Environmental Effects Research Lab/ORD
Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR 97333-
4902
USEPA National Health and Environmental Effects Research Lab/ORD
Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR 97333-
4902
USEPA National Health and Environmental Effects Research Lab/ORD
Western Ecology Division, 200 S.W. 35th Street, Corvallis, OR 97333-
4902
Chapters
9
1,2
13
6,9
3
6
12
9
5,9
10
8
12
4,9
2,5
9, 11
12
8
12
9
1,6
1,9,
7
10, 13
9
-------
Acknowledgements
We would like to thank the contributing authors for their timely writings and
especially for their patience as this document was assembled. A special thanks
to Karen Gundersen and Nancy Terhaar for locating and organizing the
publications produced from this research. Over the years many scientists—EPA
as well as those on cooperative agreements and contracts—have made critical
contributions to the NHEERL climate change research. We would like to
recognize the following individuals for their long-term participation and
contribution to this program: Sandra Brown (Winrock International), Bruce
McVeety (Battelle), Jack Winjum (NCASI), Paul Schroeder, Ron Neilson (Oregon
State University), Ted Vinson (Oregon State University), Tanya Kolchugina
(Oregon State University/Moscow State University), David Turner (Oregon State
University), Dominique Bachelet (Oregon State University), Richard Meganck
(OAS), Sandra Henderson, George King (Dynamac), Mark Trexler (Trexler and
Associates), Richard Houghton (The Woods Hole Research Center), Ed
Rastetter (MBL), Wendall Cropper and Henry Gholz (University of Florida),
David Lewis (Oklahoma State University), Dennis Lettenmaier (University of
Washington), Herman Gucinski (USDA), Danny Marks (USDA), Thomas
Loveland (USGS), Ken Andrasko (EPA), Steven Winnett (EPA), Dennis Tirpak
(EPA/UN FCCC Secretariat), Connie Burdick (EPA), and Jeffrey Lee (EPA).
The information in this document has been funded wholly (or in part) by the U.S.
Environmental Protection Agency. It has been subjected to review by the
National Health and Environmental Effects Research Laboratory's Western
Ecology Division and approved for publication. Approval does not signify that the
contents reflect the views of the Agency, nor does mention of trade names or
commercial products constitute endorsement or recommendation for use.
Peter A. Beedlow
David T. Tingey
June 2004
-------
IV
Table of Contents
List of Contributing Authors ii
Acknowledgements iii
1. Introduction 1-1
2. Water Resources 2-1
3. Freshwater Fish 3-1
4. Responses of the Irrigated Rice Ecosystem to Enhanced
UV-B Radiation and Global Climate Change 4-1
5. Agriculture - Crop yields, soil erosion, and soil carbon 5-1
6. The Global Carbon Cycle: Managing Forest Systems 6-1
7. Vegetation redistribution 7-1
8. Effects of Elevated Atmospheric Carbon Dioxide Concentration and
Temperature on Forests 8-1
9. Interactive Effects of Os and CC>2 on the Ponderosa Pine
Plant/Litter/Soil System 9-1
10. Effects of Elevated CC>2 and Nitrogen Fertilization on Fine Root Growth
in seedling Pinusponderosa. 10-1
11. Free-Air CC>2 Enrichment (FACE) Experiment 11-1
12. Effects of Global Change on Coral Health 12-1
13. Synthesis 13-1
-------
1. Introduction 1-1
1. Introduction
The climate change problem is one of truly global proportions with tremendous
implications to ecological, economic and health conditions of the Earth and its
human population. "The causes and consequences of the problem are ...
intertwined at all spatial and temporal scales, providing a single issue of
unrivaled complexity" (Reichle etal. 1985). As a result, it is critical that the scientific
basis for mitigation and adaptation policies intended to reduce the risks and take
advantage of the opportunities presented by climate change be as clear, reliable,
and up-to-date as possible, without being policy-prescriptive.
The Global Change Research Act of 1990 mandates that the US Global Change
Research Program (USGCRP) assess the potential consequences of global
change for the United States. The Environmental Protection Agency's (EPA)
Global Change Research Program within the Office of Research and
Development (ORD) is conducting research and assessment activities that
contribute to the USGCRP assessment process.
Scientists at the NHEERL, and its predecessor—the Office of Environmental
Processes and Effects Research—initiated research in 1988 anticipating the
Global Change Research Act. The purpose of this document is to summarize
ecological research conducted by NHEERL scientists under the EPA's
contribution to the USGCRP from the onset of research through approximately
2002. The intent is to provide that information as reference material for scientists
investigating the potential impacts of climate change on ecosystems.
The research was conducted through grants and cooperative agreements, and
through intramural research, which is research conducted directly by EPA
scientists. This document focuses on the intramural research in an effort to
highlight the expertise and contributions of EPA scientists. The research
summarized is, primarily, the result of activities performed at the NHEERL
ecology divisions directly involving federal scientists. The objective, here, is to
show the diversity of research conducted, and to highlight the research results in
support of EPA's mission to protect the human health and the environment.
The early research addressed health and ecological effects of exposure to
ultraviolet radiation resulting from stratospheric ozone depletion as well as the
effects of global climate change on forests, agriculture, and water resources. This
research supported both the Montreal Protocol and its amendments (UNEP
2000)—an international agreement curbing the release of ozone depleting
substances—and the 1989 EPA report to the US Congress on the consequences
of global climate change.
From 1990 through 1996, a significant portion of the ORD effort focused on
stabilizing the buildup of atmospheric carbon dioxide and other greenhouse
gases. The ecological research emphasized terrestrial ecosystem-atmosphere
-------
1. Introduction 1-2
carbon cycling, and strategies for enhancing biospheric carbon sequestration.
In 1997 as part of a USGCRP effort to better coordinate activities across federal
agencies and to focus each agency's work on those topics most consistent with
its mission, ORD redirected its Global Change Research Program to assessing
the consequences of global change.
In 1998, EPA's Global Program began conducting regional assessments in
support of the USGCRP assessment process. Also, EPA's Global Program
shifted resources away from carbon cycle and greenhouse gas mitigation
research to assessing the potential consequences of global change. While some
research on cause and effect mechanisms continued, ORD's primary
responsibility was leading regional assessments on the consequences of global
change on air quality, water quality, human health, and ecosystem health within
the United States.
NHEERL's research role has changed in concert with EPA's changing research
needs regarding global change. Ecological effects research other than that on
coral ecosystems ended in 2002. During period between 1988 and 2002,
NHEERL scientists conducted numerous projects on the following topics:
• The effects on agriculture, specifically rice—the World's most important
grain.
• The effects on the global biomes—forest migration and desertification.
• The effects on aquatic ecosystems—the thermal response of freshwater
fish.
• The effects on terrestrial ecosystems—forest response to increased
temperature and carbon dioxide, and the interaction of tropospheric
ozone.
Currently, NHEERL research is addressing coral ecosystem decline. Coral
dominated ecosystems are among the most threatened by global climate
change. Research is examining the impacts of global change stressors including
UV irradiation, temperature and nutrient loading on coral ecosystems.
The following chapters summarize the published ecological research conducted
by NHEERL scientists. The summaries give an overview of the research and
provide an entree to the technical literature. A chapter is devoted to describing
the ongoing coral ecosystem research. The final chapter attempts to synthesize
the research findings with a perspective on remaining scientific uncertainties.
Reference Cited
Reichle, D. E., J. R. Trabalka and A. M. Solomon. 1985. Approaches to studying the global
carbon cycle. Pp. 15-24 IN Trabalka, J. R., ed., Atmospheric Carbon Dioxide and the Global
Carbon Cycle. DOE/ER-0239, U.S. Dept. Energy, Washington D.C. 20545
-------
2. Water Resources 2-1
2. Water Resources
Statement of the Problem
Climate change is likely to have significant impacts on the availability of fresh water.
Already in short supply throughout many parts of the world, water for human
consumption, agriculture, and industry will be a major factor in economic growth,
ecological sustainability, and global conflict. Research was undertaken to make initial
assessments of potential impacts of climate change on stream flow and water balance
in the western United States—a region characterized by the shortage of water.
Additionally, research was conducted to address the need for models which account for
the spatial magnitude and extent of hydrologic processes. The models need to handle
key parameters such as precipitation, soil moisture, and evaporation, in response to
changing climatic conditions. The models must account for vegetation interactions with
soil moisture. This is particularly important for simulating regional vegetation response
to climate change since vegetation distribution is controlled in large part by the
availability of soil moisture.
Approach
Research focused on developing and refining detailed watershed scale hydrology
models to address stream dynamics and water storage. Regional-scale modeling
research was directed toward developing physically and mechanically-based water
balance models which can be spatially distributed at watershed, regional, and
continental scales. The research effort contributed to developing methods for spatially
distributing climatic data at scales appropriate for the models, and providing these data
bases to the climate change research community. This ORD project has been
completed; extensions of this research are continuing within the US Geological Survey.
Main Conclusions
The increasing demand for water by population and industrial growth is creating chronic
water shortages throughout the world (Revenga 2000). Add to this the potential impacts of
global climate change on water supplies and chronic shortages could reach crisis levels.
Throughout much of the western United States the supply of water for human
consumption, agriculture, and industry depends on snowpack and reservoir storage.
Most global climate warming scenarios suggest warmer winters with more rainfall and
less snowfall for much of the western United States, which would substantially reduce
snow accumulation and shift the high flow season for many rivers from the spring to the
winter (Lettenmaier et. al. 1992). A substantial amount of the natural storage of winter
precipitation that presently occurs in the snowpack would be lost resulting in increased
spills in the winter and lower reservoir levels in the summer and fall (Lettenmaier and Sheer
1991).
A significant increase in flood hazard in the western US could result from climate
change, primarily due to an increase in rain-on-snow events (Lettenmaier and Can 1990).
Such events occur when warm, wet storms move over existing snowpack. Rapid
melting of the snowpack is the result of a combination of warm air temperature, high
wind and high humidity which cause significant condensation on the snow and is
-------
2. Water Resources 2-2
particularly severe in forest openings and forest clear-cuts (Marks et al. 1998). This
research suggests that some mitigation of the adverse effects of global climate change
may be achieved by adapting land and water management practices to changes in
runoff patterns and maximizing the protective effects of natural vegetation.
Global climate changes are expected to be regional in nature, and affect land cover and
land use. Key to understanding such regional effects on water supplies is the response
of vegetation. Plant communities play a significant role in regional energy and water
balance. While hydrologic models designed to simulate large river systems are good for
operating reservoirs systems, they are not adequate for predicting changes to regional
water balance and, hence, changes in regional vegetation (Marks etal.1993). Dolph et al.
(1991) developed a spatially distributed regional water balance model to evaluate the
sensitivity of large river basins to climate change. The model was exercised for the
Columbia River Basin. This research demonstrated that the existing Historic Climate
Network of climate monitoring stations underestimate precipitation primarily because
mountainous areas are underrepresented. With climate warming, the model predicted
increased evaporative loss, decreased runoff and soil moisture. These conditions could
have profound effects on vegetation distribution and subsequently regional water
resources.
The ability to predict changes in regional vegetation is necessary to evaluate the effects
of climate change on forest resources, agriculture, and water supplies. Changes in soil
moisture and evapotranspiration resulting from climate will have large impacts on water
and vegetation. If changes in the regional water balance are significant, major shifts in
vegetation patterns and condition are a likely (Marks et al. 1993). Neilson and Marks (1994)
incorporated a distributed water balance model with a vegetation model to produce a
biogeographic model, MAPSS (Mapped Atmosphere-Plant-Soil System). This model
was used to predict changes in vegetation leaf area index, site water balance and runoff
as well as changes in biome boundaries. When applied to potential climate change
scenarios, two areas exhibiting among the greatest sensitivity to drought-induced forest
decline were determined to be eastern North America and Eastern Europe to western
Russia.
-------
2. Water Resources
2-3
Effects of Global Climate Change (GCC) on streamflow
With climate warming, mountain snow accumulation would be substantially reduced, and
river's high flow season would shift from the spring to the winter (Lettenmaier et al. 1992).
Actual evaporation would peak in late spring and early summer due to reduced summer soil
moisture. The result would be increased spills in the winter, lower reservoir levels in the
summer and fall, and increased risk of flooding (Lettenmaier and Sheer 1991).
Hydrologic sensitivities across a large part of the western US are driven primarily by runoff
shifts due to temperature change, not changes in total precipitation (Lettenmaier and Can
1990). The exception to the temperature dominance would be in river system with large
reservoir storage relative to the mean annual flow. In these cases shifts in the seasonality
of runoff would be less important than the changes in the mean annual flow, which would
be sensitive to precipitation as well as temperature changes. In populated areas of the
western US such as California, changes in water demand will almost certainly overshadow
the possible effects of GCC over the next century.
Projected Streamflow Effects from Climate Change in the Pacific Northwest
6
predicted flow in 2050's
- - - - present flow
0
Oct Nov Dec
Feb Mar Apr May Jim Jul Aug Sep
Relative to present flows (dashed), the wetter winters and drier summers simulated by climate models are very
likely to shift peak streamflow earlier in the year, increasing the risk of late-summer shortages. Source: Hamlet,
A.F. and D.P. Lettenmaier. 1999. (As shown in the National Assessment Synthesis Team report 2001).
-------
2. Water Resources
2-4
Rain-on-snow
Willamette River, Oregon 1996 flood
Marks et al. (1998) used an energy
balance snowmelt model to simulate
snowmelt processes during a warm,
very wet Pacific storm that caused
significant flooding in the Pacific
Northwest during the Winter of 1996.
Data from paired open and forested
sites located just below the Pacific
Crest were used to drive the model.
The model accurately simulated snow
cover mass and depth during the
development and ablation of the snow
cover prior to, during, and following
one of the most extreme rain-on-snow
events on record. The model
demonstrated that the melt was
caused by condensation on the snow
surface during the event, and by the
fact that a cold storm had deposited
significant snow cover down to
relatively low elevations within the
snow transition zone. In the snow
transition zone of the Cascade
Mountains, clear-cutting is a common
forest practice. This study showed
that during this event, snowmelt was
enhanced in forest openings and
clear-cuts. If GCC results in a shift to
warmer winters such rain-on-snow
events could become more frequent.
Hogo, Pass (HOP)-1450m
LiIIIs Meadows tLMDj-1220
Sanliam Jd. (SAJ) - 1145m
Oa!> Lake IDALI- 1100 T
Jump Off Joe (JOJ)- 1070m
Marion Forts (MRF)-800m
High Sile-1142m
Mid Site-929m
High Site -349 mm J
Mid Site-41 Omm
South Santiam River above Foster Lake
(236 m)
Jam Jane Jams Jan22 Jan29 FebS Feb12 Feb19 Feb26
1996
-------
2. Water Resources
2-5
Effects on regional water balance
A spatially distributed regional water balance model was used to look at the sensitivity of the Columbia Basin to climate change
(Dolph et al. 1991). A wet year (1972) and a dry year (1977) were simulated and compared to recorded data. The modeled total
runoff was significantly less than measured runoff—implying that precipitation data from the Historic Climate Network was
underestimated by the existing network of measurement stations in mountainous regions. In response to this need, several new
methods for estimating precipitation at regional scales were developed (Phillips et al. 1992, Daly et al. 1994). Spatial data bases of
precipitation, temperature, vapor pressure, evapotranspiration, and wind were created for both current conditions and 2xC02C02
scenarios for several GCMs and were made publicly available for the global climate change research community (NOAA / EPA
1992,1997).
The table below presents annual water balance results for a very wet (1972) and a very dry (1977) water year, and for
2xC02 climate conditions predicted by the GFDL general circulation model for the US portion of the Columbia River Basin.
All values are in mm H20 per unit area, so they represent an average depth of water over the basin. Measured annual
runoff at the basin outflow has been corrected to reflect only discharge from the US portion. Annual values refer to water
years (Oct. to following Sep.). NA: data not available or not applicable. Standard deviation (SD; in parentheses) is used to
indicate the extent of deviation from the basin average reported in the table; no SD is given for measured runoff from1972
and 1977 because it is derived from single values measured at the basin outflow; SD is given for the long-term average
measured runoff because it is based on 40 annual values (Marks et al. 1993).
Year Measured
Wet year
1972
annual
precip.
776
(547)
Dry year 507
1977
Long-term
average
(377)
NA
Measured
annual
runoff
1447a
332 a
741 b
(490)
Modeled
annual
runoff
437
(475)
259
(295)
NA
Annual
PET
878
(315)
898
(325)
NA
Modeled
annual
ET
311
(151)
254
(150)
NA
So;7
initial
storage
65
(61)
65
(57)
NA
So;7 final
storage
93
(60)
59
(63)
NA
636C
(543)
NA
276
(319)
1627
(470)
396
(215)
63
(57)
27
(37)
GFDL
2xCO2
scenario
aAnnual runoff over the US portion of the Columbia River Basin (Canadian portion of the flow subtracted out) from gage
measurements at the basin outflow, adjusted for storage effects.
b40-year average unit runoff for the US portion of the Columbia River Basin (Canadian portion of the flow subtracted out)
using historical runoff data.
cAverage precipitation for the US portion of the Columbia River Basin calculated from the 1972 and 1977 precipitation
data.
The water balance approach incorporating a physically based model of potential evapotranspiration and explicit calculation of soil
water holding capacity, improved our ability to simulate soil moisture under current and future climate conditions. A 2xC02 scenario
generated by the GFDL global circulation model provided climate conditions to run the Dolph et al. (1991) water balance model.
The model predicted increased PET, and ET, and decreased runoff and soil moisture. Marks et al. (1993) predicted that changes in
soil moisture and evapotranspiration resulting from global climate change will have large impacts on water and vegetation
resources.
If changes in the regional water balance are significant, major shifts in vegetation patterns and condition are a likely result of global
climate change. Neilson and Marks (1994) incorporated a distributed water balance model with a biogeographic vegetation model,
MAPSS (Mapped Atmosphere-Plant-Soil System) to predict changes in vegetation leaf area index, site water balance and runoff as
well as changes in biome boundaries. 2xC02 scenarios from five different global circulation models (GCMs) were used to predict
vegetation changes globally. Increased PET due to higher temperatures generally offsets increased precipitation under all 2xC02
scenarios. Eastern NA and Eastern Europe to western Russia were among the most sensitive regions to drought-induced forest
decline.
-------
2. Water Resources 2-6
References Cited
Daly, C., R.P. Neilson, and D.L. Phillips. 1994. A statistical-topographic model for mapping climatological
precipitation over mountainous terrain. J. Appl. Meteorol. 33: 140-158.
Dolph, J., D. Marks, and G. A. King. 1991. Sensitivity of the regional water balance in the Columbia
River basin to climate variability: Application of a spatially distributed water balance model. In New
perspectives for watershed management: Balancing Long-Term Sustainability with Cumulative
Environmental Change, (R. J. Naiman and J.R. Sedell, eds.), pp 233-265.
Hamlet, A. F., and D. P. Lettenmaier. 1999. Effects of climate change on hydrology and water
resources objectives in the Columbia River basin, Journal of the American Water Resources
Association, 35(6),pp.1597-1625.
Lettenmaier, D. P., K. L. Brettmann, L. W. Vail, S. B. Yabusaki, and M. J. Scott. 1992. Sensitivity of
Pacific Northwest water resources to global warming. The Northwest Environmental Journal 8:265-283.
Lettenmaier, D. P. and D. P. Sheer. 1991. Climatic sensitivity of California water resources. J. Water
Resources Planning and Management 117.1: 108-125.
Lettenmaier, D. P. and T. Y. Can. 1990. Hydrologic sensitivities of the Sacramento-San Joaquin river
basin, California, to global warming. Water Resources Research 26:69-86.
Marks, D., J. Kimball, D. Tingey, and T. Link. 1998. The sensitivity of snowmelt processes to climate
conditions and forest cover during rain-on-snow: a case study of the 1996 Pacific Northwest flood.
Hydrol. Process. 12:1569-1587.
Marks, D., G. A. King, and J. Dolph. 1993. Implications of climate change for the water balance of the
Columbia River Basin, USA. Clim. Res. 2:203-213.
Neilson, R. P. and D. Marks. 1994. A global perspective of regional vegetation and hydrologic
sensitivities from climatic change. J. of Vegetation Science 5:715-730.
National Assessment Synthesis Team. 2001. Climate Change Impacts on the United States: The
Potential Consequences of Climate Variability and Change, Report for the US Global Change Research
Program, Cambridge University Press, Cambridge UK,620pp.
NOAA / EPA. 1992. Global Ecosystems Database, Disc A. National Oceanic & Atmospheric
Administration / National Geophysical Data Center- Boulder, CO, and U.S. Environmental Protection
Agency / Environmental Research Laboratory - Corvallis, OR.
NOAA / EPA. 1997. Global Ecosystems Database, Disc B. National Oceanic & Atmospheric
Administration / National Geophysical Data Center- Boulder, CO, and U.S. Environmental Protection
Agency / Environmental Research Laboratory - Corvallis, OR.
Phillips, D.L., J. Dolph, and D. Marks. 1992. A comparison of geostatistical procedures for spatial analysis
of precipitation in mountainous terrain. Agric. & Forest Meterol. 58: 119-141.
Revenga, C., J. Brunner, N. Henninger, K. Kassem, and R. Payne. 2000. Pilot analysis of global
ecosystems: Freshwater systems. World Resources Institute
Washington, DC (This report is also available at http://www.wri.orq/wr2000').
-------
3. Freshwater Fish 3-1
3. Responses of Freshwater Fish to Temperature Increases
Statement of the Problem
Water temperature has long been recognized as one of the most important
environmental variables influencing the distribution offish species. Scientists at the Mid-
Continent Ecology Division, Duluth, MN have actively investigated the thermal
requirements of freshwater organisms especially fish since the 1960's and 1970's,
when a water quality research focused on requirements of aquatic organisms, with a
special focus on dissolved oxygen and temperature.
Approach
Laboratory studies were conducted on various fish species to establish temperature
requirements for survival, growth and successful reproduction, data needed for
development of temperature standards to protect fish against thermal pollution. Since
not all fish species are adaptable to laboratory testing, laboratory tests are expensive,
and conditions in the environment can alter sensitivity to thermal regimes, we have
developed a database (FTDMS = Fish Temperature Database Matching System) linking
fish presence records with thermal records in streams and rivers (Eaton etal. I995b).
Various alternative methods for estimating an upper extreme habitat temperature
(UEHT) from fish field distribution data and matched weekly mean stream temperatures
were compared and their respective advantages and disadvantages examined (Eaton et
a/i995a). As reported in Eaton etal. (I995b), an upper extreme habitat temperature,
referred to as a maximum tolerance temperature, was derived for species with adequate
data and a standard error calculated by the bootstrap method. Data above the UEHT
can be approximated by a three-parameter lognormal distribution; standard error of the
estimated UEHT varies among species from 0.1 ° C and 0.6 ° C at the 95% cumulative
probability of occurrence. For 30 common fishes of the U.S., maximum weekly mean
temperatures derived from the database are less than lethal temperatures derived from
laboratory tests, and are similar to temperature criteria derived from laboratory data
interpolated using EPA procedures (Eaton etal. I995b).
Main Conclusions
Effects on fish communities in streams and rivers
In free-flowing streams, the effect of air temperatures and thus global warming on
stream temperatures can be approximated by an adjustment factor of 0.9 times air
temperature, based on field studies of air-water temperature relationship (Stefan and
Preud'homme 1993; Eaton and Scheller 1996). The effects of a doubling of C02 on shifts in
suitable fish habitat has been estimated based on predictions of air temperature effects
from the Canadian Climate Center general circulation model (CCC-GCM) and thermal
tolerances for 57 fish species derived from the FTDMS through extreme-value analysis
(Eaton et al, I995b). Loss of cold water or cool water fish species was predicted for
-------
3. Freshwater Fish 3-2
between 35 and 70% of 1700 USGS temperature monitoring stations, with habitat
losses distributed throughout species ranges. Habitat losses were greatest for species
with limited distributions and in areas of the country with greatest warming predicted
(e.g., the central Midwest). Results for warm water fishes were less certain because of a
relative paucity of data on summer and winter thermal tolerances for species.
Effects of global warming on habitable stream reaches based on temperature effects
can be modified either positively or negatively near groundwater or tailwater discharges
from reservoirs or lakes (Sinokrot etal. 1995). Empirical models to predict groundwater
inputs to stream reaches based on watershed slope and hydraulic conductivity (based
on soil texture; Baker et al. 2001), and models in progress to predict modifications to
stream thermal regimes based on stream shading from topography or riparian
vegetation and groundwater inputs, will help to fine-tune model predictions of the effects
of global change on fish species distributions (V. Snarski, personal communication).
Effects of global climate change on warm water fish species in streams are uncertain
due to a relative paucity of data on winter thermal tolerances. Multivariate discriminate
function analysis has been used to derive models for warm water fish
presence/absence based on a combination of up to six thermal variables: cumulative
temperature as degree-weeks, degree weeks during the feeding period ( weeks > 8 deg
C), degree-weeks during the non-feeding period (weeks < 8 deg C), length of non-
feeding period in weeks, the ratio of degree-weeks during non-feeding periods to
feeding periods, and the number of weeks at or below 2 deg C (a level associated with
mortality due to osmoregulatory dysfunction or other physiological mechanisms).
For the 15 species examined, fish presence models had high specificity (60 -100%,
percent absence correctly predicted) and high sensitivity (87 -100%, percent presence
correctly predicted).
Recently, the Fish-Temperature-Database-Matching System (FTDMS; Eaton etal. I995b)
has been updated with additional data on fish presence from EMAP and STORET and
matched with corresponding stream temperatures from USGS-monitored streams to
create additional fish/temperature (F/T) sets. A user-friendly graphical interface was
developed to facilitate data import, export and query functions to make F/T data
available to clients requesting access (e.g., states and tribes, regions) without requiring
extensive programming expertise (Contract #68-W7-0055, Task Order #25, Deliverable 25-15, by
Lockheed Martin Services, Inc., for U.S. EPA, Office of Information, National Resources Services
Division, Research Triangle Park, NC 27711, March 29, 2000).
Effects on fish communities in lakes
Our ability to predict climate change effects on fish communities in lakes depends on
our ability to model the effect of climate-related variables on suitable fish habitat.
Modeling exercises have been conducted to predict fish presence/absence in
Minnesota lakes as a function of two key driving habitat variables - temperature and
dissolved oxygen (Stefan etal. 1995,1996). Model performance varies with lake class, as
-------
3. Freshwater Fish 3-3
defined by lake morphometry (maximum depth, surface area) and trophic status. For
northern Minnesota, there is full agreement between fish assemblage presence records
and model habitat suitability prediction. For cool and warm water fishes in southern
Minnesota, there is full agreement between fish assemblage presence records and
model simulation results for all 27 lake classes. For cold water fish, model predictions
agreed with fish assemblage presence data for only 18 of 27 lake classes.
Disagreements between observations and predictions are related to the presence of a
cold water fish (cisco) in lakes predicted to have unsuitable habitat for coldwater
assemblages; however, cisco is the most tolerant species in the coldwater fish
assemblage (Stefan etal. 1995).
Predicted sensitivity of suitable fish habitat to climate change based on thermal and
dissolved oxygen requirements varies with fish thermal guild (cold water, cool water,
warm water), lake morphometry (surface area: maximum depth ratio), and trophic status
(Secchi depth) (Stefan etal. 1996). Lake morphometry determines the probability of
thermal stratification and trophic status determines the depth of penetration of solar
radiation and depth of photic zone and dissolved oxygen generation from
photosynthesis. Degree of temperature change in lakes following a doubling of C02
levels and average air temperature increase of 3.8deg C depends on both lake
morphometry and lake trophic status. Eutrophic lakes with a geometry ratio ([surface
area]0 25/maxim urn depth) between 2 and 4 and oligotrophic lakes with a geometry ratio
of between 1 and 2 are predicted to show the least change in hypolimnetic temperature
(0 to 1 deg C as compared to 1-3 deg C). Eutrophic lakes with geometry ratios > 4 and
oligotrophic lakes with geometry ratios >2 are expected to experience decreases in
hypolimnetic oxygen minima of up to 3 mg/L, with anoxic conditions resulting in
eutrophic lakes with geometry ratios of 4 to 20. The length of hypolimnetic anoxia will
extend up to 60 days, and will be greatest in eutrophic lakes with geometry ratios < 5
and oligotrophic lakes with geometry ratios of < 2 (Stefan etal. 1996). Overall, cold water
fish are projected to disappear from southern Minnesota lakes, and experience habitat
losses of 41% in northern Minnesota lakes. Losses in cold water fish good-growth
potential (as reflected in suitable habitat volume) and increases in cool water fish good-
growth potential will be greater in well-mixed lakes. Largest gains in suitable habitat for
cool and warm water species will occur in oligotrophic lakes (Stefan etal. 1996).
Status of research
Research on the temperature preferences offish and predicted effects of climate
change on fish populations is no longer being pursued as a separate program under
Global Climate Change in NHEERL. However, under the Aquatic Stressors Framework,
researchers continue to examine the effects of thermal and flow regimes on fish
communities as two of many stressors affecting habitat quality. In particular, the effect
of land-use/land-cover changes on thermal regimes is being examined.
-------
3. Freshwater Fish 3-4
References Cited
Baker, M.E., M. J. Wiley, and P.W. Seelbach. 2001. CIS-based hydrologic modeling of riparian areas:
implications for stream water quality. JAWRA 37 :1615-1628.
Eaton, J.G., J.H. McCormick, H.G. Stefan, and M. Hondzo. 1995a. Extreme value analysis of a
fish/temperature field database. Ecological Engineering 4:289-305.
Eaton, J.G., J.H. McCormick, B.E. Goodno, D.G. O'Brien, H.G. Stefany, M. Hondzo, and R.M. Scheller.
1995b. A field information-based system for estimating fish temperature tolerances. Fisheries 20(4):10-
18.
Eaton, J.G. and R.M. Scheller. 1996. Effects of climate warming on fish thermal habitat in streams of the
United States. Limnol. Oceanogr. 41:1109-1115.
Sinokrot, B.A., H.G. Stefan, J.H. McCormick, and J.G. Eaton. 1995. Modeling of climate change effects
on stream temperatures and fish habitats below dams and near groundwater inputs. Climatic Change
30:181-200.
Stefan, H.G., M. Hondzo, J.G. Eaton, and J.H. McCormick. 1995. Validation of a fish habitat model for
lakes. Ecological Modelling 82:211-224.
Stefan, H.G., M. Hondzo, X. Fang, J.G. Eaton, and J.H. McCormick. 1996. Simulated long-term
temperature and dissolved oxygen characteristics of lakes in the north-central United States and
associated fish habitat limits. Limnol. Oceanogr. 41:1124-1135.
Stefan, H. G., and E. B. Preud'homme. 1993. Stream temperature estimation from air temperature. Water
Resour. Bull. 29:27-45.
-------
4. Rice 4-1
4. Responses of the Irrigated Rice Ecosystem to Enhanced UV-B
Radiation and Global Climate Change
Statement of the Problem
When this study was conceived there was a critical need for information on the
ecological effects of UV-B radiation (from stratospheric Os depletion) and global climate
change (increased atmospheric C02 concentration and air temperature) in tropical
areas to support major international assessments on the environmental effects of ozone
depletion (by the United Nations Environmental Programme), and climate change (by
Intergovernmental Panel on Climate Change). Rice is a major food source for many of
the world's people, especially in Asia, but also in Africa and South America (IRRI 1993).
The irrigated rice agroecosytem, where fields are flooded for much of the growing
season, is the most widely distributed rice system, with 55% of world's rice field area
and 75% of the world's rice production (IRRI 1993). Thus any impacts on rice production
from UV-B and climate change could have profound impacts on a key component of the
world's food supply. In addition to enhancing rice production, flooding of irrigated rice
fields results in anaerobic soil conditions conducive to the production of the greenhouse
gas methane (Neue 1993). Therefore, understanding the underlying processes and
management factors controlling the emission of methane from rice fields was important
in terms of developing strategies for the potential mitigation of emissions of greenhouse
gases to the atmosphere (Cole 1996).
Approach
To have the most impact and relevance to real field conditions, research on irrigated
rice was conducted in tropical countries, in cooperation with local scientists. Thus, the
rice research was conducted through a unique international partnership between the
U.S. EPA and the International Rice Research Institute (IRRI) in Los Banos, the
Philippines; with collaboration by other institutions and researchers in the United States,
the Netherlands, Germany, Japan, China, Korea, India, Malaysia, and Sri Lanka (oiszyk
and Ingram 1991). The research approach included field experiments, modeling activities
and assessments which presented possible impacts of UV-B and climate change on a
regional scale for eastern and southeastern Asia. The research was designed to
consider responses of irrigated rice production from an ecosystem viewpoint,
considering not only the direct effects of UV-B, C02 and temperature on the rice plant,
but also indirect effects of these stressors on the insects, diseases of rice, and weed
competition. The roles of C02 and temperature in methane production were also
studied. The EPA/IRRI study was coordinated with other international global change
research through the International Geosphere-Biosphere Programme (IGBP) of
research on Global Change and Terrestrial Ecosystems (GCTE), Focus 3, Global
Change Impact on Agriculture, Forestry and Soils.
-------
4. Rice 4-2
Main Conclusions
This research provided critical data for international assessments on the impacts of UV-
B radiation and climate change on rice and on options to mitigate those impacts not only
on the rice crop, but on emissions of the greenhouse gas CH4 from rice fields (Peng etal.
1995). The data were included in the extensive literature produced by the project
including 3 books, 20 book chapters and over 75 peer-reviewed journal papers.
Key results indicated that rice yields likely will not be affected by increases in UV-B
predicted from stratospheric ozone depletion under realistic tropical-field conditions
based on extensive and intensive field experiments (Dai etal. 1997). Under greenhouse
conditions, enhanced UV-B injury was associated with active oxygen metabolism in rice
leaves (Dai etal. 1997), and could affect the susceptibility of rice to the important disease,
rice blast (Finckh etal. 1995).
In contrast to enhanced UV-B, elevated C02 and temperature likely will have dramatic
effects on irrigated rice production, not only by directly affecting the plant, but also
through indirect effects on other aspects of the rice ecosystem (insects, diseases, and
weed competition). Elevated C02 enhanced rice plant growth and grain yield provided
that N fertilization was not limiting growth (Olszyk etal. 1999; Weerakoon etal. 1999; Ziska etal.
1998; Moya etal. 1998). In contrast, while elevated temperature enhanced plant growth, it
decreased crop yield due to spikelet sterility. Combining elevated C02 and elevated
temperature resulted also resulted in enhanced plant growth, but with spikelet sterility.
Climate change also was predicted to affect rice productivity by altering disease
occurrence (Luo etal. 1995) and insect infestations (Heong eta/. 1995).
Computer simulations and spatial analysis were used successfully to assess the
potential impacts of climate change on rice productivity across south and Southeast
Asia (sidebar). In the EPA/IRRI analysis, potential rice yield either decreased or
increased depending on the global climate model, crop model, and site within a country.
Overall, the analysis found an average 3.8% decrease in rice production across south
and Southeast Asia with future increases in C02 and temperature compared to current
conditions. Though relatively small, this predicted change would occur at a time when
rice yields must increase substantially to keep in step with increases in human
population in the area.
Unique field experiments indicated that the effects of elevated C02 and temperature on
rice plants could increase methane emissions from rice fields, providing an important
feedback to climate change from rice cultivation (Olszyk etal. 1999; Ziska etal. 1998).
Elevated C02 or in combination with elevated temperature produced a large increase in
methane emissions from rice fields compared to current conditions; primarily due to a
large increase in belowground biomass (see sidebar). In contrast, elevated temperature
alone tended to decrease methane emissions from rice fields. The magnitude of these
changes in methane emissions from rice fields were not predicted by current plant
growth simulation models (Olszyk et al. 1999).
-------
4. Rice 4-3
In addition to demonstrating impacts of climate change on the irrigated rice systems,
research indicated avenues to mitigate those impacts for this intensively managed
agricultural system. The wide-range in variability among rice cultivars and plant types in
terms of adverse effects from enhanced UV-B and elevated temperature, as well as
beneficial effects from elevated C02, indicates the potential for plant breeding to
maintain or enhance rice yields in the future (Moya etal. 1998; Dai etal. 1994). Similarly,
methane emissions from rice fields varied considerably with rice cultivar, fertilizer
amount and form, irrigation timing, and other factors, indicating the potential to reduce
methane emissions from rice fields through altered management practices (Neue etal.
1995).
-------
Rice 4-4
Elevated UV-B Radiation from Stratospheric O3 Depletion not expected to affect
Rice Yields
With depletion of the stratospheric O3 layer, ground-level UV-B levels are expected to increase. The
effect of potential increases in UV-B under realistic field conditions was determined in rice fields at the
International Rice Research Institute at Los Banos, the Philippines. Over five growing seasons, both wet
(cloudy, rainy) and dry (more sunlight, dry) two widely grown (yet potentially UV-B susceptible) rice
cultivars IR 72 and IR 74 exposed to current and enhanced UV-B radiation. There was no significant
UV-B effect on rice yield for either cultivar in any season. Across all seasons and both cultivars the
average yield was the same at 608 g m for both control and enhanced UV-B rice plants. Source: Dai et
al. 1997.
Increased Atmospheric CO2 and Air Temperature Affects Rice Yields and
Methane Emissions from Rice Fields
The effects of increased atmospheric CO2 and consequent predicted increases in air temperature were
studied for rice - the world's most important crop for direct human consumption. Both rice yield and
methane emissions, a greenhouse gas produced in rice soils, were measured for rice plants grown in
open-top chambers under realistic tropical field conditions at the International Rice Research Institute in
the Philippines. Yield and methane emissions were determined for the widely grown rice cultivar, IR 72,
grown for two wet and two dry seasons under current ambient CO2 and temperature conditions (ACAT)
and under three future climate scenarios of elevated CO2 and ambient temperature (ECAT), ambient CO2
and, elevated CO2 and elevated temperature (ECET). By itself, elevated CO2 increased rice yields, as
shown for many other crops grown under conditions of optimum N fertilization and water. However,
elevated temperature tended to decrease rice yields and thus the increase in rice yield with elevated CO2
alone was negated when temperature also elevated. Emissions of methane were increased when rice
plants were exposed to elevated CO2 either with or without elevated temperature, which was associated
with an increase in root biomass; while elevated temperature alone tended to decrease methane
emissions. Source: Olszyk, et al. 1999; Moya et al. 1998; Ziska et al. 1998.
Scenario3 Parameter 1994 Wet 1995 Dry 1995Wetb 1996 Dry
ACAT Grain Yield (g m"2) 366 683 — 874
ECAT Change Grain Yield (%)+29 +24 — +15
ACET Change Grain Yield (%)-26 -16 — -13
ECET Change Grain Yield (%)-14 +9 — -6
ACAT Methane (mg m"2 d"1) — — 142 260
ECAT Change in Methane (%) — — +60 +48
ACET Change in Methane (%) — — — -54
ECET Change in Methane (%) — — — +45
a Experimental values in bold are significantly different from ambient CO2 and ambient temperature at
p<0.05.
Rice yield severely decreased due to typhoon prior to crop maturity.
-------
4. Rice
4-5
Changes in Rice Grain Yield across East and South Asia with Elevated CO2 and
Elevated Temperature
Potential effects of climate change (elevated CO2 and elevated temperature) on irrigated rice production
across south and East Asia were estimated based on computer simulations and spatial analysis.
Climate change scenarios from the General Fluid Dynamcis Laboratory (GFDL), Goddard Institute of
Space Studies (GISS), and United Kingdom Meteorological Office (UKMO) General Circulation Models
(GCMs,) were used, assuming a doubling of current atmospheric CO2. The outputs from those models
were used with site-specific weather data and two plant process-based rice crop simulation models,
ORYZA1 and SIMRIWto predict potential rice yield under current and future climate conditions at sits
across Asia. The changes in rice yield with climate change were assessed using a Geographic
Information System (CIS). An example of the pattern of these changes in yield from current climate
conditions based on the UKMO GCM and ORYZA1 model is shown below. In this simulation, global
climate change produced increases in potential yield (green colors) for much of India and southeast Asia,
and decreases in yield (yellow to orange colors) in most of China, Japan and Korea; with an average
5.6% reduction in yield across all of Asia (Source: Matthews, Horie etal. 1995).
Percent change
CH -51 to -40
1 1 -3° to -27
L~H -26 to -14
d -13 to -1
D 0
m i to 10
m n to 20
HI 21 to 30
HI 31 to 41
Percent change in rice yield using UKMO climate compared
to current climate.
-------
Rice 4-6
References Cited
Cole, V. (Lead Author), 1996. Agricultural options for mitigation of greenhouse gas emissions, pp. 745-
771. In: Watson, R.T., Zinyowera, M. C., Moss. R.H., (Eds.), Climate Change 1995 Impacts, Adaptations
and Mitigation of Climate Change: Scientific Technical Analyses. 878 pp. Cambridge University Press,
New York.
Dai, Q., S. Peng, A.Q. Chavez, and B.S. Vergara. 1994. Intraspecific responses of 188 rice cultivars to
enhanced UV-B radiation. Environmental and Experimental Botany Vol. 34,433442.
Dai, Q. , B.Yan, S. Huang, X. Liu, S. Peng, Ma. L.L. Miranda, A.Q. Chavez, B.S. Vergara and D.M.
Olszyk. 1997. Response of oxidative stress defense systems in rice (Oryza sativa) leaves with
supplemental UV-B radiation. Physiologia Plantarum 101,301-308.
Dai, Q. , S. Peng, A.Q. Chavez, Ma. L.M. Miranda, B.S. Vergara, and D.M. Olszyk. 1997. Supplemental
Ultraviolet-B radiation does not reduce growth or grain yield in rice. Results From a 7-season field study.
Agronomy Journal 89,793-799.
Finckh, M.A., A.O. Chavez and P.S. Teng. 1995. Effects of UV-B radiation on the susceptibility of rice to
rice blast. Agriculture, Ecosystems & Environment 52,223-233.
Heong, K.L., Y.H. Song, S. Pimsamarn, R. Zhang, and S.D. Bae. 1995. Global warming and rice
arthropod communities, pp. 326-335, In, Peng S., K. Ingram, H. U. Neue, L. Ziska, Eds. Climate change
and rice. Springer- Verlag, Berlin.
International Rice Research Institute (IRRI), 1993. 1993-1995 IRRI Rice Almanac, IRRI, Los Banos,
Philippines.
Luo Y., D.O. TeBeest, P.S. Teng, and N.G. Fabellar. 1995. Simulation studies on risk analysis of rice leaf
blast epidemics associated with global climate change in several Asian countries. Journal of
Biogeography 22:673-678.
Matthews, R.B., T. Horie, M.J. Kropff, D. Bachlelet,H.G. Centeno, J.C. Shin, S. Mohandass, S. Singh, Z.
Defeng, and M.H. Lee. 1995. A regional evaluation of the effect of future climate change on rice
production in Asia, pp. 95-139, In, Matthews, R.B., M.J. Kropff, D. Bachlelet, and H.H. Van Laar, eds.
Modeling the impact of climate change on rice production in Asia. CAB International, Wallingford, U.K.
Matthews, R.B., M.J. Kropff, D. Bachlelet, and H.H. Van Laar. 1995. Modeling the impact of climate
change on rice production in Asia. CAB International.
Moya, T., O.S. Namuco, L.H. Ziska, and D. Olszyk. 1998. Growth dynamics and genotypic variation in
tropical, field-grown paddy rice (Oryza sativa L.) with increasing carbon dioxide and temperature. Global
Change Biology 4,645-656.
Neue, H-U. 1993. Methane emission from rice fields. BioScience 43,466-474.
Neue. H.-U., Wassmann, R., and R.S. Lantin. 1995. Mitigation options for methane emissions from rice
fields, pp. 136-144, In, Peng S., K. Ingram, H. U. Neue, L. Ziska, Eds. Climate change and rice. Springer-
Verlag, Berlin.
Olszyk, D.M. and K.T. Ingram. 1991. Effects of UV-B and global change on rice production: The EPA/IRRI
-------
4. Rice 4-7
Cooperative Research Plan. Pp. 234-253. In, M. llyas, Ed., Ozone Depletion Implications of the
Tropics.University Science Malaysia and U.N. Environmental Programme.
Olszyk, D., Q. Dai, P. Teng, H. Leung, Y. Luo and S. Peng . 1996. UV-B Effects on Crops: Response of
the Irrigated Rice Ecosystem. Journal of. Plant Physiology, 148,26-34.
Olszyk, D.M., H.G.S. Centeno, L.H. Ziska, J.S.Kern, and R.B. Matthews. 1999. Global Change, Rice
Productivity and Methane Emissions: Comparison of Predicted and Experimental Results. Agricultural
and Forest Meteorology 9,87-101.
Peng S., K. Ingram, H. U. Neue, L. Ziska, Eds. Climate change and rice. 1995. Springer- Verlag, Berlin.
Weerakoon, W. M., D.M. Olszyk, and D.N. Moss. 1999. Effects of Nitrogen Nutrition on Responses of
Rice Seedlings to Carbon Dioxide. Agriculture Ecosystems and Environment 72,1-8.
Zhang, R., K.L. Heong, and Q. Dai. 1994. Effect of elevated ultraviolet-B radiation on abscisic acid and
indoleacetic acid content of rice leaves. IRRN 19,:56-57 September.
Ziska, L.H., P.A. Manalo, and R. Ordonez. 1996. Intraspecific variation in the response of rice (Oryza
sativa L.) to increased C02: Evaluation of 17 cultivars. Journal of Experimental Botany 47,1353-1359.
Ziska, L.H. and P.A. Manalo. 1996. Increasing night temperature reduces seed set in tropical rice.
Australian Journal of Plant Physiology. 23,791-794.
Ziska, L. H., 0. S. Namuco, T. B. Moya, T. Matsui, and J. Quilang. 1997. Growth and yield
response of field-grown tropical rice to increasing C02 and air temperature. Agronomy Journal 89,45-53.
Ziska, L.H., W. Weerakoon, O.S. Namuco, and R. Pamplona. 1996. The influence of nitrogen on the
elevated C02 response in field-grown rice. Australian Journal of Plant Physiology 23,45-52.
Ziska, L.H., T. Moya, O.S. Namuco, R. Levine, R. Wassman, and D. Olszyk. 1998. Elevated carbon
dioxide stimulates methane emission in tropical paddy rice. Global Change Biology 4:657-665.
-------
5. Ag Soils 5-1
5. Agriculture - Crop yields, soil erosion, and soil carbon
Statement of the Problem
Rising atmospheric C02 concentrations and global climate change could potentially
have significant effects on American agriculture. While elevated C02 may have a
beneficial effect on crop growth, increased temperature and changes in precipitation,
wind, and other climatic variables may alter crop yields. These climatic changes may
also affect rates of soil erosion and the carbon content of agricultural soils, which may
affect carbon sequestration.
Soils are a major reservoir of global carbon, and are equal in magnitude to the
combined global carbon content of the entire atmosphere plus all aboveground
biomass. Loss of agricultural soil carbon through erosion, management, and
decomposition adds to the atmospheric loading of CC^. Agricultural management
practices which conserve or sequester soil carbon can help mitigate the rate of increase
of atmospheric CC^. Assessments of the potential for such mitigation through
widespread adoption of best management practices for major American agricultural
areas are needed as well.
Approach
Research focused on model assessments of the sensitivity of soil erosion to
precipitation change scenarios across the US, and more detailed evaluations of crop
yield, soil erosion, and soil carbon responses to climate change scenarios including
temperature, precipitation, wind, and C02 in the US Corn Belt. The research focused on
two erosional processes: (1) water erosion which is the loss of soil due to rainfall runoff
from field crops, and (2) wind erosion which is the loss of soil due to wind blown
particles. Assessments were also made of the effects of widespread adoption of
various management practices on soil erosion and soil carbon in the United States to
mitigate the rate of atmospheric C02 increase. Management scenarios included the
current mix of tillage and crop rotation practices, and increased use of crop rotation and
conservation tillage practices which have become more prevalent in recent years.
Main Conclusions
Projected water erosion of soil for U.S. croplands, pasturelands, and rangelands
increased with increases in precipitation in the 2xC02 climate change scenarios from
four atmospheric General Circulation Models (Phillips et al. I993b). Changes in erosion
were greater when precipitation changes were assumed to be from changes in storm
intensity rather than storm frequency, indicating the importance of the manner in which
climatic changes occur in addition to their mean magnitude. Recent reductions in
national soil erosion indicate the potential for management changes to mitigate the
magnitude of erosion increases projected under these climate change scenarios.
-------
5. Ag Soils 5-2
In a detailed model assessment using 36 climate/CC^ scenarios for croplands in the
U.S. Corn Belt, water erosion linearly tracked increasing or decreasing precipitation, but
wind erosion showed dramatic increases as mean wind speeds increased (Lee etai.
1996). Increasing temperature alone decreased water erosion while increasing wind
erosion and total erosion (water and wind). But, beneficial effects of elevated C02 on
plant growth nullified this effect on total soil erosion.
Typical of agricultural soils under long-term cultivation, soil carbon decreased over the
100 year simulations, adding to atmospheric C02 loadings. This carbon loss was
accelerated by increased temperature and precipitation, but elevated C02 slowed the
loss rate. Corn and soybean crop yields were projected to decrease slightly due to
temperature or wind increases alone, track precipitation increases or decreases, and
increase markedly in response to an 80% increase in C02 (Phillips etal. 1996).
Model assessments of alternative management practices in the U.S. Corn Belt showed
that increasing use of conservation tillage practices such as mulch-till and no-till could
substantially reduce the loss of soil carbon due to erosion and decomposition (Phillips et
al. I993a, Lee etal. 1993). Agricultural soils could become a small sink for carbon with
widespread use of no-till cultivation and use of a winter cover crop (Lee etal. 1993). This
indicates the potential for changing agricultural management practices to mitigate the
buildup of atmospheric C02 and associated climatic change. Conservation tillage is
economically and functionally feasible and is likely to occur because of land and soil
conservation benefits from conservation tillage and rising fuel costs (Kern and Johnson
1993).
-------
5. Ag Soils
5-3
Wind and water erosion
Sensitivity of Corn Belt soil erosion to climatic changes
I
40
30
20
c
o
'55
2
HI
=5 10
A
Wind
Erosion
Water
Erosion
0.8 0.9 1.0 1.1
Precipitation or Wind Speed Ratio
1.2
This figure shows projected soil loss by water and wind erosion across croplands in
the U.S. Corn Belt under an elevated atmospheric C02 concentration of 625 ppm
and a temperature increase of 2° C above current conditions. Current conditions for
precipitation and wind speed are represented by a ratio of 1.0. When precipitation in
the climate scenario is varied from 20% below current levels (ratio of 0.8) to 20%
above current levels (ratio of 1.2), water erosion increases linearly. In contrast as
mean wind speeds in the climate scenario are varied from -20% to +20% compared
to current levels, there is a dramatic non-linear increase in wind erosion.
-------
5. Ag Soils 5-4
Carbon Sequestration in Soil
Soil organic matter is the largest global terrestrial carbon (C) pool and is a source of C02, ChU, and other
greenhouse gases. Soil management affects the amount of C held in soil and the greenhouse gas emissions
from soil. In the agricultural sector conventional tillage practices such as the use of a moldboard plow, lead to
a steady loss of soil C to the atmosphere. In contrast, conservation tillage practices that include minimum
tillage and no-till conserve soil C and reduce that amount of fossil fuel needed for tillage.
Kern and Johnson (1993) conducted an analysis of the amount of soil C that would either be lost or
sequestered and the amount of fossil fuel required for agriculture in the contiguous United States using three
scenarios of conservation tillage: 27% (Scenario 1), 57% (Scenario 2) and 76% (Scenario 3). The analysis
covered 30 years beginning in 1990. For Scenario 1, the level of conservation tillage was held constant at the
actual 1990 level of 27% for 30 years. For Scenarios 2 and 3, both began at 27% in 1990 and linearly ramped
up to 57% and 76%, respectively, over the first 20 years of the analysis and were held constant for the
remaining 10 years.
Maintaining 1990 levels of conventional and conservation tillage resulted in a net loss of 41 Tg of soil C (1 Tg =
1012g) over the 30-year period while using 157 Tg of fossil fuel. A combined 198 Tg of C was estimated to be
added to the atmosphere under Scenario 1. For Scenario 2, a net sequestration of C in soil (+80 Tg) was
achieved while fuel consumption dropped slightly. Fossil fuel consumption did not drop concomitantly because
reduced tillage systems require more herbicides and pesticides - derived from fossil fuels - than conventional
tillage systems. For Scenario 3, an additional 364 Tg of soil C sequestered and 146 Tg of fossil fuel
consumed, for a net gain of 218 Tg of C.
Changes in soil organic C and fossil fuel C emission for three scenarios of
conservation tillage (CT) for agriculture in the contiguous U.S. projected from 1990
to 2020.
Scenarios of Conservation Tillage (CT)
27% CTa 57% CTb 76% CTC
Tillage System Soil Fuel Soil Fuel Soil Fuel
Conventional Tillage -41 -121 -24 -87 -13 -67
Minimum Tillage 0 -30 0 -52 0 -66
No-Tillage 0 -6 +104 -10 +377 -13
Sums -41 -157 +80 -149 +364 -146
Net Loss (-) or Gains (+) -198 -69 +218
a)27% CT scenario uses the level of conservation tillage used in 1990 (-27%) held constant for 30 years until
2020.
b) 57% CT scenario begins in 1990 with 27% conservation tillage and linearly ramps up to 57% conservation
tillage over 20 years (2010) and remains constant at 57% until 2020.
c) 76% CT scenario begins in 1990 with 27% conservation tillage and linearly ramps up to 76% conservation
tillage over 20 years (2010) and remains constant at 76% until 2020.
-------
5. Ag Soils 5-5
References Cited
Kern, J.S. and M.G. Johnson. 1993. Conservation Tillage Impacts on National Soil and Atmospheric
Carbon Levels. Soil Science Society of America Journal 57:200-210.
Lee, J.J., D.L. Phillips, and R. Liu. 1993. The effect of trends in tillage practices on erosion and carbon
content of soils in the U.S. Corn Belt. Water, Air, and Soil Pollution 70: 389-401.
Lee, J.J., D.L. Phillips, and R.F. Dodson. 1996. Sensitivity of the U.S. Corn Belt to climate change and
elevated CO2: II. Soil erosion and organic carbon. Agricultural Systems 52: 503-521.
Phillips, D.L., P.O. Hardin, V.W. Benson, and J.V. Baglio. 1993a. Non-point source pollution impacts of
alternative agricultural management practices in Illinois: a simulation study. Journal of Soil and Water
Conservation 48: 449-457.
Phillips, D.L., D. White, and C.B. Johnson. 1993b. Implications of climate change scenarios for soil
erosion potential in the United States. Land Degradation and Rehabilitation 4: 61-72.
Phillips, D.L., J.J. Lee, and R.F. Dodson. 1996. Sensitivity of the U.S. Corn Belt to climate change and
elevated CO2: I. Corn and soybean yields. Agricultural Systems 52: 481-502.
-------
6. Forest Management 6-1
6. The Global Carbon Cycle: Managing Forest Systems
Statement of the Problem
The accumulation of C02 in the atmosphere due to fossil fuel use, deforestation and other
anthropogenic sources is changing the global climate (Harries etal. 2001; IPCC 2002). Current
understanding of the global carbon cycle suggests that managing forests and agricultural
lands to increase the sequestration of greenhouse gases (GHG) provide credible policy
options (Dixon and Turner 1991, Winjum etal. 1993a, Brown 1996a, Brown etal. 1996). EPA/WED
research efforts during the 1990's estimated the amount of that carbon which could be
sequestered by purposeful management actions, and the incidental amount of carbon that
inadvertent land use is likely to release to the atmosphere in the future. The three specific
objectives of this research were to: 1) develop or refine global, country-level and regional
estimates of carbon pools and fluxes in forests, 2) evaluate the potential to conserve and
manage forests to expand the accumulation of carbon, and, 3) project future forest carbon
pools and fluxes during expected changes in climate and land-use. The annual exchange of
carbon between forests and the atmosphere, and the amounts of carbon stored in forests,
varies widely with the nature of forest cover. With land use and management, and with
climatic constraints, our research showed that management of forests can significantly
increase the long-term sequestration of atmospheric CC^. However, management efforts
aimed at storing carbon in the tropics - the largest pools on Earth - are being countered by
carbon emissions from forest destruction.
Approach
We developed several methods to quantify the major carbon pools and fluxes in forested
ecosystems (Winjum etal. 1993b, Turneretal. 1995,1997, Brown etal. 1999). Forest carbon budgets
were constructed with recently completed national carbon budgets, and with global, national
or regional databases of carbon densities in various above and below-ground forest pools
(Dixon and Turner 1992; Kolchugina and Vinson 1993a; Cairns etal. 1997), in forest products (Winjum etal.
1998), and in differing land uses (Brown I996b) and forest areas (Gaston etal. 1994,1997).
NHEERL researchers applied available static geographic models (Turner and Leemans, 1992; King
and Neilson 1992, Lugo et al, 1999) or developed new models (Prentice etal. 1992; Solomon etal. 1993;
Neilson 1995; Kirilenko and Solomon 1998), each using the distributions of current climate variables
as proxies for vegetation and carbon stocks. The data sets and information developed in
these studies were then used as a base against which to contrast the amounts of carbon that
is sequestered by various management techniques (e.g., Winjum et al I993b, Dixon 1995,1997;
Dixon etal. 1993,1994b). The distribution of future climatic conditions projected by climate
models could then be used to assess distributions and amounts of future carbon stocks. The
future global carbon stock estimates from the static geographic models are discussed under
"F-Vegetation Redistribution" and will not be reiterated here.
Main Conclusions
Forests play a prominent role in the global carbon cycle and the accumulation of GHG in the
atmosphere, but the roles vary regionally (Dixon et al. 1994). In the conterminous United States,
for example, total forest carbon was calculated to be 36.7 Gt C (Gt = Gigatons, i.e., a billion
tonnes), with annual uptake of about 331 Mt (million tons) C, and losses to harvests of 266 Mt
-------
6. Forest Management 6-2
C (Turner et al. 1995). However, a different method suggested that annual carbon uptake for
eastern U.S. forests during the late 1980s and early 1990s was about 416 Mt C/yr (Brown and
Schroeder 1999). In the eastern United States, forest carbon stocks were estimated at 20.5 Gt,
80% of that found in hardwoods (Brown et a/. 1999). Schroeder et al. (1997) noted that these
carbon stocks were distributed primarily in small stands or lots with small trees, and in larger
stands with large trees. This suggests that most carbon in the eastern U.S. is stored in young
forests growing on abandoned farms and in forest reserves with large mature trees. An error
analysis of the southeastern carbon stocks (Phillips et al. 2000) showed that sampling error was
only about 1% (95% confidence intervals) but that annual carbon increments carried errors of
about +/- 40%.
These carbon stocks and fluxes from the temperate U.S. forests were compared to estimates
we developed in boreal and tropical regions, and for the world as a whole. Globally, forest
vegetation and soils contain about 1146 Gt of C, with approximately 37% of this carbon in low-
latitude forests, 1/7 in mid-latitudes, and 49% at high latitudes. Over two-thirds of the carbon
in forest ecosystems is contained in soils and associated peat deposits (Dixon et al. I994a). The
carbon stocks and fluxes of the former Soviet Union (FSU) were examined in several papers
which focused on the large portion of the world's biomass held by the boreal forests and
peatlands.
Based on calculations from mapped ecoregions of the FSU, and estimated carbon stocks and
fluxes in those ecoregions, the FSU forests were estimated to contain 69 and 110 Gt C above
ground, and 331 and 337 Gt C below ground (Kolchugina and Vinson, 1993b and 1993c,
respectively). A third paper in the series (Vinson and Kolchugina 1993) indicated similar values of
118 Gt C above ground for all vegetation, and 423 Gt C below ground. Unique environments
(permafrost, peatlands) of the FSU were analyzed separately, indicating that permafrost
carried 17 Gt C above ground and 155 Gt C in soils and litter (Kolchugina and Vinson 1993d,
I993e), including peatland carbon. Carbon in peatlands evaluated alone (Botch et al. 1995) was
estimated at 215 Gt C.
Estimates of carbon stocks and fluxes from several tropical regions provided additional depth
to the analysis. Africa, for example, was determined to contain 50.6 Gt C in all vegetation
cover, both above and below ground (Gaston et al. 1998). In the western Hemisphere, Brazil
contains the world's largest expanse of tropical forests, with 136-162 Gt C in above and
below-ground vegetation and litter (Schroeder and Winjum I995a), and net emissions of carbon to
the atmosphere of 174-233 Mt yearly (Schroeder and Winjum I995b) projected for the 20-yr period
of 1990 to 2010 (Schroeder and Winjum 1995c, Schroeder 1996). Delany et al (1997,1998) determined
that Venezuelan forests held 300-500 T/ha C, with 20-37% of that on and below ground and
with turnover time of litter into C02 being very rapid (<2 yrs). Biomass burning in Costa Rica
(Helmerand Brown 2000) contributed to considerable C02 emissions as well, primarily from
lowland forest destruction.
In Mexico, like Costa Rica, most carbon stock changes near the end of the 20th century were
attributable to destruction of tropical and subtropical forests (Cairns et al. 1995,1996), from
southern Mexico (Riley et al. 1997, Schuft et al. 1998, Cairns et al. 2000), to the Mexican central
highlands (De Jong etal. 1999,2000). The data from Brazil, Mexico, the U.S. and the former
-------
6. Forest Management 6-3
Soviet Union, were combined in several papers, both for comparing overall carbon budgets
(Turner etal. 1997, 1998, without Mexico), and to compare land use effects (Cairns etal. 1997).
The results amplified conclusions reached in earlier analyses, demonstrating the importance
of reducing land use impacts on forest biomass in tropical areas, and of applying forest
management techniques to enhance carbon sequestration in tropical, temperate and boreal
regions.
Slowing deforestation, combined with an increase in forestation and other management
measures to improve forest ecosystem productivity, could conserve or sequester significant
quantities of C. Future forest carbon cycling trends attributable to losses and regrowth
associated with global climate and land-use change are uncertain (Dixon etal. 1999). Model
projections and field experiments suggest that forests could be carbon sinks or sources in the
future (Dixon etal. 1994). To the end, forest carbon conservation and sequestration options have
become major policy instruments of the UN Framework Convention on Climate Change
Activities (UNFCCC) Implemented Jointly (AIJ) pilot over the past decade (Dixon 1999, Dixon
1995).
-------
6. Forest Management 6-4
Estimates of carbon pools and flux in forest vegetation in world forests
Latitudinal Belt
High
Russia
Canada
Alaska
Subtotal
Mid
Cont'l US
European3
China
Australia
Subtotal
Low
Asia
Africa
Americas
Subtotal
TOTAL
1Pg=1015
C Pools
Vegetation
74
12
2
88
15
9
17
18
59
41b-54
52 b
119b
212
359
(Pg)
Soils
249
211
11
471
26
25
16
33
100
43
63C
110C
216
787
g or 1 gigatonne
The table shows estimated carbon
pools and area-weighted carbon
densities in forest vegetation (above-
and below-ground living and dead
mass) and soils (O horizon, mineral
soil to a depth of I m, and co-located
peatlands) in forests of the world
(from Dixon et al 1999).
a Includes Nordic nations. A factor of
1.75 was used to convert stem to total
vegetation biomass. For soil C, an
average of 9 kg m2 for temperate forests
and the forest area in Table 1 was used.
b Estimated as the product of carbon
densities by ecofloristic zone and areas
of forest in each zone, corrected for
roots, non-tree components, and woody
debris.
c Estimated as the product of forest area
and an average of 12 kg m2 of soil
organic C.
Forests are important in the global
carbon cycle because they store more
than 55% of the global carbon stored in
vegetation and more than 45% of that
stored in soils, exchange carbon with
the atmosphere through photosynthesis
and respiration, are sources of
atmospheric carbon when they are
disturbed by human or natural causes
and become atmospheric carbon sinks
during regrowth after disturbance
Forests can influence climate change
by affecting the level of C02 in the
atmosphere; through the production of
other greenhouse gases such as
carbon monoxide, ozone, and nitrous
oxide; and through changes in albedo of
land as forests are converted to other
land cover types.
Globally, forest vegetation and soils
contain approximately 359 and 787 Pg
of C, respectively (Pg= 1,000 million
tonnes). Earlier projections ranged
from 953 to 1400 Pg of global C. The
allocation of carbon between vegetation
and soils differs by latitude, with a large
part of the vegetation (25%) and soil
(59%) carbon pools located in the high-
latitude forests. Mid-latitude forests
account for a small portion of the global
carbon pool (16 and 13% of the
vegetation and soil, respectively). Low-
latitude tropical forests are relatively
heterogeneous and contain 59 and 27%
of global forest vegetation and soil C,
respectively (Dixon et al. 1994a).
-------
6. Forest Management
6-5
Carbon Sequestration Potential
Global estimates of potential amount ofC that could be sequestered and
conserved by forest management practices between 1995 and 2050 (from
Brown et al 1996a)
Latitudinal Country/ Practice C Sequestered/
Belt Region Conserved (Gt)
High Canada Forestation 0.68
Nordic Europe 0.03
FSU 1.76
Subtotal 2.4
Mid Canada Forestation 0.43
USA 3.07
Europe 0.96
China 1.70
Asia 2.19
South Africa 0.44
South America 1.02
Australia 0.31
New Zealand 1 .7
Subtotal 11.8
USA Agroforestry 0.29
Australia 0.36
Subtotal 0.7
Low Tr. America Forestation 8.02
Tr. Africa 0 90
Tr. Asia 7.50
Subtotal 16.4
Tr. America Agroforestry ' •""
Tr. Africa 2.63
Tr. Asia 2.03
Subtotal 6.3
Tr. America Regeneration2 4.8-14.3
Tr. Africa 3.0-6.7
Tr. Asia 3.8-7.7
Subtotal 11.5-28.7
Tr. America Slow 5.0-10.7
Deforestation1
Tr. Africa 2.5-4.4
Tr.Asia 3.3-5.8
Subtotal 10-8-20.8
Total 60-87
'Includes an additional 25% of aboveground C to account for belowgmund C in
roots, litter, and soil (based on data in Brown eta/.., 1996); range in values
is based on the use of low and high estimates of biomass C density resulting
from the uncertainty in these estimates.
Humans change the size of carbon
^f
pools and alter the flow of carbon
between them through forest
management. Forests can become
atmospheric carbon sinks during
regrowth and can be managed to alter
their role in the carbon cycle. Local
forests management for carbon
conservation and sequestration could
mitigate emission of carbon C02 by an
amount equivalent to 1 1 to 15 percent
Of fOSSil fuel emissions (Brown etal. 1996).
Estimates of unrealized global forest
carbon conservation and sequestration
range from 1 to 3 Pg C annually for as
much as a century. Forest
management practices to conserve
and sequester carbon can be grouped
into four major categories: 1) maintain
existing carbon pools (e.g., slow
deforestation) (Dixon etal. 1993), 2)
expand existing carbon sinks and pools
through forest management (Dixon
1997), 3) create new sinks and pools by
expanding tree and forest cover (Winjum
etal. 1992), and, 4) substitute renewable
wood-based fuels and products for
those derived from fossil fuels (Dixon et
al. I994b). Management of forests as
carbon reservoirs often complements
other environmental goals including
protection of biologic, water, and soil
resources.
-------
6. Forest Management 6-6
References
Botch, M. S., K. I. Kobak, T. S. Vinson and T. P. Kolchugina. 1995. Carbon pools and accumulation in peatlands
of the former Soviet Union. Global Biogeochemical Cycles 9:37-46.
Brown, S. 1996a. Tropical forests and the global carbon cycle: Estimating state and change in biomass density.
Pp. 135-144 IN M. Apps and D. Price, eds., The Role of Forest Ecosystems and Forest Management in the
Global Carbon Cycle. NATO ASI Series No. 140, Springer-Verlag, NY.
Brown, S. 1996b. Present and potential roles of forests in the global climate change debate. Unasylva 185:3-9.
Brown, Sandra, J. Sathaye, Melvin Cannell and P. Kauppi. 1996. Management of forests for mitigation of
greenhouse gas emissions. In Climate Change 1995. Robert T. Watson, Marufu C. Zinyowera and Richard H.
Moss, editors. Ch 24:773-797.
Brown, S. and P. E. Schroeder. 1999. Spatial patterns of aboveground production and mortality of woody
biomass for eastern U.S. forests. Ecological Applications 9:968-980.
Brown, S., P. E. Schroeder and J. S. Kern. 1999. Spatial distribution of biomass in forests of the eastern USA.
Forest Ecology and Management 123:81-90.
Cairns, M. A., R. Dirzo and F. Zadroga. 1995. Forests of Mexico. Journal of Forestry 93:21024.
Cairns, M. A., J. R. Barker, R. W. Shea and P. K. Haggerty. 1996. Carbon dynamics of Mexican tropical
evergreen forests: Influence of forestry mitigation options and refinement of carbon-flux estimates. Interciencia
21:216-223.
Cairns, M. A., J. K. Winjum, D. L. Phillips, T. P. Kolchugina and T. S. Vinson. 1997. Terrestrial carbon dynamics:
Case studies in the former Soviet Union, the conterminous United States, Mexico and Brazil. Mitigation and
Adaptation Strategies for Global Change 1:363-383.
Cairns, M. A., P. K. Haggerty, R. Alvarez, B. H. J. De Jong and I. Olmsted. 2000. Tropical Mexico's recent land-
use and land-cover change: A region's contribution to the global carbon cycle. Ecological Applications 10:1426-
1441.
De Jong, B. H. J., M. A. Cairns, P. K. Haggerty, N. Ramirez-Marcial, S. Ochoa-Gaona, J. Mendoza-Vega, M.
Gonzalez-Espinosa, and I. March-Mifsut. 1999. Land-use change and carbon flux between the 1970's and
1990's in central highlands of Chiapas, Mexico. Journal of Environmental Management 23:373-385.
De Jong, B. H. J., S. Ochoa-Gaona, M. A. Castillo-Santiago, N. Ramirez-Marcial and M. A. Cairns. 2000. Carbon
flux and patterns of land use/land-cover change in the Selva Lacandona, Mexico. Ambio :503-511.
Delany, M., S. Brown, A. Lugo, A. Torres-Lezama and N. B. Quintero. 1997. The distribution of organic carbon in
major components of forests located in six life zones of Venezuela. Journal of Tropical Ecology 13:697-708.
Delany, M., S. Brown, A. Lugo, A. Torres-Lezama and N. B. Quintero. 1998. The quantity and turnover of dead
wood in permanent forest plots in six life zones of Venezuela. Biotropica 30:2-11.
Dixon,R.K. 1995. Agroforestry systems: sources or sinks of greenhouse gases? Agroforestry Systems 31:99-
116.
Dixon, R.K. 1997. Silvicultural options to conserve and sequester carbon in forest systems: preliminary
economic assessment. Critical Reviews in Environmental Science and Technology 27:139-151.
Dixon, R.K. and D.P. Turner. 1991. The global carbon cycle and climate change: responses and feedbacks from
below-ground systems. Environmental Pollution 73: 245-262.
-------
6. Forest Management 6-7
Dixon and Turner, 1992.
Dixon, R.K., J.K. Winjum, P.E. Schroeder. 1993. Conservation and sequestration of Carbon: The potential of
forest and agroforest management practices. Global Environmental Change 3:159-171.
Dixon, R.K., S. Brown, R.A. Houghton, A.M. Solomon, M.C. Trexlerand J. Wisniewski. 1994a. Carbon pools and
flux of global forest ecosystems. Science 263:185-190.
Dixon, R.K., J.K. Winjum, K.J. Andrasko, J.J. Lee and P.E. Schroeder. 1994b. Integrated land-use systems:
assessment of promising agroforest and alternative land use practices to enhance carbon conservation and
sequestration. Climatic Change 27:71-92.
Dixon,R.K., J.B. Smith, S. Brown, O. Masera, L.J. Mata, I. Buksha. 1999. Simulations of forest system response
and feedbacks to global change: experiences and results from the U.S. Country Studies Program. Ecological
Modelling 122:289-305.
Gaston, G. G., P. L. Jackson, T. S. Vinson, T. P. Kolchugina, M. Botch and K. Kobak. 1994. Identification of
carbon quantifiable regions in the former Soviet Union using unsupervised classification of AVHRR global
vegetation index images. International Journal of Remote Sensing 15:3199-3221.
Gaston, G. G., P. M. Bradley, T. S. Vinson, and T. P. Kolchugina. 1997. Forest ecosystem modeling in the
Russian Far East using vegetation and land-cover regions identified by classification of GVI. Photogrammetric
Engineering and Remote Sensing 63:51-58.
Gaston, G. G., S. Brown, M. Lorenzini and K. D. Singh. 1998. State and change in carbon pools in the forest of
tropical Africa. Global Change Biology 4:97-114.
Harries, J. E., H. E. Brindley, P. J. Sagoo and R. J. Bantges. 2001. Increases in greenhouse forcing inferred from
the outgoing longwave radiation spectra of the Earth in 1970 and 1997. Nature 410:355-357.
Helmer, E. H. and S. Brown. 2000. Gradient analysis of biomass in Costa Rica and an estimate of total
emissions of greenhouse gases from biomass burning. Pp. 503-526 IN C. A. Hall, ed. Ecology of Tropical
Development: The Myth of Sustainable Development in Costa Rica. Academic Press, San Diego CA.
IPCC, 2001. Climate Change 2001. Volumes 1-3, Third Assessment Report, Intergovernmental Panel on Climate
Change, Cambridge University Press, Cambridge UK.
King, G. A. and R. P. Neilson. 1992. The transient response of vegetation to climate change: A potential source
of CO2 to the atmosphere. Water, Air and Soil Pollution 64:365-383.
Kirilenko, A. P. and A. M. Solomon. 1998. Modeling dynamic vegetation response to rapid climate change using
bioclimatic classification. Climatic Change 38:15-49.
Kolchugina, T. P. and T. S. Vinson, 1993a. Comparison of two methods to assess the carbon budget of forest
biomes in the former Soviet Union. Water, Air and Soil Pollution 70:207-221.
Kolchugina, T. P. and T. S. Vinson. 1993b. Carbon sources and sinks in forest biomes of the former Soviet
Union. Global Biogeochemical Cycles 7:291-304.
Kolchugina, T. P. and T. S. Vinson. 1993c. Equilibrium analysis of carbon pools and fluxes of forest biomes in
the former Soviet Union. Canadian Journal of Forest Research 23:81-88.
Kolchugina, T. P. and T. S. Vinson. 1993d. Climate warming and the carbon cycle in the permafrost zone of the
former Soviet Union. Permafrost and Periglacial Processes 4:149-163.
-------
6. Forest Management 6-8
Kolchugina, T. P. and T. S. Vinson. 1993e. Carbon balance of the countinous permafrost zone of Russia.
Climate Research 3:13-21.
Lugo, A. E., S. Brown, R. Dodson, T. M. Smith and H. H. Shugart. 1999. The Holdridge Life Zones of the
conterminous United States in relation to ecosystem management. Journal of Biogeography 26:1025-1038.
Neilson, Ronald P. 1995. A model for predicting continental-scale vegetation distribution and water balance.
Ecological Applications 5:362-385.
Phillips, D. L., S. Brown, P. E. Schroeder and R. A. Birdsey. 2000. Toward error analysis of large-scale forest
carbon budgets. Global Ecology and Biogeography 9:305-313.
Prentice, I. C., W. Cramer, S. P. Harrison, R. Leemans, R. A. Monserud, and A. M. Solomon. 1992. A global
biome model based on plant physiology and dominance, soil properties and climate. Journal of Biogeography
19:117-134.
Riley, R. H., D. L. Phillips, M. J. Schuft and M. C. Garcia. 1997. Resolution and error in measuring land-cover
change: Effects on estimating net carbon release from Mexican terrestrial ecosystems. Int. J. Remote Sensing
18:121-137.
Schroeder, P. E. and J. K. Winjum. 1995a. Assessing Brazil's carbon budget I. Biotic carbon pools. Forest
Ecology and Management 75:77-86.
Schroeder, P. E. and J. K. Winjum. 1995b. Assessing Brazil's carbon budget II. Biotic fluxes and net carbon
balance. Forest Ecology and Management 75:87-99.
Schroeder, P. E. and J. K. Winjum. 1995c. Brazil's carbon budget for 1990. Interciencia 20:68-75.
Schroeder, P. E. 1996. A carbon budget for Brazil: Influence of future land-use change. Climatic Change 33:369-
383.
Schroeder, P. E., S. Brown, J-M. Mo, R. Birdsey and C. Cieszewski. 1997. Biomass estimation for temperate
broadleaved forest of the United States using inventory data. Forest Science 43:424-434.
Schuft, M. J., J. R. Barker and M. A. Cairns. 1998. Spatial distribution of carbon stocks in southeast Mexican
forests. Geocarto International 13:77-86
Solomon, A. M., I. C. Prentice, R. Leemans and W. P. Cramer. 1993. The interaction of climate and land use in
future terrestrial carbon storage and release. Water, Air, and Soil Pollution 70:595-614.
Turner, D. P., G. J. Koerper, M. E. Harmon and J. J. Lee. 1995. A carbon budget for forests of the conterminous
United States. Ecological Applications 5:421-436.
Turner, D. P. J. K. Winjum, T. P. Kolchugina, and M. A. Cairns. 1997. Accounting for biological and
anthropogenic factors in national land-base carbon budgets. Ambio 26:220-226.
Turner, D. P. J. K. Winjum, T. P. Kolchugina, T. S. Vinson, P. E. Schroeder, D. L. Phillips and M. A. Cairns.
1998. Estimating the terrestrial C carbon pools of the former Soviet Union, the conterminous United States and
Brazil. Climate Research 9:183-196.
Vinson, T. S. and T. P. Kolchugina. 1993. Pools and fluxes of biogenic carbon in the former Soviet Union. Water,
Air and Soil Pollution 70: 223-237.
Winjum, J.K., R.K. Dixon and P.E. Schroeder. 1993a. Forest management and carbon storage: analysis of 12
key forest nations. Water, Air and Soil Pollution 70:239-257.
-------
6. Forest Management 6-9
Winjum,J.K., R.A. Meganck, and R.K. Dixon. 1993b. Expanding global forest management: an easy-first
approach. Journal of Forestry 91: 38-42.
Winjum, J.K., R.K. Dixon and P.E. Schroeder. 1992. Estimating the global potential of forest and agroforest
management practices to sequester carbon. Water, Air and Soil Pollution 64:213-228.
Winjum, J. K., S. Brown and B. Schlamadinger. 1998. Forest harvests and wood products: sources and sinks of
atmospheric carbon dioxide. Forest Science 44:272-284.
-------
7. Vegetation 7-1
7. Vegetation Redistribution
Statement of the Problem
Global C02 emissions may generate two classes of ecological impacts at the
global scale. One involves the global carbon cycle and another involves the
Earth's biodiversity. Both are affected in large part by the potential redistribution
of vegetation on the Earth. Currently, the many different kinds of unmanaged
vegetation are adapted to today's climate; as climate changes, each kind of
vegetation must change as well, dying out in places the where climate becomes
too stressful, and prospering where climate becomes salubrious. As the Earth
warms from increasing atmospheric greenhouse gases, the redistribution of
vegetation can induce the terrestrial biosphere to become either a source of
additional C02 (quickening the warming) or a sink for C02 (reducing the
warming). Which course it will take is not known. For example, a warmer earth
should support more forests that contain high carbon densities, but the warmest
places on earth today support only sparsely-vegetated deserts. As vegetation
changes, so do the ecosystems on which populations of plants and animals
depend for their existence. Hence, biodiversity will also be impacted by
vegetation redistribution. The NHEERL research effort of the 1990's focused on
the carbon cycle implications of vegetation redistribution.
Approach
Estimating future vegetation redistribution was based on developing predictive
models. One group of models was designed to correlate the geography of
climate with the geography of vegetation types. Then the future distribution of
climate was used as a basis for redrawing the geography of the vegetation types
(including agriculture). Once the new distributions of vegetation types were
defined, the carbon they could store was calculated - assuming that their current
carbon densities would be supported in their future distributions.
A second group of models accounted mechanistically for processes which
determine the growth, shifting density, and carbon uptake of vegetation during
chronic climate change. These processes include the rapid dieback,
reproduction, and slow regrowth of forests - all processes which induce lags in
vegetation response to rapid climate change. Although these processes could
not be treated mechanistically in the correlative models described above, we did
approximate the process effects in the correlative models, using values
consistent with known biotic change rates.
Main Conclusions
The redistribution of global vegetation in response to climate and land use
change during the next century is likely to generate a several-decade long pulse
of carbon dioxide from the biosphere into the atmosphere. The result will
enhance the buildup of greenhouse gases resulting from anthropogenic
emissions.
-------
7. Vegetation 7-2
Critical to the modeling effort was developing precise data bases for climate and
vegetation (e.g., EPA/NOAA 1992,1993). Early work used life form classifications
(e.g., Sedjo and Solomon 1988; King and Neilson 1992). Later work used known climate
thresholds to assemble different plant functional types (PFTs) in each % X %
degree of latitude and longitude (Prentice etal. 1992). The presence of different
combinations of PFTs defined biomes (temperate deciduous forest, cold
grasslands, etc.). In addition to assessing vegetation redistribution impacts on
the carbon cycle (e.g., Solomon, etal. 1993,1996; Solomon 1996,1997), we also
assessed land use effects (Cramer and Solomon 1993, Leemans and Solomon 1993,
Solomon and Leemans 1997), rapid tree dieback, differential availability of seeds, and
slow regrowth of vegetation (Solomon and Kirilenko 1997, Kirilenko and Solomon 1998).
Primary conclusions were:
1) The capacity of the terrestrial biosphere to remove and store
atmospheric carbon should be greater under a warmer global climate.
2) The slow death and growth responses by vegetation would generate a
pulse of carbon from vegetation 15-20% as great as that from
anthropogenic emissions.
3) Increasing intensity of agriculture in higher latitudes would permanently
reduce the capacity of the earth to store carbon below its' current storage
capacity.
A second modeling approach used climate correlations (rather than climate
thresholds) to define the climate space occupied by U.S. vegetation types (Neilson
etal. 1992), and then applied a physiology model which calculated the uptake of
C02 by photosynthesis and emission of C02 by respiration in each vegetation
type (Neilson I993a, 1995). This approach used climate projections calculated by
global climate models to define new vegetation distributions. Then, based on the
new distributions of vegetation types, the projected balance of carbon uptake and
emission from vegetation was determined. Expanded to a global scale (Neilson
I993b, 1998, Neilson and Marks 1994), this approach could simulate the direct effects
of increasing C02 (a plant nutrient) on biomass storage. Applied to future climate
conditions using several climate scenarios, this research suggested, but did not
confirm, the potential presence of a multi-decade transient pulse of atmospheric
carbon (Neilson 1993b, 1998).
The modeling effort could not estimate the effects on carbon storage of slow
vegetation responses to rapid climate changes. Instead, carbon storage was
projected assuming that climate and vegetation distributions are stable. However,
"there is no indication that a stable climate will appear in the foreseeable future.
Indeed, the global change problem to be assessed involves rapidly changing
climate, not stable climate" (Solomon etal. 1996). Forest gap models were used to
estimate the time-related responses of vegetation to rapid climate change. These
models replicate the death, reproduction, growth, and maturity of trees, and the
development of forest ecosystems (Solomon and Bartlein 1992, Solomon and West 1993,
-------
7. Vegetation
7-3
Bugmann and Solomon 1995, 2000). Although assessment exercises with these
models (Solomon and Bartlein 1992, Bugmann etal. 2001) confirmed the potential for the
long-term carbon pulse that was described by the static correlative models, the
gap models have not yet been applied on the globally-comprehensive basis
needed to thoroughly evaluate the carbon pulse phenomenon.
Measured Global Vegetation Biomes
Map of measured global vegetation biomes, including land dominated by
agriculture, from various literature sources compiled and mapped by J. S. Olson,
et a/.., 1983 (from Solomon and Leemans, 1997, p. 141). Notice the effects of low
temperature limits to plant growth shown by the latitudinal bands of boreal
vegetation in the polar regions, and the dominance of low moisture limits to plant
growth (1) in temperate and regions, shown by the longitudinal bands of
agricultural and natural vegetation, and (2) in tropical regions shown by the
latitudinal presence of hot deserts along the subtropical convergence zone where
sinking air blocks frontal passage and thus precipitation. The finer-scale
complexity of the global biome distribution patterns is derived from the local and
regional variations in soils, topography, and land use.
| Depauperate Temp. Dec. Forest
Agricultural Land
\ Tropical Dry Forest Savanna
j Tropical Seasonal Forest
| Tropical Rain Forest
| Xeraphytic Wood/Shrub
Hot Desert
Warm Grass/Shrub
I Evergreen/Warm mixed Forest
I Temp. Deciduous Forest
Cool mixed Forest
Cold mixed Forest
I Cold Conifer Forest
Cool Grass/Shrub
| Southern Cool Decid. Forest
[ Cold Decid. Forest
| Taiga
Northern Taiga
I Wooded Tundra
[ Non-wooded Tundra
Semi Desert
Ice/Polar Desert
-------
7. Vegetation
7-4
Modeled Global Vegetation Biomes
Map of modeled global vegetation biomes, including land suitable for agriculture.
This map is defined entirely by known cardinal climate thresholds applied through
the BIOME model, with no reference to the actual vegetation present. Modeled
biomes are identified in the legend above (from Solomon and Leemans 1997, p. 141).
Comparing this map with the previous one, notice that the model maintains the
biome distribution patterns with regard to low temperature and low moisture
dominance in polar, temperate and tropical regions, as well as many of the finer-
scale biome distribution patterns derived from the local and regional variations in
soils, topography, and land use. The ability to use climate data as proxy
vegetation to reproduce the known patterns of biome distribution is critical to
subsequent efforts aimed at projecting maps of future vegetation and carbon
storage under climate warming scenarios.
Depauperate Temp. Dec. Forest
Agricultural Land
Tropical Dry Forest Savanna
Tropical Seasonal Forest
Tropical Rain Forest
Xerophytic Wood/Shrub
Hot Desert
Warm Grass/Shrub
Evergreen/Warm mixed Forest
Temp. Deciduous Forest
Cool mixed Forest
Cold mixed Forest
Cold Conifer Forest
Cool Grass/Shrub
Southern Cool Decid. Forest
Cold Decid Forest
Taiga
Northern Taiga
Wooded Tundra
Non-wooded Tundra
Semi Desert
Ice/Polar Desert
-------
7. Vegetation
7-5
Future Global Vegetation Biomes
Map of future global vegetation biomes, including land suitable for agriculture, under a
future climate at the time atmospheric CO2 concentrations double. The climate changes
used to drive the BIOME model are among the mildest simulated by general circulation
models of the atmosphere, that is, the global climate model (ECHAM-1 by the Max Plank
Institute, Hamburg; see Greco etal. 1994) is only moderately sensitive to greenhouse gas
concentrations.
Note the great increase in land suitable for agriculture toward polar areas, a feature
which follows from expected climate changes: all general circulation models of the
atmosphere (global climate models) project a greater increase in warming at the poles
than at the equator, a greater warming in winter than in summer, and a greater warming
at night than in daytime. As a result, the projected climate in high latitudes is expected to
increase greatly in days with temperatures constantly above freezing, and in the annual
growing season length. Indeed, polar growing seasons have already increased 12 to 18
days since 1980, as measured by satellites.
Note also that, compared with the previous map, this map shows areas of natural
vegetation in temperate areas dominated by dryland biomes, especially thorn shrub
vegetation, and boreal forests severely reduced as potential agriculture covers low
latitude growing areas, with little space to grow toward the higher latitudes.
Arable Land
Tropical Dry Forest Savanna
Tropical Seasonal Forest
Tropical Rain Forest
Xerophytic Wood/Shrub
Hot Desert
Warm Grass/Shrub
Evergreen/Warm mixed Forest
Temp. Deciduous Forest
Cool mixed Forest
Cold mixed Forest
Cold Conifer Forest
Cool Grass/Shrub
Southern Cold Dead Forest
Northern Cold Decid Forest
Southern Taiga
Northern Taiga
Wooded Tundra
Non-wooded Tundra
Semi Desert
Ice/Polar Desert
-------
7. Vegetation
7-6
The CO2 Pulse
Total carbon stored by the terrestrial biosphere in separate biomes and in total in
Pg (petagrams, 1015g). Carbon storage is simulated for 500 years into the future,
with a warming scenario from ECHAM-1, by the Max Plank Institute in Hamburg
(Greco etal. 1994), from year 0 to that from a doubling of atmospheric C02
concentrations at year 100. Minus values represent release of carbon from the
terrestrial biosphere to the atmosphere, positive values represent storage of
carbon into the terrestrial biosphere from the atmosphere (from an unpublished
version of the MOVE model (Kirilenko and Solomon 1998) which includes stochastic
rather than constant rates of tree mortality and growth).
80 -i
-60
SIMULATION YEARS
•BorFor TempFor TropFor ^—Tundra
•WarmDes ^—Grasslnd ^—TOTAL
The total biomass of the terrestrial biosphere declines markedly for the first 100+
years of this simulation, defining the multi-decadal pulse of carbon to the
atmosphere discussed in the text. Note that only grassland vegetation initially
increases in biomass, as it replaces the woody vegetation types which dieback
during early warming and which only gradually regrow to out compete the
herbaceous vegetation.
-------
7. Vegetation 7-7
References Cited
Bugmann, H.K.M. and A.M. Solomon. 1995. The use of a European forest model in North
America: A study of ecosystem response to climate gradients. J. Biogeography 22:477-484.
Bugmann, H.K.M. and A.M. Solomon. 2000. Explaining forest composition and biomass across
multiple biogeographical regions. Ecological Applications 10:95-114.
Bugmann, H. K. M., S. D. Wullschleger, D. T. Price, K. Ogle, D. F. Clark, and A. M. Solomon.
2001. Comparing the performance of forest gap models in North America. Climatic Change
51:349-388.
Cramer, W. P. and A. M. Solomon. 1993. Climatic classification and future distribution of global
agricultural land. Climate Research 3:97-110.
EPA/NOAA. 1992. Global Change Database: Global Ecosystems Database, CD Disk A., Nat.
Geophys. Data Center, Boulder CO.
EPA/NOAA. 1993. Global Change Database: Global Ecosystems Database, CD Disk B., Nat.
Geophys. Data Center, Boulder CO.
Greco, S., R. H. Moss, D. Viner, and R. Jenne, 1994. Climate Scenarios and Socioeconomic
Projections for IPCC WG II Assessment. Material assembled for Lead Authors by IPCC WG II
TSU. Washington D.C.
King, G. A. and R. P. Neilson, 1992. The transient response of vegetation to climate change: a
potential source of CO2 to the atmosphere. Water, Air, and Soil Pollution 64:365-383.
Kirilenko, A. P. and A. M. Solomon. 1998. Modeling dynamic vegetation response to rapid
climate change using bioclimatic classification. Climatic Change 38:15-49.
Leemans, R. and A. M. Solomon. 1993. The potential change in yield and distribution of the
earth's crops under a warmed climate. Climate Research 3:79-96.
Neilson, R. P., 1993a. Transient ecotone response to climatic change: some conceptual and
modeling approaches. Ecological Applications 3:385-395.
Neilson, R. P. 1993b. Vegetation redistribution: A possible biosphere source of CO2 during
climatic change. Air Water and Soil Pollution 70:659-673.
Neilson, Ronald P. 1995. A model for predicting continental-scale vegetation distribution and
water balance. Ecological Applications 5:362-385.
Neilson, R. P., 1998. Simulated changes in vegetation distribution under global warming. Annex
C, pp. 439-456 IN Watson, R. T., M. C. Zinyowera, R. H. Moss and D. J. Dokken, eds., The
Regional Impacts of Climate Change. Cambridge Univ. Press, NY.
Neilson, R. P., G. A. King and G. Koerper, 1992. Toward a rule-based biome model. Landscape
Ecology 7:27-43.
Neilson, R. P. and D. Marks. 1994. A global perspective of regional vegetation and hydrological
sensitivities from climatic change. J. Veg. Sci. 5:715-730.
Olson, J. S., J. A. Watts, and L. J. Allison. 1983. Carbon in Live Vegetation of Major World
Ecosystems. ORNL/TM-5862, Oak Ridge National Laboratory, Oak Ridge TN.
Prentice, I. C., W. Cramer, S. P. Harrison, R. Leemans, R. A. Monserud, and A. M. Solomon.
1992. A global biome model based on plant physiology and dominance, soil properties and
climate. Journal of Biogeography 19:117-134.
Sedjo, R. A. and A. M. Solomon, 1989. Climate and forests, pp. 105-119 IN Rosenberg, N. J.,
W. E. Easterling, P. R. Crosson, and J. Darmstadter, Eds., Greenhouse Warming: Abatement
and Adaptation. Resources for the Future, Washington, D.C.
-------
7. Vegetation 7-8
Solomon, A.M. 1996. Potential responses of global forest growing stocks to changing climate,
land use and wood consumption. Commonw. For. Rev. 75:65-75.
Solomon, A.M. 1997. Natural migration rates of trees: Global terrestrial carbon cycle
implications. Pp. 455-468 IN Huntley, B., W.P. Cramer, A.V. Morgan, H.C. Prentice and J.R.M.
Allen. Past and future rapid environmental changes: The spatial and evolutionary responses of
terrestrial biota. Springer-Verlag, NY
Solomon, A. M. and P. J. Bartlein. 1992. Past and future climate change: Response by mixed
deciduous-coniferous forest ecosystems in northern Michigan. Canadian Journal of Forest
Research 22:1727-1738.
Solomon, A. M. and A. P. Kirilenko. 1997. Climate change and terrestrial biomass: What if trees
do not migrate? Global Ecol. and Biogeogr. Let. 6:139-148.
Solomon, A.M. and R. Leemans. 1997. Boreal forest carbon stocks and wood supply: Past,
present and future responses to changing climate, agriculture and species availability. Journal of
Agricultural and Forest Meteorology 84:137-151.
Solomon, A. M. and D. C. West. 1993. Evaluation of stand growth models for predicting
afforestation success during climatic warming at the northern limit of forests, p. 167-188 IN R.
Wheelon, ed. Forest Development in Cold Regions. Proceedings, NATO Advanced Research
Workshop. Plenum Publ. Corp., NY.
Solomon, A. M., I. C. Prentice, R. Leemans and W. P. Cramer. 1993. The interaction of climate
and land use in future terrestrial carbon storage and release. Water, Air, and Soil Pollution
70:595-614.
Solomon, A.M., N.H. Ravindranath, R.B. Stewart, S. Nilsson and M. Weber. 1996. Wood
production under changing climate and land use. Chapter 15, pp. 487-510. IN Climate Change
1995: Impacts, Adaptations and Mitigation of Climate Change. Working Group II, Second
Assessment Report, Intergovernmental Panel on Climate Change (IPCC), Cambridge University
Press, Cambridge UK.
-------
8. CO2 & Temperature Effects 8-1
8. Effects of Elevated Atmospheric Carbon Dioxide
Concentration and Temperature on Forests
Statement of the Problem
Concentrations of carbon dioxide (C02) and other trace gases have been
increasing in the atmosphere due to human activity. By the 1980s, accumulating
evidence suggested that increasing levels of these gases could produce higher
global temperatures and changes in precipitation patterns. More information on
how the biosphere controls atmospheric C02 was needed to understand the
Earth's carbon cycle. Foremost, an understanding of source-sink relations
between the atmosphere and the various components of the biosphere was
needed. Consequently, research was undertaken to delineate the relations
between atmospheric C02 concentrations, changes in global climate drivers, and
responses of the soil-plant-atmosphere continuum (EPA 1993). The science
questions governing the research were:
What are the effects of elevated CCb and climate change on the growth
and productivity of forest trees?
elevated C02 and climate change alter the sequestration/exchange of
carbon in the soil-plant-atmosphere continuum?
• What is the magnitude of these elevated C02 and climate change impacts
and will they be widely distributed?
Approach
Research was conducted to investigate ecosystem responses to elevated
atmospheric C02 and associated increases in atmospheric temperature over
several years. NHEERL scientists built a state-of-the-science, sun-lit, controlled-
environment chamber facility in which climatic and edaphic factors could be
controlled and/or monitored during the multi-season exposure period (Tingey et al.
1996). A tree forest ecosystem was reconstructed in the chambers using Douglas-
fir seedlings supported by one of its widely represented soil types (Rygiewicz et al.
2000). Climatic treatments were applied based on the natural, temporal variations
in ambient climatic conditions found at the facility site, thus subjecting the
reconstructed ecosystem to a realistic climatic profile (Tingey et al. 1996).
Experimental treatments included increased levels of atmospheric CC^and
elevated temperature (Olszyk and Tingey 1996).
Main Conclusions
Generally, the effects of increasing the atmospheric C02 concentration on the
reconstructed Douglas-fir-soil ecosystem appear to have been limited by low
nitrogen availability in the soil - a condition common in forest soils of the Pacific
Northwest. This result was supported by the Maine Biological Laboratory's
-------
8. CO2 & Temperature Effects 8-2
General Ecosystem Model (GEM), used after completing the climate change
experiment, to project longer-term and broader-scale consequences of climate
change in Pacific Northwest Douglas-fir forests. Application of GEM to various
sites in the western Cascades suggests that soil nitrogen is a primary constraint
on changes in ecosystem carbon storage (McKane etal. 1997). For the nitrogen-
poor montane site where the soil for the chamber experiment was obtained, the
model predicts that total ecosystem carbon storage will increase by less than
10% during the next 100 years in response to projected increases in atmospheric
C02 and temperature. In contrast, GEM predicts that carbon storage will increase
by over 25% during the same period for a nitrogen-rich site in the western
Cascades foothills.
Even though elevated atmospheric CCb increased photosynthetic rates (Lewis et
al. 1999, Lewis et a\. 2001), and while chlorophyll and carotenoid concentrations in
the needles decreased under elevated C02 (Ormrod et al. 1999), the additional
carbon acquired was not allocated to produce seedlings of greater biomass
(oiszyk et al. 2003). Rather, it appears that the carbon was allocated to soil
organisms which convert stored, unavailable forms of nutrients into available
forms (Lin et al. 1999, Lin et al. 2001). These available forms can then be acquired by
diverse and stable mycorrhizal fungi resident on the ephemeral, nutrient-
absorbing fine roots (Rygiewicz et al. 2000, Hobbie et al. 2001).
While total carbon storage in the soil increased during the experiment, due to
seedling growth and decomposition processes in the soil and litter layer, the
amount of total stored carbon was not different among the climatic treatments.
However, stable isotopic data suggest that a variable allocation of carbon into
soil organic matter (SOM) of different qualities may have occurred, thus altering
the long-term storage potential of the soil for carbon. In a related project on
ponderosa pine, the effect of nitrogen to alter the seedlings' responses to
atmospheric C02 concentration was clearly evident (Johnson et al. 2000), and
reinforced the results found in the chamber study done on Douglas-fir. Taken
collectively, these results indicate the overriding influence of the low nitrogen
found in Pacific Northwest forests.
Projecting to larger scales, the responses of forest ecosystems to elevated C02
may be highly variable temporally and globally. In particular, the responses
appear highly dependent on the quantity and availability of nutrient resources,
and the capacity of nutrient acquisition processes relative to the increased
amount of carbon available in the atmosphere. As the Douglas-fir study was run
for only four growing seasons, it is uncertain if the observed responses to
elevated C02 were transient, and eventually would change as ecosystem
compartments continued to adjust to the altered ratios of available carbon to
available nutrients.
Elevated temperature had a greater, and negative, impact on the seedlings than
did the elevated C02 treatments. Elevated temperature directly and negatively
affected the development and morphology of the seedlings. Seedlings grown
-------
8. CO2 & Temperature Effects 8-3
under elevated temperatures had greater numbers of aborted and malformed
buds, and abnormal needle primordial tissue compared with seedlings in the
ambient temperature treatments (Apple etal. 1998, Apple etal. 2000). In addition, the
seedlings grown under the higher temperatures were shorter and more "bush-
like" in morphology, thus hindering their ability to gain height (Olszyk etal. I998a,
oiszykef a/. I998b). Elevated temperature delayed needle hardening in the fall,
slowed dehardening in the spring and reduced the maximum hardiness;
rendering the trees less resistant to low temperatures (Guakef a/. 1998).
Climate change will affect forested ecosystems differentially. While elevated
temperature will most likely affect the growth of plant species directly, the effects
on ecosystem structure and functioning may be more subtle to discern, but no
less significant. Elevated temperature could lead to the replacement of sensitive
species by more heat tolerant species. In the Pacific Northwest, the predominant
lumber species, Douglas-fir, could experience abnormal growth patterns. But as
Douglas-fir is a genetically diverse species, adaptation, either natural or
managed, is likely. However, the cost to timber production is unknown.
Ecosystem effects of increasing levels of atmospheric C02 will depend on the
nutrient status of specific forests. Increased forest production will occur where
soils contain adequate nitrogen. In areas where nitrogen is limiting, elevated C02
levels will not increase the growth of trees - even though photosynthesis may
increase. Without sufficient nitrogen, the trees cannot use the additional C02 for
growth. The additional carbon is used by soil organisms and respired to the
atmosphere (Rygiewicz and Andersen 1994). In addition to contributing to C02
buildup in the atmosphere such changes in the soil foodweb, which controls
nutrient availability for plants, could have long-term effects on ecosystem
functioning.
-------
8. CO2 & Temperature Effects
8-4
Experimental Approach to Study Seedling and Ecosystem Processes
A 2 X 2 factorial treatment design was
used: [ambient CO2 and ambient +
200 ppm CO2 (179 ppm achieved),
ambient temperature, and ambient + 4
°C (3.8 °C achieved)]. Each of the
four climatic conditions was replicated
three times, which resulted in a total of
12 chambers being used for the
pynprimpnt
SPAR (Soil-Plant Atmosphere Research) chambers (1
x 2 m footprint) were used to simulate natural
seasonal and diurnal changes in atmospheric [CO2],
air and soil temperatures, vapor pressure deficit
(VPD), and soil moisture. Fourteen, two-year-old
Douglas-fir seedlings were planted in each chamber in
a natural, widely-represented, Cascade Mountains,
high-elevation (1220 m) soil. The seedlings originated
from open-pollinated seeds harvested from 5 low-
elevation (300 to 460 m) seed zones in the Cascade
and Coastal Mountain Ranges near Corvallis. Total N
in the soil was < 0.1% (w/w), and NCV and NH4+ in
soil solution were below detection limits (0.04 and
0.10 mg I"1, respectively). Six cm of forest floor were
placed on top of the soil. Climatic treatments were
imposed for 4.5 growing seasons.
An Integrated Sampling Approach Was Designed to Track Carbon, Water and
Nutrients through the Reconstructed Ecosystem
TASK1
Shoot Carbon and
Water Fluxes
TASK 3
System Nutrients
• Plant Nutrients
Soil Nutrients
TASK 6
Root Growth and
Phenology
TASK 2
Shoot Growth and
Phenology
TASK 4
System Water
Plant Water
Soil Water
TASKS
Soil Organic
Matter
The project was
highly-integrated
across the above-
and below-ground
portions of the
reconstructed
ecosystem, and
organized around
eight tasks focused
on individual seedling
and ecosystem state
variables and
processes.
Ecosystem budgets
for carbon, water and
nutrients, therefore,
could be calculated.
Collecting samples
and taking
measurements were
closely linked across
above- and below-
ground phenological
events. An analysis
was conducted as the
project was
-------
8. CO2 & Temperature Effects
8-5
Elevated CO2 Increased Photosynthesis but not Growth
<\mb. Temp., Amb. CO2 ^| Amb. CO2, + 4°C
<\mb. Temp., + 200 ppm + 4°C, + 200 ppm
Maximum Average
PPFD Co nditions
C loudy
15
DC "
8
—
O
£
1
O
1
Q.
Amb, Temp.
+4°C
Amb. CO2
+ 200 ppm
10 15 20 25 30
Temperature (°C)
Greater instantaneous photosynthetic rates (left panel) were observed under elevated CO2
and temperature in the spring and winter. Some acclimation of photosynthetic rates to
elevated CO2 was evident as the exposure to climatic treatments progressed (data not
shown). Even so, by the third and fourth growing seasons, elevated CO2 increased net
photosynthesis by an average of 21% across the two temperature treatments. The additional
carbon acquired under elevated CO2 was not released through increased "dark" respiration
(respiration not associated with the process of photosynthesis).
The increased carbon uptake under elevated CO2 and elevated temperature did not increase
the final size of the seedlings. Moreover, elevated CO2 had no other significant effects on
whole seedling or individual seedling component biomass, % biomass allocation, or leaf area
(not all data are shown) Other sinks for the additional carbon acquired are the continual
production, death and decomposition of the ephemeral, nutrient-absorbing fine roots; the
various organisms of the soil food web (both their biomass and respiration); and the soil
organic matter (SOM). PPFD is Photosynthetic Photon Flux Density, expressed as urnol
photons m"2 s"1. (Lewis etal. 1999).
Under elevated temperature, compared with the ambient condition, shifts occurred only in the
amounts of carbon allocated to needles and buds (Olszyk etal. 2003). Allocation of carbon
related to the production, death and decomposition of the ephemeral, nutrient-absorbing, fine
roots can not be determined from the final biomass of the seedlings as these roots were
produced and decayed during the exposure period. The retrospective analysis of the
allocation of carbon to produce these roots throughout the exposure is ongoing.
-------
8. CO2 & Temperature Effects
8-6
Elevated Temperature Affected Needle and Bud Growth
Douglas-fir buds (left panel)
showed several signs of
damage due to elevated
temperature: (A) Dissected
normal bud from the ambient
climatic treatment; (B)
Dissected abnormal bud from
elevated temperature
treatment with bud-scale-like
needle primordial (arrow), and
(C) convoluted bud scales
(arrows); (D) Exterior of normal
bud from ambient conditions;
(E) Exterior of resetted bud
from elevated temperature
treatment; (F) Normal buds
from ambient conditions; (G) to
(I) all are elevated temperature
treatment showing - (G)
resetted abnormal buds, (H) a
shoot with two small buds and
reduced needles, and (I) a bud
with reduced needles and
elongated stalk originating from
tree truck. Scale = 1 mm.
Source: Apple etal. 1998.
Under elevated temperature, a greater percentage of leader and branch buds opened early in the
growing season (lower left panel). However, by the end of bud burst, a smaller total percentage of
buds had opened under the higher temperatures. Needles produced under elevated temperature
conditions were less able to withstand the colder temperature of winter (lower right panel).
Indicated is the freezing temperatures at which 50% of the needles displayed visible signs of
tissue damage (Lt50 °C). Source: Guak etal. 1998.
-------
8. CO2 & Temperature Effects
8-7
Seedling Size Was Negatively Affected by Elevated Temperature
1400
1200-
1000-
'E 800-
— 600-
I—
g 400-
£ 200^1
0-
-200-
-400-
Jun 1, !
Height
30-
25.
E"
§20-
Y.
U
ACAT n ECAT Change
ACET Change o ECET Change
nmnm n nqmnq^nnn n nini^
Jun 1, 94
Jun 1, 95
Jun 1, 96
Jun 1, 97
Stem Diameter
..X
*
ACAT
ACET Change
o ECAT Change
n ECET Change
o o
i •
Legend: ACAT = ambient CO2, ambient temp; ECAT = elevated CO2, ambient temp.; ACET = ambient CO2; elevated temp.;
ECET = elevated CO2, elevated temp.
Elevated temperature resulted in shorter Douglas-fir seedlings, beginning during the second
growing season. The left graph indicates the increase in height over time for seedlings grown
under the ambient CC>2 and temperature levels (ACAT). The other three treatments are
shown as changes relative to the ACAT treatment. For example the ACET Change = ACET-
ACAT. Elevated CC>2 by itself had no effect on plant height (ECET Change). In contrast,
neither elevated temperature nor elevated CC>2 affected stem diameters. The right graph
indicates annual increases in stem diameter for the ACAT seedlings and the lack of any
relative change in stem diameter for seedlings grown under any of the other elevated
temperature or elevated CC>2treatments. Modified from: Olszyk et al. 1998a.
Elevated CO2 and Temperature Altered Fine Root Distribution but not
Production and Turnover
Cumulative Annual Fine Root Production
ACAT ---ECAT ACET ECET
i-
Cumulative Annual Fine Root Turnover
—ACAT - — ECAT AC£T CCLT
Fine roots play a key in the acquisition of
water and nutrients needed to sustain
growth. The growth of fine roots is
coordinated with shoot growth so that the
plant has sufficient resources.
The effects of elevated C02 and
temperature on fine production and
turnover were determined over a 4-year
period. Elevated C02 and temperature
altered fine root distribution; there were
more fine roots deeper in the soil. There
were no C02 effects on annual fine root
production or turnover. During the first 2
years, elevated temperature (at ambient
C02) increased fine root production, but
there were no differences in the latter part
of the experiment. Limited N availability
likely minimized C02 response
belowground as it did aboveground.
-------
8. CO2 & Temperature Effects
8-8
The Rhizosphere Responded to Elevated Atmospheric CO2
A. Tot»l toil CO, i inn.
C. Litter decomposition
: 100
Elevated Elevated Elevated CO2
C02 temperature s Temperature
Elevated Elevated Elevated C02
CO2 temperature & Temperature
Percent increase or decrease in the total flux of CO2 released from the
soil (A), and from its component sources (B, C, D) relative to respective
CO2 fluxes in the ambient climatic treatment,.
The amounts of carbon
forming the total soil CO2
efflux were mathematically
partitioned into their source
compartments within the soil.
Since the atmospheric carbon
delivered to the seedlings was
depleted in 13C, it served as a
tracer to analyze soil carbon
dynamics. The dominant
source of the soil CO2 efflux in
the soil-Douglas-fir ecosystem
was the decomposition of the
litter, followed by rhizosphere
respiration (= root respiration
+ respiration of root-
associated soil biota), and
then from the oxidation of soil
organic matter (SOM) (data
not shown). Elevated CO2
stimulated total soil respiration
(Graph A).
Rhizosphere respiration was stimulated by elevated CO2 and less so by temperature (Graph B).
In contrast, litter decomposition was stimulated mostly by temperature (Graph C). The SOM
response was highly variable (Graph D): from a decrease in oxidation under elevated CO2, to an
increased oxidation under elevated temperature; note that elevated CO2 in the double elevated
treatment countered the oxidation found in the elevated-temperature-only treatment. Differences
in responses between 1994 and 1995 are attributed to the physical disruption done to the soil
when it was transported from the Cascade Mountains to the chambers. The likelihood that the
increased rhizosphere respiration was due to a transient, increased standing crop of the
ephemeral, fine roots is still being analyzed.
-------
8. CO2 & Temperature Effects 8-9
Carbon Delivered to Soil Foodweb to Explore Ecosystem for Nutrients
NUVBERS OF IWCORRHZAL ROOT TIPS PER M_ SQL
—SCAT -"-ACE! -»-ECET
NUVBEFS OF DIFFERENT MORPHOTYPES
-o-ACAT —-ECAT -°-ACET -»-ECET
S04 R34 S85 R5 S86 R6 S97
S94 F94 S95 F95 S96 R96 S97
T T
Legend: ACAT = ambient CO2, ambient temp; ECAT = elevated CO2, ambient temp.; ACET = ambient CO2; elevated temp.;
ECET = elevated CO2, elevated temp.
The increased soil CO2 efflux attributed to rhizosphere respiration (= root respiration +
respiration of root-associated soil biota) (previous sidebar) likely is due to increased standing
crop of the ephemeral, fine roots and their decomposition, and/or the standing biomass, activity
and decomposition of soil fungi. Coniferous forest ecosystems rely on free-living and symbiotic
fungi (attached to the fine roots) to mobilize nutrients stored in the forest floor and soil, and to
transport the mobilized nutrients to, and into, the plants to balance the carbon acquired
aboveground. All low-nutrient terrestrial ecosystems increase their dependence on these fungi
compared to higher nutrient conditions. The Douglas-fir seedlings formed high concentrations
of mycorrhizal root tips in the low-nutrient soil (left graph), and exhibited a high degree of root
colonization (nearly 100% of the root tips that developed were colonized, data not shown).
The fungal community formed on the roots was highly-diverse and its structure was resistant to
the climatic treatments (right graph). However, the most extensive portion of the symbiotic
fungal biomass is the portion living at distance from the roots, and which explores the soil for
nutrients, delivering them to the tree. Through the use of direct counting procedures and
measuring the amounts of stable isotopes delivered into the soil foodweb, we anticipate
identifying to which trophic structure(s) in the soil ecosystem the additional carbon acquired
under elevated CO2 was allocated, and then subsequently deposited as soil organic matter
(SOM).
-------
8. CO2 & Temperature Effects 8-10
Soil Organic Matter May Be Depository for the Acquired Carbon
25
20-
O
=5
^15-
E
0
o>
0-
ACAT ACET ECAT ECET
Treatment
The amount of carbon stored in soil
as organic matter (SOM) increased
during the exposure, predictably as
one might expect because of plant
growth. However, none of the climatic
treatments affected the total amount
of carbon stored as SOM (graph at
left). Soil 13C data suggest that SOM
levels actually may have increased
under elevated CO2. As the total
amount of SOM may not have been
altered by the climatic treatments, the
isotopic data suggest that certain
quality fractions of SOM may have
been differentially affected by the
treatments. Thus the large total
amount of SOM may be masking the
more subtle responses in the
individual quality fractions. Ultimately,
the quality of SOM that is formed
determines long-term storage of
carbon in, and productivity of, forested
ecosystems. SOM from the
experiment has been separated into
its quality fractions, and stable
isotopic analyses are underway to
address this aspect of the fate of the
additionally-acquired carbon.
-------
8. CO2 & Temperature Effects
8-11
Soil Nitrogen Availability Constrained Carbon Storage in Response to
Elevated COa and Temperature
We used the General Ecosystem Model (GEM), a process-based model of terrestrial
ecosystem biogeochemistry, to project longer-term and broader-scale consequences of
increases in atmospheric CO2 and temperature in Pacific Northwest Douglas-fir forests.
Foothills Site
Montane Site
Elevation (m)
Total Soil Nitrogen (Mg/ha)
Mean Annual Temperature (°C)
Mean Annual Soil Moisture (%)
with Global Change (+26%) ,-'
with Global Change (+10%)
Pacific
Ocean
o
1995 2015 2035 2055 2075 2095
Year
1995 2015 2035 2055 2075 2095
Year
GEM was used to predict and analyze the effects of projected changes in CO2, temperature
& soil moisture on ecosystem carbon storage at the Foothills and Montane mature forest
sites. The model was run with and without the projected changes in CO2, temperature &
soil moisture. All simulations started in 1995 with post-harvest conditions (90% of tree
biomass removed).
Results illustrate that elevated CO2 increases plant growth and net ecosystem C storage
only when there are sufficient supplies of soil nitrogen as at the Foothills Site. A sensitivity
analysis showed that CO2 was much more important than temperature in increasing
ecosystem C storage, and that elevated CO2 increased storage of C in plants more than in
soils.
-------
8. CO2 & Temperature Effects 8-12
References Cited
Apple, M.E., M.S. Lucash, D.M. Olszyk and D.T. Tingey. 1998. Morphogensis of Douglas-fir buds
is altered at elevated temperature but not at elevated CO2. Environ. Exp. Bot. 40:159-172.
Apple, M.E., D.M. Olszyk, DP. Ormrod, J. Lewis, D. Southworth and D.T. Tingey. 2000.
Morphology and stomatal function of Douglas fir needles exposed to climate change: Elevated
CO2 and temperature. Int. J. Plant Sci. 161:127-132.
EPA. 1993. Research Plan: Effects of elevated CO2 and climate change on forest trees.
Environmental Research Laboratory - Corvallis.
Guak, S., D.M. Olszyk, L.H. Fuchigami and D.T. Tingey. 1998. Effects of elevated CO2 and
temperature on cold hardiness and spring bud burst and growth in Douglas-fir (Pseudotsuga
menziesii). Tree Physiol. 18:671-679.
Hobble, E.A., D.M. Olszyk, P.T. Rygiewicz, D.T. Tingey and M.G. Johnson. 2001. Foliar nitrogen
concentrations and natural abundance of 15N suggest nitrogen allocation patterns of Douglas-fir
and mycorrhizal fungi during development in elevated carbon dioxide concentration and
temperature. Tree Physiol. 21:1113-1122.
Johnson, D.W., R.B. Thomas, K.L. Griffin, D.T. Tissue, J.T. Ball, B.R. Strain and R.F. Walker.
1998. Effects of carbon dioxide and nitrogen on growth and nitrogen uptake in ponderosa and
loblolly pine. J. Environ. Qual. 27:414-425.
Johnson, M.G., D.L. Phillips, D.T. Tingey and M.J. Storm. 2000. Effects of elevated CO2, N-
fertilization, and season on survival of ponderosa pine fine roots. Can. J. For. Res. 30:220-228.
Lewis, J.D., D.M. Olszyk and D.T. Tingey. 1999. Seasonal patterns of photosynthetic light
response in Douglas-fir seedlings subjected to elevated atmospheric CO2 and temperature. Tree
Physiol. 19:243-252.
Lewis, J.D., M. Lucash, D. Olszyk and D.T. Tingey. 2001. Seasonal patterns of photosynthesis in
Douglas fir seedlings during the third and fourth year of exposure to elevated CO2 and
temperature. Plant, Cell Environ. 24:539-548.
Lin, G., J.R. Ehleringer, P.T. Rygiewicz, M.G. Johnson and D.T. Tingey. 1999. Elevated CO2 and
temperature impacts on different components of soil CO2 efflux in Doug las-fir terracosms. Global
Change Biology 5:157-168.
Lin, G., P.T. Rygiewicz, J.R. Ehleringer, M.G. Johnson and D.T. Tingey. 2001. Time-dependent
responses of soil CO2 efflux to elevated atmospheric [CO2] and temperature treatments in
experimental forest mesocosms. Plant and Soil. 229:259-270.
McKane, R.B., D. Tingey, P.A. Beedlow, P.T. Rygiewicz, M.G. Johnson, J.D. Lewis. 1997. Spatial
and temporal scaling of CO2 and temperature effects on Pacific Northwest forest ecosystems.
Amer. Assoc. Adv. Science Pacific Div. Abstracts 16(1):56.
Olszyk, D.M., M.G. Johnson, D. Tingey, P.T. Rygiewicz, C. Wise, E. VanEss, A. Bensen and M.
Storm. 2003. Whole seed biomass allocation, leaf area, and tissue chemistry for Douglas-fir
exposed to elevated CO2 and temperature for 4 years.
-------
8. CO2 & Temperature Effects 8-13
Olszyk, D.M and D.T. Tingey. 1996. Environmental modification and shoot growth in a closed
ecosystem to evaluate long-term responses of tree seedlings to stress. Acta. Hort. 440:129-134.
Olszyk, D., C. Wise, E. VanEss and D. Tingey. 1998a. Elevated temperature but not elevated
CO2 affects long-term patterns of stem diameter and height of Douglas-fir seedlings. Can. J. For.
Res. 28:1046-1054.
Olszyk, D., C. Wise, E. VanEss, M. Apple and D. Tingey. 1998b. Phenology and growth of
shoots, needles, and buds of Douglas-fir seedlings with elevated CO2 and (or) temperature. Can.
J. Bot. 76:1991-2001.
Ormrod, DP., V.M. Lesser, D.M. Olszyk and D.T. Tingey. 1999. Elevated temperature and
carbon dioxide affect chlorophylls and carotenoids in Douglas-fir seedlings. Int. J. Plant Sci.
160:529-534.
Rygiewicz, P.T. and C.P. Andersen. 1994. Mycorrhizae alter quality and quantity of carbon
allocated belowground. Nature 369:58-60.
Rygiewicz, P.T., K.J. Martin and A.R. Tuininga. 2000. Morphotype community structure of
ectomycorrhizas on Douglas-fir (Pseudotsuga menziesii Mirb. Franco) seedlings grown under
elevated atmospheric CO2 and temperature. Oecologia 124:299-308.
Tingey, D.T., B.D. McVeety, R. Waschmann, M.G. Johnson, D.L. Phillips, P.T. Rygiewicz and
D.M. Olszyk. 1996. A versatile sun-lit controlled-environment facility for studying plant and soil
processes. J. Environ. Quality 25:614-625.
-------
9. O3 & CO2 9-1
9. Interactive Effects of Oa and CO2 on the Ponderosa
Pine Plant/Litter/Soil System
Statement of the Problem
Carbon dioxide is required by plants to grow and is a major greenhouse gas
contributing to global climate change. Tropospheric ozone (Os) is the major
phytotoxic air pollutant in the U.S. which adversely impacts crops and forests.
While much is known about the effects of Os or C02 alone, there has been little
research on the potential interactive effects of these gases on terrestrial
ecosystems, even though they co-occur. Most of the research has focused on
the response of individual species rather than at the ecosystem level. There is a
growing interest in Os x C02 combinations fueled by concerns regarding potential
effects on vegetation from increases in regional Os levels. These increases
occur concurrently with an increased global C02 concentration.
Approach
Therefore, we carried out an in-depth study to address three general hypotheses
regarding the effects of Os and C02 on C, N, and H20 cycling through
ecosystems (Olszykefa/. 1997):
1) Elevated Os decreases C, N and H20 cycling rates.
2) Elevated C02 increases C, N, and decreases H20 cycling rates.
3) Elevated C02 eliminates negative effects of Os on C and N cycling rates
and has an additive negative effect on H20 cycling rates.
Our hypotheses were tested using experimental data and simulation models to
evaluate C, N, and H20 cycles (Olszykef a/. 2001). A reconstructed ponderosa pine
soil/tree seedling ecosystem was used, as this is system widespread in the
western U.S., and is known to be affected by both increasing C02 and Os. The
experiment was conducted in sunlit, controlled environment chamber facility (see
sidebar in previous section) to examine above- and belowground responses.
These chambers allowed for precise monitoring and control of climatic and
edaphic—soil—conditions and for calculation of whole system C02 and H20
balances (Tingey etal. 1996, Olszyk and Tingey 1996). The experimental design was a
2x2 factorial with 2 levels of C02, 2 levels of 63 and three replicate chambers
per treatment. Carbon dioxide was an elevated level of +280 ppm above ambient
reflecting an increase in greenhouse gases vs. the ambient concentration.
Ozone was at a high level representative of regional oxidant pollution vs. a low
level which is representative of a more pristine area. Research tasks measured:
i) system C02, 03 and H20 gas exchange; ii) plant phenology, allometry and
carbon allocation; iii) litter and soil/rhizosphere microbiological community
structure and function; iv) litter and soil chemical and physical properties; and v)
system C, N and H20 budgets, pools and fluxes. The modeling research used
-------
9. O3&CO2 6/17/04 9-2
the Marine Biological Laboratory's General Ecosystem Model (GEM) (Rastetteref
a/. 1991) to evaluate for system scale C and N cycling, and the process-based
whole-tree growth model TREGRO (Tingey etal. 2001), to study the potential
impact of increased Os and C02 on photosynthesis, respiration, carbon
accumulation, and carbon allocation.
Main Conclusions
Elevated C02 increased the photosynthetic C uptake by the seedlings beginning
early in the study (Olszyk etal. 2001) and persisting to the end (Olszyk etal. 2002)
(sidebar). The increase in photosynthesis was associated with an increase in
water use efficiency (the ratio of CC^ taken up to H20 loss by transpiration). The
increased C uptake appeared to stimulate plant growth as elevated C02
increased stem diameters (sidebar). This C02 induced-increase in stem diameter
was especially noticeable early during the study. Over time, the stimulation in
stem diameter leveled off, possibly due to growth-limiting factors such as a low
soil-N fertility level. Elevated C02 also affected N cycling in the system as
indicated by lower leaf N concentrations with elevated C02 (Olszyk etal. 2001).
In contrast to C02, Os alone had little effect on the plants, and those responses
that did occur were affected by the variable Os concentrations among the three
years. There were suggestions of significant C02 x Os interactions for some
parameters where the response to the combined pollutants was different from
that expected based on the responses to the individual pollutants. For example,
in late August 2000 photosynthesis decreased with high Os for seedlings at
ambient C02 but increased with high Os for seedlings at elevated C02. There
also was a significant C02 x Os interaction on plant growth early in the study, as
stem diameters were greater with elevated C02 and low Os compared with
elevated C02 and high 03 (Olszyk et al. 2001).
When the data have been completely evaluated from this study, the results will
provide unique information on the responses of ecosystem functions due to the
interactions of C02 and 03, as well as responses to the individual gases.
-------
9. O3 & CO2
9-3
Effects of Elevated CO2 and O3 on Net Photosynthesis in Ponderosa pine
Elevated CO2 increased photosynthetic rates over much of the experiment as shown by
the higher values for seedlings grown under elevated
elevated CO2 and high O3 (ECHO) vs. seedlings
low 03 (ACLO) or high O3 (ACHO. The "*" and "
CO2 at either low
03 (ECLO) or
grown under ambient CO2 and either
o" symbols in the "C" row at the top of
the figure indicate those periods during which there was a significant CO2 effect on
photosynthesis based on analysis of variance at
respectively. High O3 had only a minor effect on
alone effects for only three periods as shown by
the p<0.05 and p<0.10
levels,
photosynthesis, with significant O3
the symbols in the "O"
and significant CO2 x O3 interactions for only 4 periods
row at the top,
in the "CxO" row at the top. The
symbols are averages "SE (bars) for 3 replicate chambers except for 2 replicate
chambers for the treatment. The dashed
lines at base
of figure are approximate dates
of O3 exposures. Source: Olszyk etal. 2002.
• ACLO •
20.1
.
-
.
,_, 16-
c-j
'J 12-
o
E
,2,
VI
• — n
£ °~
_C
-I— '
&
W
£ 4-
0
JZ
D_
n
•
0
I i
° I v Ji
o (D m r Yi
4- []j * • ^
* s t •+ '
• » I i
• a <
I
ACHO n
0
0
i
* I
:
!*
ECLO
o
ECHO
" • » 0 " '
" 0
0
c
i
9
r [
i.
3 W
'^
T
>
i (
.
I '
T '
•j 1
t
j
ic
*
1
1-Oct-1998 1-Apr-1999 1-0ct-1999 1-Apr-2000
:i
L A 1
r <
P
1
f,
•
]
3
I
1 fb
4 !
I 1 '
u
1-0ct-2000
T
Si
SJ
c
0
CxQ
1-Apr-2001
-------
9. O3 & CO2
6/17/04
9-4
Effects of CO2 & O3 on Ponderosa Pine Seedlings
Stem diameter was measured as a key indicator of the overall growth of Ponderosa pine
seedlings. Rapid growth periods, as shown by an increase in stem diameter, occurred
during spring and summer of 1998, 1999, and 2000. Over three years, seedlings growing
with elevated CO2 and either with low (ECLO) or high (ECHO) O3, had larger stem
diameters than seedlings grown under ambient CO2 and low (ACLO) or high (ACHO) O3
(top figure). Beginning early in the study, compared to plants growing under control
conditions (ACLO), there was a greater increase in stem diameter for ECLO compared
with ECHO seedlings, indicating that high O3 inhibited some of the effect of elevated CO2
(lower figure). Source, Olszyk etal. 2001 and unpublished data.
35
,30 q
A. STHVI DIAMETER
Apr 1,98 Oct 1,98 Apr 1,99 Oct 1,99 Apr 1,2000 Oct 1, 2000
DATE
r±
W3-|
LU
CO
0-
B DIFFERENCEVS ACLO
c ECEO
c ACEO
.__. .
ECLO
^^"..
0 -°° o 8o°o „ o
Apr 1, 98 Oct 1,98 Apr 1, 99 Oct 1, 99 Apr 1,2000 Oct 1,2000
DATE
-------
9. O3 & CO2 9-5
References Cited
Barnes, J.D. and Wellburn, A.R. 1998. Air Pollutant Combinations. In Responses of Plant
Metabolism to Air Pollution and Global Change (ed. L.J. De Kok, & I. Stulen). pp. 147-164.
Backhuys Publishers, Leiden, The Netherlands.
Olszyk, D.M., Tingey,D.T., Wise, C., and Davis, E. 2002. CO2 and O3 alter photosynthesis and
water vapor exchange for Pinus ponderosa needles. Submitted to Phyton.
Olszyk, D.M., Tingey,D.T., Watrud, L, Seidler, R. and Andersen, C. 2000. Interactive Effects of
O3 and CO2: Implications for Terrestrial Ecosystems. In Trace Gas Emissions and Plants, (ed.
S.N. Singh), pp. 97-136. Kluwer Academic Publishers, Dordrecht, Germany.
Olszyk, D.M., Johnson , M. G., Phillips, D.L., Seidler, R.. , Tingey,D.T and Watrud, L.S. 2001.
Interactive effects of O3 and CO2 on a ponderosa pine plant/litter/soil mesocosm. Environ. Pollut.
115,447-462.
Olszyk, D.M., Tingey,D.T., Watrud, L.,Seidler, R. and Andersen, C. 2000. Interactive Effects of
O3 and CO2: Implications for Terrestrial Ecosystems. In Trace Gas Emissions and Plants, (ed.
S.N. Singh), pp. 97-136. Kluwer Academic Publishers, Dordrecht, Germany.
Olszyk, D.M., Tingey,D.T., Johnson , M. G.,, Seidler, R., Watrud, L., Weber, J., Phillips, D., &
Andersen, C., Cairns, M., Hogsett, W., Brown, S.and McKane, R. 1997. Research Plan:
Interactive Effects of O3 and CO2 on the Ponderosa Pine Plant/Litter/Soil System. US EPA,
NHEERL-COR-876R.
Rastetter E.B., Ryan M.G., Shaver G.R., Melillo J.M., Nadelhoffer K.J., Hobble J.E., Aber J.D.
1991. A general biogeochemical model describing the responses of the C and N cycles in
terrestrial ecosystems to changes in CO2, climate and N deposition. Tree Physiology 9:101-126.
Rudorff, B.F.T., Mulchi, C.L. & Lee, E.H. 2000. Plant Responses to Elevated CO2 and
Interactions with O3. In Trace Gas Emissions and Plants, (ed. S.N. Singh), pp. 155-179. Kluwer
Academic Publishers, Dordrecht, Germany.
Tingey, D. T., J. A. Laurence, J. A. Weber, J. Greene, W. E. Hogsett, S. Brown, and E. H. Lee.
2001. Elevated CO2 and temperature alter the response of Pinus ponderosa to ozone: a
simulation analysis. Ecological Applications 11:1412-1424.
-------
10. Fine Roots 10-1
10. Effects of Elevated CO2 and Nitrogen Fertilization on Fine
Root Growth in seedling Pinus ponderosa
Statement of the Problem
In forest trees, less than 20% of the total biomass is belowground while more
than 50% of the carbon acquired annually by plants may be allocated
belowground (George & Marschner 1996). With rising atmospheric carbon dioxide
(CC^) the potential for effects of elevated C02 on forest trees is large. A number
of studies have evaluated the effects of elevated C02 on plants (e.g., Ceulemans &
Mousseau 1994; Curtis & Wang 1998, Norby 1994, Rogers et al. 1999, Taylor et al. 1994). Their
general conclusion is that elevated C02 leads to increased photosynthesis and
increased plant biomass, including increased root biomass. Will this increase in
biomass lead to a greater proportion of the carbon being allocated belowground
and potentially sequestered there?
Three science questions guided the study on ponderosa pine (Pinus ponderosa
Dougl.J:
• Will the size of the root systems of ponderosa pine seedlings increase to
facilitate resource (water or nutrients) acquisition in response to elevated
C02?
• Will ponderosa pine root systems be affected by the availability of nitrogen?
• Will the dynamics of ponderosa pine fine root production and mortality be
affected by elevated C02 and/or nitrogen treatments?
Approach
Plants were exposed to C02 and nitrogen (N) fertilization in open-top field-
exposure chambers located at the US Forest Service Institute of Forest Genetics
near Placerville, CA. The experimental design was a replicated 3x3 factorial with
3 C02 levels (ambient air [~350 umol mol-1]; ambient air + 175 umol mol"1 and
ambient air + 350 umol mol"1) and 3 levels of nitrogen (N) addition (0, 100 and
200 kg ha"1); however, the 100 kg ha"1 N treatment at ambient + 175 umol mol"1
C02 was omitted from the experimental design because of financial limitations.
There were 3 replicates of each C02 and N treatment. The nitrogen was
broadcast applied each March as ammonium sulfate. Soils were kept moist and
relatively constant over the course of the study. Root images were collected from
three minirhizotron tubes in each chamber every 2 months on S-VHS tape using
a minirhizotron camera. The root images were analyzed using software that
allows the user to measure the length and diameter of all roots and annotate
mycorrhizae and fungal hyphae occurrence.
-------
10. Fine Roots 10-2
Main Conclusions
Fine roots explore soil for water and nutrients to support plant growth. Plants
produce more or fewer fine roots as their resource needs change. A given
species may produce more fine roots in nutrient poor soils than in nutrient rich
soils. In arid environments plants typically produce more fine roots than in wetter
environments. In this experiment the ponderosa pine trees - normally a dry forest
species - were well watered in order to examine the effects of elevated
atmospheric carbon dioxide (CC^) and nitrogen (N) on fine root dynamics.
Elevated C02 and N treatments both increased plant height, stem diameter and
leaf area (Tingey et al. 1996,1997). Elevated C02 resulted in significantly higher root
biomass in the first 3 years and higher fine root turnover in the last 2 years. No
significant N effects were noted for annual root biomass production, or turnover.
Fine root nutrient cycling rates varied from 74 to 362 g m~2 yr"1 for C and 0.9 to
4.6 g m~2 yr"1 for N (Phillips et al, unpublished results).
Fine-root production and life span were strongly influenced by season and soil
temperature (Johnson et al. 2000). Fine roots declined in importance with time and
were replaced with mycorrhizae which continued to increase with time. This
temporal pattern of root and shoot growth was not altered by providing additional
C02 or N fertilization (Tingey et al. 1996).
Both C02 and N affected the fine roots, but the effects were independent and
displayed contrasting effects. In this study, elevated C02 increased above and
below ground plant growth because nitrogen was not limiting even in the
unfertilized plots. Although elevated C02 increased fine root growth, it did not
change the relationship between fine roots and needles indicating that elevated
C02 did not increase the proportion of carbon allocated belowground (Tingey et al.
1996). Elevated C02 increased root lifespan but N decreased it (Johnson etal. 2000,
Tingey et al. 1997). Initially, elevated N reduced the fine root area relative to the
needle area, but this ratio was not altered by elevated C02 treatments.
Soil exploration by the roots increased with elevated C02, but was unaffected
when nitrogen was abundant as in the fertilized plots. Fine root production was
increased by elevated C02 whereas N fertilization had no effect on fine root
production (Tingey et al. 1996,1997). This suggests that as the limiting resource,
nitrogen in this case, increases the plants do not need to produce as many fine
roots to explore more soil to acquire enough of the resource. In contrast,
increased C02 resulted in more images containing roots suggesting more soil
exploration by roots.
Elevated C02 increased mycorrhizal and fungal occurrence earlier than N
fertilization, and elevated C02 increased C flux into mycorrhizae (Rygiewicz et al.
1997, Tingey et al. 1997). Higher levels of N resulted in increased mycorrhizal activity
relative to fine root production. The amount of mycorrhizae relative to the amount
of fine roots did not change with increased C02 - they both increased in the
same proportion. However, N fertilization resulted in more mycorrhizae relative to
-------
10. Fine Roots 10-3
roots. Under elevated C02 fine roots increased providing additional infection
sites, and, consequently, mycorrhizal occurrence increased proportionally. In
contrast, nitrogen fertilization increased root branching without increasing the
amount of fine roots, thereby providing more site for mycorrhizal infection.
In summary, limiting resources determined the response of ponderosa pine root
systems to changes in atmospheric C02 and soil nitrogen. As plants needed
more nitrogen their roots explored more soil area to acquire this resource.
Elevated C02 allowed the trees to take up more carbon for growth both above
and below ground, but the amount allocated to the root system decreased as soil
nitrogen become more available. Again, in this study water was not limiting and
consequently did not affect the root system. With time mycorrhizae became more
important to the root systems and effectively replaced the fine roots. Their
abundance increased proportionally with fine roots under increased levels of
C02, but increased in greater proportion than fine roots with higher levels of soil
nitrogen.
-------
10. Fine Roots
10-4
Effects of Elevated CO2 on Root Production & Turnover
A 4-year study was conducted to determine the effects of atmospheric
C02 and N-fertilization on Pinus ponderosa fine root (<2 mm) responses.
Seedlings were grown in open-top chambers at 3 C02 levels (ambient,
ambient+175 ppm, ambient+350 ppm) and 3 N-fertilization levels (0, 10,
20 g-m~2-yr~1). Length and width of individual roots were measured from
minirhizotron video images collected bimonthly over 4 years. Biomass
estimates were made by cross-calibrating with soil core root biomass.
Neither C02 nor N-fertilization treatments affected root production and
turnover seasonal patterns. Elevated C02 resulted in significantly higher
biomass (g-m~2) in the first 3 years and higher turnover (g-m~2-yr~1) in the
last 2 years. No significant N effects were noted for annual root biomass,
production, or turnover. Fine root nutrient cycling rates varied from 74-
362 g-m -yr for C and 0.9-4.6 g-m -yr for N. Higher turnover in
elevated C02 was due to higher biomass rather than shorter life-span.
Fine roots lived longer in elevated C02, and turnover relative to biomass
was generally < that in ambient CC^, emphasizing the importance of root
turnover definitions.
100
L M H C02
- 4 - Year
-------
10. Fine Roots
10-5
Effects of CO2 and Nitrogen Fertilization of Fine Root Life Span
Ponderosa pine seedlings were grown at varying atmospheric CO2
concentrations paired with varying concentrations of exogenously-applied
nitrogen. Increasing CO2 levels increased the lifespan of the ephemeral,
nutrient-absorbing fine roots. Whereas, increasing the amount of applied
nitrogen decreased root lifespan. These results illustrate: (1) the enhanced
role of the ephemeral, nutrient-absorbing fine roots under elevated CO2 to
acquire nitrogen needed to balance the increased available CO2, and (2)
how the role of these roots was reduced as the available nitrogen increased.
Source: Johnson et al. 2000.
140
T
1
A+175 A+35Q MQ
Treatment
M1DO N2QQ
-------
10. Fine Roots 10-6
References Cited
Ceulemans R, Mousseau M. 1994. Effects of elevated atmospheric CO2 on woody plants.
NewPhytologisf\27: 425-446.
Curtis PS, Wang X. 1998. A meta-analysis of elevated CO2 effects on woody plant mass,
form and physiology. Oecologia 113: 299-313.
George E, Marschner H. 1996. Nutrient and water uptake by roots of forest trees. Zeitschrift
fur Pflanzenernahrung und Bodenkulture 159: 11-21
Johnson, M.J., D.L. Phillips, D. T. Tingey and M.J Storm. 2000. Effects of elevated CO2, N-
fertilization and season on survival of ponderosa pine fine roots. Canadian Journal of Forest
Research 30:220-228.
Norby RJ. 1994. Issues and perspectives for investigating root responses to elevated
atmospheric carbon dioxide. Plant and Soil 165: 9-20.
Rygiewicz, P.T., M.G. Johnson, M.J. Storm, D.T. Tingey and L. Ganio. 1997. Lifetime and
temporal occurrence of ectomycorrhizae on ponderosa pine (Pinus ponderosa Laws.)
seedlings grown under varied atmospheric CO2 and nitrogen levels. Plant and Soil 189:275-
287.
Tingey, D.T., D.L. Phillips, M.G. Johnson, M.J. Storm and J.T. Ball. 1997. Effects of elevated
CO2 and N-fertilization on fine root dynamics and fungal growth in seedling Pinus ponderosa.
Environmental Experimental Botany 37:73-83.
Tingey, D.T., M.G. Johnson, D.L. Phillips, D.W. Johnson and J.T. Ball. 1996 Effects of
elevated CO2 and nitrogen on the synchrony of shoot and root growth in ponderosa pine.
Tree Physiology 16:905-914.
-------
11. FACE Experiment 11-1
11. Free-Air CO2 Enrichment (FACE) Experiment
Statement of the Problem
A number of effects of elevated atmospheric C02 concentrations on plants have been
demonstrated in greenhouse and controlled environment chamber studies. However,
such studies have inherent limitations that reduce their value in predicting responses to
rising C02: (1) physical facilities constrain the plant size and complexity of system which
can be used, (2) the experimental conditions in these chambers which may be
unrealistic, and (3) the experiments are short-term and may be unable to detect either
delayed or transient effects. Greater understanding of direct effects of elevated C02
requires experiments on intact natural ecosystems, composed of multiple interacting
species of a variety of sizes and ages, and continued over an extended period of time
(multiple years).
Approach
Technology has been developed for Free-Air C02 Enrichment (FACE) facilities which
allow C02 exposure experiments to be performed on large (~500 m2) plots in intact
ecosystems. US EPA scientists are collaborating with scientists in the US Department
of Energy and the University of Nevada at the Nevada Test Site in the Mojave Desert -
the only desert ecosystem FACE facility. EPA scientists are conducting long-term
monitoring of belowground responses to elevated C02.
Main Conclusions
To date, University of Nevada scientists found that elevated C02 increases
photosynthetic rates and aboveground biomass growth - at least in years where
sufficient soil moisture is available (Hamerlynck eta\. 2000, Smith et al. 2000, Huxman and Smith
2001). The desert plants generally showed decreases in stomatal conductance (loss of
water through leaf pores) and higher water use efficiency when grown in elevated C02
(Nowakef a/. 2001, Pataki et al. 2000). However, soil moisture was no higher in elevated C02
plots. Presumably this was because the increased water use efficiency per unit
biomass was balanced by higher aboveground biomass.
Belowground, EPA researchers have found no differences in the total length,
production, or turnover of roots, indicating that the same size root systems were able to
sustain larger aboveground biomass of plants because of the higher water use
efficiency (Phillips et al. 2002). These results are important in helping us understand the
likely responses of large tracts of arid lands under global changes of atmospheric C02
content.
-------
11. FACE Experiment
11-2
Nevada Desert FACE Facility
FACE system maintains elevated CO2 over 25 m diameter plots
The Free-Air CO2 Enrichment (FACE) technology developed by the Brookhaven National
Laboratory enables CO2 exposure experiments to be performed on intact ecosystems. The
Mojave Desert ecosystem, shown here, is one of eight such state-of-the-art facilities that
have been constructed in various ecosystems across United States. Atmospheric CO2
concentrations and wind speed and direction are continuously monitored. In elevated CO2
plots, computer controlled valves on the vertical pipes open on the upwind side of the plot,
releasing CO2 to maintain a CO2 concentration 200 ppm higher than the ambient CO2 of
-360 ppm. Transparent plastic tubes inserted to a depth of 1 m in the soil (shown here with
white insulating caps on top) are used with specialized video cameras to monitor the
growth and mortality of roots in the experimental plots, to determine the belowground
effects of elevated CO2.
-------
11. FACE Experiment 11-3
Elevated CO2 did not affect fine root standing crop, production, or turnover
Tube Location = Larrea
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0.0
Standing crap
Ambient
On a monthly basis, specialized video cameras are inserted in transparent tubes installed
in the soil to make photographic images of roots. These images are digitized and the
production, growth, and mortality of each root can be tracked over time. These data provide
detailed dynamics of root populations and how they are affected by CO2 exposure as well
as season, soil moisture, and other conditions. Elevated CO2 did not significantly affect the
standing crop (total length), production, or turnover of roots over a very wet year (1998) and
a dry year (1999) (Phillips et a/. 2002). This indicates that the same size root systems were
able to sustain the larger aboveground biomass of plants in elevated CO2 treatments
because of higher water use efficiency. Total root length varied from year to year
depending on soil moisture availability.
-------
11. FACE Experiment 11 -4
References Cited
Hamerlynck, E.P., I.E. Huxman, R.S. Nowak, S. Redar, M.E. Loik, D.N. Jordan, S.F. Zitzer, J.S.
Coleman, J.R. Seemann, S.D. Smith. 2000. Photosynthetic responses of Larrea tridentata to a step-
increase in atmospheric CO2 at the Nevada Desert FACE Facility. Journal of Arid Environments 44: 425-
436.
Huxman, I.E., and S.D. Smith. 2001. Photosynthesis in an invasive grass and native forb at elevated
CO2 during an El Nino year in the Mojave Desert. Oecologia 128: 193-201.
Nowak, R.S., L.A. DeFalco, C.S. Wilcox, D.N. Jordan, J.S. Coleman, J.R. Seemann, and S.D. Smith.
2001. Leaf conductance decreased under free-air CO2 enrichment (FACE) for three desert perennials in
the Nevada desert. New Phytologist 150: 449-458.
Pataki, D.E., I.E. Huxman, D.N. Jordan, S.F. Zitzer, J.S. Coleman, S.D. Smith, R.S. Nowak, and J.R.
Seemann. 2000. Water use of two Mojave Desert shrubs under elevated CO2. Global Change Biology 6:
889-897.
Phillips, D.L., D.T. Tingey, M.G. Johnson, C.E. Catricala, and T.L. Hoyman. 2002. Effects of elevated
CO2 on fine root biomass, production, and turnover in a Mojave Desert ecosystem: a FACE study.
Manuscript in preparation.
Smith, S.D., T.E Huxman, S.F. Zitzer, T.N. Charlet, D.C. Housman, J.S. Coleman, L.K. Fenstermaker,
J.R. Seemann, and R.S. Nowak. 2000. Elevated CO2 increases productivity and invasive species
success in an arid ecosystem. Nature 408: 79-82.
-------
12. Coral Health 12-1
12. Effects of Global Change on Coral Reef Ecosystems
Statement of the Problem
Corals and coral reefs of the Caribbean and throughout the world are deteriorating at an
accelerated rate. Several stressors are believed to contribute to this decline, including
global changes in atmospheric gases and land use patterns (Fig. 1). In particular,
warmer water temperatures and elevated exposure to ultraviolet radiation has been
linked to coral bleaching, which occurs when corals lose symbiotic algae. Bleached
corals may recover, contract infectious diseases, or become overgrown with a layer of
macroalgae. Loss of corals has significant socioeconomic repercussions; in Florida,
Hawaii and most U.S. territories in the Caribbean and Pacific Ocean, coral reefs provide
valued services in the form of fisheries, recreation, tourism and coastal protection from
storm erosion. Furthermore, with hundreds of thousands of interdependent species,
coral reefs are one of the largest global reservoirs of biodiversity and a potential wealth
of undiscovered natural products. The abundant and diverse reef species are the
substance of a flourishing and extensive marine ecosystem.
Geological records show that coral community structure has been stable over the last
220,000 years (Chadwick-Furman 1996, Aronson and Precht 1997). Yet, during the last 30
years, coral bleaching and disease have escalated worldwide (Hughes 1994, Hughes and
Tanner 2000, Gardner et al. 2003, Hughes et al. 2003, Pandolfi et al. 2003). In 1998, the largest
bleaching event on record affected about 16% of the world's coral reefs. It has been
estimated that 27% of the world's reefs were lost in the last three decades and that 60%
will be eliminated by 2030 (Wilkinson 2000). Many believe that ecological extinction for
coral reefs could occur in this century if current trends persist (Gardner et al. 2003, Hughes
etal.2003).
Although the situation is alarming, relatively little is known about the environmental
factors and interactive stresses that lead to coral bleaching. The term 'bleaching' refers
to the loss of color when corals lose their symbiotic algae (Fig. 2), which are
photosynthetic dinoflagellates often called zooxanthellae. Usually bleaching signifies
environmental stress leading to a breakdown of the coral-algae symbiosis. In fact,
bleaching at the local scale has been associated with several stressful environmental
conditions (Goreau 1964, Glynn 1984) including high and low temperatures, high and low
solar radiation, reduced salinity, and coral exposure to air, ultraviolet radiation,
sediments, toxic chemicals, and high levels of bacteria (Mitchell and Chet 1975, Hoegh-
Guldberg and Smith 1989, Glynn 1996, Brown 1997a).
Large-scale bleaching, however, is most strongly associated with elevated sea water
temperature (Williams et al. 1987, Glynn and de Weerdt 1991, Milliman 1993, Brown 1997b, Hoegh-
Guldberg 1999, Barber et al. 2001, Fitt et al. 2001). Many coral species may be susceptible to
thermal bleaching because they live near the upper limit of their temperature tolerance
(Scavia et al. 2002). Prior to 1980, bleaching was infrequent and events were confined to
local scales (Goreau 1964, Goreau and Hayes 1994, Aronson et al. 2000). Since then, however,
-------
12. Coral Health 12-2
the extent, severity and frequency of bleaching events have increased dramatically.
The link between coral bleaching and global climate change is compelling. Massive
episodes of coral bleaching have accompanied the last several El Nino phases of the
Southern Oscillation (ENSO). These events have occurred world-wide and irrespective
of other local anthropogenic stressors (Hoegh-Guldberg 1999, Wilkinson et al. 1999). Greater
frequency, intensity, and spatial extent of bleaching have been documented since the
1982-1983 ENSO, including an exceptionally strong 1997-1998 ENSO that exhibited
record sea-surface temperatures and coincided with the most geographically
widespread and severe bleaching in history (Glynn 1984, Wilkinson 1998). Up to 95% of the
living coral reefs from the central Indian Ocean and its margins were bleached, and
bleaching occurred along the margins of the Caribbean Sea, the Indian Ocean and the
Pacific Ocean. Although ENSO phases are measured in the Pacific Ocean, climate and
weather patterns are altered worldwide. In the Caribbean, ENSO phases generate
higher sea water temperatures and calm, stratified water conditions (doldrums) that
allow increased penetration of solar radiation. These conditions are tailor-made for
bleaching because of the interactive effects of high temperature and the high ultraviolet
light that reaches coral reefs.
Corals rely on photosynthetic energy derived from algal symbionts found within the
polyps, or colonial units of the coral. Since photosynthesis requires solar radiation, most
corals are confined to shallow coastal waters penetrated by sunlight. Coral reefs are
located in tropical and sub-tropical oceans that are exposed to the most intense solar
radiation on Earth (Madronich etal. 1998). This distribution, however, places corals at risk
from exposure to ultraviolet light (UV), particularly the damaging UV-B wavelengths
(Shicket al. 1996). Increased penetration of UV-B to the earth's surface has been
attributed to a decline in UV-absorbing ozone in the stratosphere. Although
stratospheric ozone depletion in the tropics is not as great as at the poles, there is
concern that any increase in the high levels already experienced could affect coral
health. The most variable aspect of coral exposure to UV-B is its penetration through
the water above reefs. Many local variables, such as water quality and weather, can
influence attenuation of UV-B with depth. For example, dissolved organic matter
absorbs UV-B and reduces its penetration, whereas hot, windless conditions create
thermal stratification of the water column that increases UV-B penetration.
Approach
To fulfill EPA's assessment role in the US Global Change Research Program, NHEERL
research is directed toward reducing assessment uncertainties and developing
assessment tools. Specifically, the NHEERL program uses field and laboratory studies
to determine which coral species, reefs and geographic regions are most valuable (i.e.,
providing ecosystem services), most at risk, and most responsive to management
alternatives. Research is focused in two principal areas: Development and application of
methods to assess and compare coral reef condition, and characterization of stressor-
response patterns to determine thresholds for global climate stressors. The research
approach emphasizes the fact that changes in the environment affect both partners, the
-------
12. Coral Health 12-3
corals and the algal symbionts, and that effects on either can alter the symbiotic
relationship. The primary stressors under investigation are elevated temperature and
UV-B. Other environmental stressors, such as nutrients, contaminants and sediments,
are expected to exacerbate bleaching at local scales.
Methods to Assess and Compare Coral Reef Condition
The Florida Keys coral reef tract provides a substantive opportunity to investigate the
causes and effects of global change on coral reefs. Not only is it a relatively large tract
(44 km2) with reefs in both remote areas and near human population centers, but it has
experienced major declines in coral health and coral cover during the last thirty years. A
Coral Reef Monitoring Project has been supported by US EPA Region 4 since 1996 to
annually determine the total percent of live coral coverage at 160 permanent stations in
the Florida Keys National Marine Sanctuary (FKNMS). After 5 years (1996-2000), a
38% decline in live coral coverage has been documented (Fig. 3; Jaap et al. 2000, Wheaton
et al. 2001, Porter et al. 2002). Much of this loss has been attributed to bleaching events and
the emergence of new diseases (Antonius 1981,1985,1988, Dustan and Halas 1987, Santavy and
Peters 1997, Richardson et al. 1998, Santavy et al. 1999, 2001, 2004). Of particular concern has
been the dramatic decline of fast-growing, reef-building acroporid corals (Patterson etal.
2002), including elkhorn coral (Acropora palmata) and staghorn coral (A. cervicornis).
A complementary survey has been conducted by NHEERL scientists to document
bleaching and disease across the entire reef tract. Performed in collaboration with
NOAA (FKNMS), the NHEERL survey includes 60 stations, selected by probability,
ranging from the Upper Keys to the Dry Tortugas (Fig. 4). Each colony in a radial belt
transect (113 m2) is examined, counted and identified (Fig. 5); fifteen coral species and
eleven disease syndromes are documented. Results show that up to 28% of the coral
populations near Key West are affected by disease (Santavy et al. 2001). Corals in this
area do not appear to be recovering and, in the case of elkhorn coral, there has been
nearly complete destruction (Patterson et al. 2002). NHEERL collaborative research with
the University of Georgia has shown that elkhorn corals are susceptible to white pox
disease caused by Serratia marcescens, a common soil and enteric microorganism
(Patterson et al. 2002). Yet, across the Florida Keys reef tract the prevalence of disease is
considerably less (Santavy et al. 2004). In August, 2002, the greatest prevalence
(percentage of diseased corals at any site) was 13%, but this occurred in only 2.2% of
the sampling area (Fig. 6). Seventy-nine percent of the area had less than 6% disease
prevalence.
The annual field surveys were initiated and performed in response to the emergence of
several diseases that were unknown prior to 1970. With continued declines in South
Florida corals, the NHEERL research effort has expanded to characterize coral
condition. New measurements are being introduced to evaluate the cumulative
consequences of bleaching and disease, as well as other stressors, on coral individuals
and populations. Reef-to-reef comparisons of disease prevalence are sometimes
confounded by different taxonomic composition (e.g., some sites do not have
susceptible host species); the new condition measures are unrelated to taxonomic
-------
12. Coral Health 12-4
composition and allow direct comparisons across reefs and geographic areas.
Three condition endpoints have been added to the disease survey that estimate total
coral surface area, the percent of living coral, and the living coral surface area of each
coral encountered in the transect. Total surface area (TSA) serves as a surrogate for
reef structural complexity and the habitat value associated with high complexity. It also
supplies a record of the cumulative, or historical, capacity of the habitat to grow and
sustain corals. Percent living coral (%LC) can be used to examine potential associations
of adverse effects from diseases or other stressors. Living surface area (LSA) is an
indicator of the more recent capacity of the environment to support corals; LSA also
represents the amount of coral with potential to grow and reproduce.
A pilot project was conducted in 2003 to investigate the feasibility of acquiring these
data in combination with bleaching and disease surveys. Five stations at two study
areas, Key West and Dry Tortugas, were surveyed. The Key West area has high human
density relative to the remote Dry Tortugas. Comparison of data demonstrated wide
differences in species composition, abundance, TSA and %LC (Table 1), but the actual
living coral (LSA) was nearly identical at both study areas. One promising tool is the
comparison of %LC among species (Fig. 7), which will indicate whether one species
has lost more tissue than other species in the same area, and whether the same
species has lost more tissue in one study area over another. It is anticipated that these
measures of coral condition will ultimately be integrated into a condition index for
comparison of reefs and geographic areas over time. Until then, the bleaching, disease
and condition information provided by the field surveys is directly useful in the
management of the Florida Keys National Marine Sanctuary and the Dry Tortugas
National Park.
Although condition indicators can provide useful insight to status and trend of coral
populations, it is imperative for future management that declining condition is ultimately
linked to a cause. Condition indicators can be used to compare reefs with putative coral
stressors. To this end, NHEERL scientists are investigating chemical contaminants in
coral reef areas, and collaborate both with Florida International University to measure
nutrients and chlorophyll and with NERL scientists to measure temperature and UV-B at
coral reefs. Any associations of these factors with declining coral condition can be
investigated in the laboratory, as described below.
Characterization of Stressor-Response Patterns.
Relating coral decline to global change stressors requires knowledge of the thresholds
at which changing environmental conditions create adverse effects. NHEERL has
developed unique laboratory facilities and expertise to expand this knowledge. Two
'solar simulator' systems have been constructed to expose corals and algal symbionts
to varying levels of both photosynthetically-active radiation and UV-B. In addition,
NHEERL scientists retain in culture over 15 reef-building coral species and 28 algal
symbiont (Symbiodinium spp.) isolates for controlled laboratory experiments (Figs. 8
and 9). Research using algal symbionts is particularly promising because the interaction
of temperature and UV-B very likely affect the photosynthetic processes of symbionts.
-------
12. Coral Health 12-5
Also, results of experiments have potential worldwide application because corals have
established symbioses with relatively few algal symbiont groups (clades).
Early studies in the solar simulators validated that different coral species exhibited
different bleaching responses to elevated UV-B radiation. During these early studies,
methods for documenting changes in zooxanthellae number, photopigments,
mycosporine-like amino acids, and photosynthetic efficiency were validated and
improved. Temperature studies on algal symbionts have documented lethal thresholds
(35° C) and declining growth rates at temperatures above 31 °C during short-duration
exposures. Studies on the interactions of UV-B and temperature have confirmed, for the
first time in a laboratory system, that elevated UV-B exposure exacerbates the adverse
effects of high temperature (Fig. 10).
Several physiological mechanisms are being investigated to understand the interactive
effects elevated temperature and UV-B and to develop biomarkers able to distinguish
susceptible corals in the field. Corals are experimentally bleached in the solar
simulators and both corals and algal symbionts are examined for changes that could be
used as biomarkers of susceptibility. For example, it is expected that changes in
photopigment concentrations will be an early response to elevated UV-B. To refine
current methods, an efficient methanol extraction process was developed to quantify
changes in the symbiotic algae photopigments (Rogers and Marcovich 2004). The technique
is much improved over previous techniques, yielding greater than 95% recovery of
pigments in less than half the time. Another technique requires pulse-amplitude
modulated fluorometry to examine photosynthetic efficiency of the symbiotic algae and
may help to determine how photosynthesis is affected by temperature and UV-B. An
immunoassay technique has been adapted in collaboration with the University of
California to detect thymine dimer formation in coral DMA (Fig. 11; Anderson et al. 2001,
2004); these specific mutations are characteristically formed only by UV-B exposure. As
they are generated, biomarkers will be tested in the field to determine their ability to
predict species at risk to both global change and local stresses.
Main Conclusions
Coral health in the Florida Keys is deteriorating at unprecedented levels. Tools to
evaluate coral reef condition are needed to assess potential consequences of this
decline and to guide management options. Field surveys that estimate prevalence and
distribution of coral bleaching and disease, using a probability-based sampling design
and a radial belt transect (113 m2), have been validated and applied at 60 sampling
stations across the Keys (41 km2). Bleaching and disease prevalence in the Lower Keys
was particularly high in 1998 relative to other years (1998-2002), and was higher than
comparison sites in the Dry Tortugas. A pilot project, comparing only five sites in the
Lower Keys with five sites in the Dry Tortugas, demonstrated a greater percentage of
dead coral in the Lower Keys area.
Various endpoints are being validated to document coral condition. When combined,
these endpoints must reflect the growth, survival, health and reproduction of corals;
identify at-risk species; be comparable across stations, reefs and regions; and identify
-------
12. Coral Health 12-6
associations of condition with disease prevalence and other putative stressors. To
achieve this goal, bleaching and disease surveys are being supplemented with three
estimates made for each coral colony in the survey — total surface area, percent living
coral tissue, and total living coral surface area. Results from a pilot project have
demonstrated that these measures can be combined to indicate coral population health,
survival and capacity to reproduce. Continued surveys of coral populations in the
Florida Keys is expected to lend insight to the species, reefs and regions that are most
valuable, most at risk, and potentially most responsive to management action.
Relating coral decline to global change stressors requires knowledge of the thresholds
at which changing environmental conditions create adverse effects. Controlled
laboratory exposures, using novel solar simulator systems, have established
temperature and UV thresholds for various coral species and algal symbionts. Early
studies demonstrated that different coral species exhibited different bleaching
responses upon exposure to UV radiation. Temperature studies have confirmed the
adverse effects above 31 °C for coral symbionts and the interactive effects of high
temperature with elevated UV-B. Future laboratory studies will document differences in
sensitivity among the various groups (clades) of algal symbionts to temperature and UV
radiation, and will evaluate changes in sensitivity from short (acute) to long (chronic)
exposures. Various biomarkers are being investigated to provide insight to the
physiological mechanisms of bleaching and for indications of coral susceptibility to
bleaching. Characterization of stressor-response patterns for different coral species and
algal clades can be used interactively with field studies to identify which stressors are
most affecting the various species, reefs and regions of the Florida Keys.
-------
12. Coral Health
12-7
ATMOSPHERIC CHANGE
LAND USE CHANGE
Greenhouse
Gases
Deforestation
& Urbanization
Nutrients, sediments
contaminants & micro
CORALREE
Figure 12-1. Coral reefs are
affected by environmental
changes in temperature, UV-B,
photosynthetically-active
radiation (PAR), carbonate
(HCOs") availability in sea water,
nutrients, sediments,
contaminants and
microorganisms that fluctuate in
relation to global atmospheric
and land use changes.
Figure 12-2. Bleaching is a term used to
describe the loss of pigmented symbiotic algae
from coral tissue. Their loss leaves the coral
with the stark white appearance of the coral
skeleton. Coral tissue still covers the surface of
the skeleton, but is transparent.
Figure 12-3. Mean percent
coral cover declined over 160
stations in the FKNMS during
1996-2000 (from Wheaton et
al. 2001). The 2000 coral
cover represents a 38%
decline from the 1996 coral
cover
Mean Percent Stony Coral Cover
Sanctuary Wide, 160 Stations, 1996-2000
•in D7o -
O
(J
s 6%-
m
o
Q.
20/ «
/O "
Do/
/o
T"
1
}3t% T9.93%
1
j8.33%
±
T6.42% ^55^
1
1
1996 1997 1998 1999 2000
-------
12. Coral Health
12-8
Dry
Tortugas
Figure 12-4.
Coral Reef
areas and
NHEERL study
sites in the
Florida Keys
and Dry
Tortugas.
Figure 12-5. Using SCUBA, surveyors count
and identify each colony in a 113m2 radial belt
transect and examine each for evidence of
bleaching and disease.
Figure 12-6.
Cumulative
distribution function
depicting overall area
estimates associated
with coral disease
prevalence in South
Florida (with 95%
confidence intervals
(Santavy et al. 2004).
ro
o>
4 6 8 10 12
% Colonies Diseased
14
-------
12. Coral Health
12-9
Number of TSA
Colonies (m-)
Dry Tortugas
BK06
BK07
LR05
LR06
LR07
Total
Key West
SK01
SK02
SK03
ED01
WS03
Total
178
94
149
165
104
690
240
350
162
155
90
997
42.4
33.1
33.4
38.1
29.0
175.9
73.8
85.1
26.5
25.8
29.6
240.9
LSA
32.4
26.7
26.2
32.0
22.7
140.0
44.4
41.8
17.7
15.5
17.4
136.9
%LC
76.4
80.8
78.6
84.1
78.2
79.6
60.1
49.2
66.8
59.8
58.6
56.8
Table 12-1. Number of coral colonies, total estimated surface area (TSA), calculated
surface area of living coral (LSA) and the estimated percent of living coral (%LC) for all
colonies encountered within the transects at each of five stations in the Dry Tortugas
and Key West study areas. Totals were determined from combined data of all stations in
each study area.
100
80
60
20
Percent Living Coral (%LC)
IDT DKW
Figure 12-7. Percent
living coral for several
coral species that co-
occurred at Dry Tortugas
and Key West study
areas. Corals, in order,
are Acropora cervicornis,
Colpophyllla natans,
Dichocoenia stokesii,
Diploria clivosa, D.
strlgosa, Montastrea
annularis, M. cavernosa,
M. faveolata, Ponies
porltes, and Slderastrea
slderea.
-------
12. Coral Health
12-10
Figure 12-8. Laboratory culture
of different coral species allows
comparisons of susceptibility to
varying levels of temperature
and UV-B under controlled
experimental conditions.
Figure 12-9. Laboratory culture
of isolated algal symbionts
(Symbiodinium sp.) allows a
rapid examination of
temperature and UV-B effects on
the photosynthesis, pigment
production, growth and survival.
-------
12. Coral Health 12-11
References Cited
Anderson, S.A., R. Zepp, J. Machula, D. Santavy, L. Hansen and E. Mueller. 2001. Indicators of UV
exposure in corals and their relevance to global climate change and coral bleaching, human and
ecological risk assessment. Human Ecolog. Risk Assess.7:1271-1282.
Anderson, S., S. Jackson, J. Machula, L. Hansen, L. Oliver, R. Zepp, G. Cherrand H. Brown. 2004.
Diurnal variation in thymine dimers in the coral Porites porites using a sensitive immunoassay. (In review).
Antonius, A. 1981. Coral reef pathology: a review. Proc4th Int. Coral Reef Symp. 2:3-6.
Antonius, A. 1985. Coral diseases in the Indo-Pacific: A first record. PSZNI Mar Ecol 6:197-218.
Antonius, A. 1988. Distribution and dynamics of coral diseases in the Eastern Red Sea. Proc6th Int Coral
Reef Symp 2:293-299.
Aronson R.B. and W.F. Precht 1997. Stasis, biological disturbance, and community structure of a
Holocene coral reef. Paleobiol. 23: 336-346.
Aronson, R.B., W.R. Precht, I.G. Macintyre and T.J.T. Murdoch 2000. Ecosystems - Coral bleach-out in
Belize. Nature 405:36.
Barber, R.T., A.K. Hilting and M.L. Hayes 2001. The changing health of coral reefs. Hum. Ecol. Risk
Assessmt. 7(5):1255-1270.
Brown, B.E. 1997a. Disturbances to reefs in recent times. In: Life and Death of Coral Reefs, (Birkeland,
C., Ed.), pp. 354-379, New York, Chapman & Hall.
Brown, B.E. 1997b. Coral bleaching: causes and consequences. Coral Reefs 16:129-138.
Chadwick-Furman, N.E. 1996. Reef coral diversity and global change. Global Change Biology 2:559-568.
Dustan, P.A. and J. Halas 1987. Changes in reef-coral communities of Carysfort Reef, Key Largo, Florida:
1974-1982. Coral Reefs 6: 91-106
Fitt, W.K., B.E. Brown, M.E. Warner, and R.P. Dunne 2001. Coral bleaching: interpretation of thermal
tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51-65.
Gardner, T.A., I.M. Cote, J.A. Gill, A. Grant and A.R. Watkinson 2003. Long-term region-wide declines in
Caribbean corals. Science. 301:958-960.
Glynn, P.W. 1984. Widespread coral mortality and the 1982-1983 El Nino warming event. Environ. Cons.
11:133-146.
Glynn, P. 1996. Coral reef bleaching: Facts, hypotheses, and implications. Global Change Biol. 2:495-
509.
Glynn, P.W. and W.H. de Weerdt 1991. Elimination of two reef-building hydrocorals following the 1982-83
El Nino warming event. Science 253:69-71.
Goreau, T.F. 1964. Mass expulsion of zooxanthellae from Jamaican reef communities after Hurricane
Flora. Science 145:383-386.
Goreau, T.J. and R.L. Hayes 1994. Coral bleaching and ocean "hot spots". Ambio 23:176-180.
Hoegh-Guldberg, O. 1999. Climate change, coral bleaching and the future of the world's coral reefs. Mar.
Freshwater Res. 50:839-866.
Hoegh-Guldberg, O. and G.J. Smith 1989. The effect of sudden changes in temperature, light and salinity
on the population density and export of zooxanthellae from the reef corals Stylophora pistillata. Esper and
Seriatopora hystrix. Dana. J. Exp. Mar. Biol. Ecol. 129:279-304.
-------
12. Coral Health 12-12
Hughes, T.P. 1994. Catastrophes, phase-shifts and large-scale degradation of a Caribbean coral reef.
Science 265:1547-1551.
Hughes, T.P. and J.E. Tanner 2000. Recruitment failure, life histories, and long-term decline of Caribbean
corals. Ecology 81:2250-2263.
Hughes, T.P., A.H. Baird, D.R. Bellwood, M. Card, S.R. Connolly, C. Folke, R. Grosberg, O. Hoegh-
Guldberg, J.B.C. Jackson, J. Kleypas, J.M. Lough, P. Marshall, N, Nystrb'm, S. R. Palumbi, J.M. Pandolfi,
B. Rosen, and J. Roughgarden 2003. Climate change, human impacts, and the resilience of coral reefs.
Science. 301:929-933.
Jaap, W.C., J.W. Porter, J. Wheaton, K. Hackett, M. Lybolt, M. Callahan, C. Tsokos, G. Yanevand P.
Dustan 2000. Coral Reef Monitoring Project Executive Summary, EPA Science Advisory Panel, available
at http://floridamarine.org/features/.
Madronich, S., R.L. McKenzie, L.O. Bjb'rn and M.M. Caldwell 1998. Changes in biologically active
ultraviolet radiation reaching the Earth's surface, J. Photochem. Photobiol. B: Biology 46:1-27.
Milliman, J.D. 1993. Coral reefs and their responses to global climate change. Climatic Change in the
Intra-American Seas, p. 306-321. In:, United Nations Environment Programme and Intergovernmental
Oceanographic Commission (G.A. Maul ed.), Edward Arnold, London, UK.
Mitchell, R. and I. Chet 1975. Bacterial attack of corals in polluted seawater. Microb. Ecol. 2:227-233.
Pandolfi, J.M, R.H. Bradbury, E. Sala, T.P. Hughes, K.A. Bjorndal, R.G. Cooke, D. McArdle, L.
McClenachan, M.J.H. Newman, G. Paredes, R.R. Warner and J.B.C. Jackson 2003. Global trajectories of
the long-term decline of coral reef ecosystems. Science 301:955-958.
Patterson, K.L., J.W. Porter, K.B. Ritchie, S.W. Poison, E. Mueller, E. Peters, D.L. Santavy and G.W.
Smith 2002. The etiology of White Pox, a lethal disease of the Caribbean elkhorn coral, Acropora
palmata. Proc. Nat. Acad. Sci. 99(11):8725-8730.
Porter, J.W., V. Kosmynin, K.L. Patterson, K.G. Porter, W.C. Jaap, J.L. Wheaton, K. Hackett, M. Lybolt,
C.P. Tsokos, G. Ynev, D.M. Marcinek, J. Dotten, D. Eaken, M. Patterson, O.W. Meier, M. Brill and P.
Dustan 2002. Detection of Coral Reef Change by the Florida Keys Coral Reef Monitoring Project. In: The
Everglades, Florida Bay, and Coral Reefs of the Florida Keys, An Ecosystem Sourcebook. (J.W. Porter
and K.G. Porter, eds), pp 749-770, CRC Press, Boca Raton.
Richardson, L.L., W.M. Goldberg, R.G. Carlton and J.C. Halas 1998. Coral disease outbreak in the
Florida Keys: Plague type II. Rev. Biol. Trap. 46 Suppl 5:187-189.
Rogers, J.E. and D. Marcovich. 2004. A simple method for the extraction of photopigments from
Symbiodinium spp. (in review).
Santavy, D.L., E. Mueller, E.G. Peters, L. MacLaughlin, J.W. Porter, K.L. Patterson and J. Campbell 2001.
Quantitative assessment of coral diseases in the Florida Keys: strategy and methodology. Hydrobiologia
460:39-52.
Santavy, D.L. and E.G. Peters 1997. Microbial pests: Coral disease research in the western Atlantic. In:
(Lessios, H.A. and I.G. Maclntyre, eds.) Proceedings of the 8th International Coral Reef Symposium
1:607-612.
Santavy, D.L., E.G. Peters, C. Quirolo, J.W. Porter and C.N. Bianchi 1999. Yellow -blotch disease
outbreaks on reefs of the San Bias Islands, Panama. Coral Reefs 19:97.
Santavy, D.L., J.K. Summers, V.D. Engle and L.C. Harwell 2004. The condition of coral reefs in south
Florida using coral disease as an indicator. Environ. Monitoring and Assess. (In press).
Scavia D., J.C. Field, D.F. Boesch, R.W. Buddemeier, V. Burkett, D.R. Cayan, M. Fogarty, M.A. Harwell
R.W. Howarth, C. Mason, D.J. Reed, T.C. Royer, A.H. Sallenger and J.G. Titus 2002. Climate change
impacts on U.S. coastal and marine ecosystems. Estuaries 25:149-164.
-------
12. Coral Health 12-13
Shick, J.M., M.P. Lesser and P.L. Jokiel 1996. Ultraviolet radiation and coral stress. Global Change
Biology 2:527-545.
Wheaton, J.W., C. Jaap, J.W. Porter, V. Kosminyn, K. Hackett, M. Lybolt, M.K. Callahan, J. Kidney, S.
Kupfner, C. Tsokos and G. Yanev2001. EPA/FKNMS Coral Reef Monitoring Project, Executive Summary
2001. In: FKNMS Symposium: An Ecosystem Report Card. Wash., D.C. Available from:
http://www.floridamarine.org.
Wilkinson, C. 1998. The 1997-1998 mass bleaching event around the world. Pages 15-38 in C. Wilkinson,
editors. Status of Coral Reefs of the World: 1998. Australian Institute of Marine Science and Global Coral
Reef Monitoring Network, Townsville, Queensland, Australia.
Wilkinson, C.R. 2000. World-wide coral reef bleaching and mortality during 1998: a global climate change
warning for the new millennium? Pages 43-57 in C. Sheppard, editor. Seas at the Millennium: An
Environmental Evaluation. Elsevier, New York.
Wilkinson, C., O. Linden, H. Cesar, G. Hodgson, J. Rubens and A.E. Strong 1999. Ecological and
socioeconomic impacts of 1998 coral bleaching in the Indian Ocean: an ENSO impact and a warning of
future change? Ambio 28:188-196.
Williams, E.H., Jr., C. Goenaga and V. Vincente 1987. Mass bleachings on Atlantic coral reefs. Science
238:877-888.
-------
13. Synthesis 13-1
13. Synthesis
Introduction
The Global Change Research Program's mission is to improve the scientific
basis for evaluating effects of global change in the contexts of other stressors
and human dimensions, to assess the consequences of global environmental
change, and to improve society's ability to effectively respond to the risks and
opportunities presented by global change as the emerge. NHEERL's role within
this program has evolved over the years as the program's emphasis shifted from
research on carbon cycling and terrestrial ecosystems to research on and
assessment of impacts on aquatic ecosystems, including coral reefs.
As the global climate change debate was heating up in the late 1980's and early
1990's the United States Environmental Protection Agency (EPA) was rethinking
its approach to environmental protection. After two decades of "end-of-pipe"
regulation, and faced with non-point sources of pollution like agricultural runoff,
serious questions were being raised about the cost-effectiveness of
environmental policy. The EPA's Science Advisory Board (SAB) was convened
to develop recommendations for guiding the agency's policy and research for the
1990's and into the 21st century (SAB 1990). The board recommended targeting
research on problems with the greatest risk while exploring new regulatory
processes such as market incentives and public education. The high-risk
ecological problems identified by the SAB were (1) global climate change, (2)
stratospheric ozone depletion, (3) habitat alteration and destruction, and (4) loss
of biodiversity. These four issues are not mutually exclusive but interrelated in
mechanism and mitigation.
In 1988 at the request of Congress, EPA initiated the first national-scale
assessment of potential global climate change effects (Smith and Tirpak 1989).
Research within EPA's Office of Research and Development (ORD) supported
that Report to Congress and became part of the United States Global Change
Research Program (USGCRP). Started as a Presidential initiative in 1989, the
USGCRP was codified by Congress in the Global Change Research Act of 1990
(P.L. 101-606). The act established a research program "aimed at understanding
and responding to global change, including the cumulative effects of human
activities and natural processes on the environment, [and] to promote
discussions toward international protocols in global change research..." Initially,
the ORD research addressed stratospheric ozone depletion and global climate
change to support international treaty negotiations—the Montreal Protocol and
the United Nations Framework Convention on Climate Change (UNEP 2000,
UNFCCC 2002).
Today, the USGCRP climate change research is managed within the US Climate
Change Science Program along with the Climate Change Research Initiative
(CCSP 2003). The latter is a Presidential initiative which establishes near-term
-------
13. Synthesis 13-2
priorities for climate change research focusing on scientific information that can
be used to address global change risks, including: the role of aerosols in climate
forcing, inventorying carbon sources and sinks, improved climate modeling, risk
management, and improved observation and monitoring of the earths climate
system.
Early research at EPA was geared toward evaluating potential global impacts
that could most seriously affect humans and the ecosystems on which they
depend. As part of a larger EPA program addressing potential impacts to
agriculture, natural resources and human welfare, scientists at ORD's National
Health and Environmental Effects Research Laboratory (NHEERL)—and its
predecessor organizations—addressed potential changes to regional vegetation,
impacts to rice production in Asia, and the effects on North American freshwater
fish. The loss of forests, desertification and movement of major biomes with
global warming were effects that the general public could envision.
As the world became more aware of the potential seriousness of climate change,
an interest was stimulated in control technologies to reduce the accumulation of
greenhouse gases in the atmosphere. The EPA initiated projects on efficient use
of fossil fuels, accounting for emissions of greenhouse gases country by country,
and the ecological sources and sinks of carbon compounds. NHEERL scientists
focused on the terrestrial carbon cycle. A key issue in international negotiations
was whether or not forests could sequester carbon from the atmosphere in
amounts that might offset emissions.
These two policy drivers—demonstrating environmental effects of such scale as
to warrant international attention, and the ability of forests to sequester carbon
and offset emissions—triggered a long-term research effort at NHEERL to
understand the interactions between ecosystems and human-caused climate
change. Throughout the 1990's this research contributed to the scientific
underpinnings of mitigation strategies for sequestering atmospheric carbon using
forests and agriculture. Moreover, this research supported assessments of
potential ecological effects resulting from climate change both in the US and
abroad. NHEERL scientists were prominent in assessments of ecological
vulnerabilities in conjunction with the national assessment process (National
Assessment Synthesis Team 2000), and contributions to the assessments of the
International Panel on Climate Change (IPCC 1995,2001 a).
Here, we review the research accomplishments of NHEERL scientists in light of
changing policy issues, past, present and future. The intent is to show how the
laboratory's scientists responded to changing policy needs as the issue of global
climate change grew from a scientific curiosity to a major worldwide concern. We
conclude with a discussion that provides a view of emerging scientific issues
related to effects of global climate change that may impact the EPA's mission.
-------
13. Synthesis 13-3
Humans and ecosystems
Climate change has affected human populations throughout history—indeed, our
evolution as a species. Dramatic societal changes have resulted from past
climate change. Climate change could affect the human condition directly as a
result of extreme temperatures, sea level rise, and catastrophic storms and,
perhaps more profoundly, indirectly through ecological change (Watson and
McMichael 2001). The potential impact of global climate change to world food
production was a major focus of EPA research
Food production is already a critical issue in light of expanding human
populations worldwide. Potential impacts of climate change on are, therefore, of
great importance. Whereas carbon conservation and fuel use are the primary
concerns associated with global climate change in industrialized countries,
sustainable production of major food crops and drinking water are major issues
facing non-industrialized countries throughout much of the world (Speidei 2000). An
early issue raised by the USGCRP was whether or not changing climate could
compromise food production needed to support the world's growing human
population. Assessing the impacts of global climate change on major crop
species and crop production systems was critical in international negotiations
(UNFCCC2002).
Rice is the most important source of calories in the world. It is the principle food
source for approximately 1.6 billion people, and another 400 million are
dependent on it for a quarter to half of their caloric intake (Moya etai. 1998). To
meet the demands of human population growth over the coming decades an
estimated 70% increase in yield over 1990 levels is needed (IRRI 1993). Of the
major cultivation practices, irrigated rice makes up 55% of the world's harvested
rice area and 75% of world rice production (IRRI 2002).
NHEERL scientists conducted joint research with the International Rice Research
Institute in The Philippines. In concert with broader EPA-funded research on how
global climate change may affect the world's major crops, this research
examined the effects of climate change and stratospheric ozone (Os) depletion
on rice production in Asia. Higher UV-B levels do not appear to affect irrigated
rice production, however, elevated CCb and temperature can affect production
both directly and indirectly through disease and pests. Elevated C02 enhances
rice plant growth and grain yield if soil nitrogen is not limiting (oiszykef a/. 1999,
Weerakoon etal. 1999, Ziska etal. 1996), but nitrogen is, generally, limiting and
fertilizer is a major expense for farmers. In reality, the benefit of increased
production from elevated atmospheric C02 may not be realized throughout much
of the world. Additionally, higher temperatures can result in increased sterility in
rice leading to reduced grain yield (Moya etal. 1998). Regional analyses for Asia
predict a nearly 4% decrease in rice yield across south and Southeast Asia with
projected changes in temperature and precipitation associated with a doubling of
atmospheric C02 concentrations over 1990 levels (Matthews etal. 1995).
-------
13. Synthesis 13-4
As part of the larger EPA crop assessment program, NHEERL scientists
determined that for US Corn Belt, soil erosion is likely to increase with increasing
frequency and intensity of precipitation, and wind erosion will increase with
increasing temperature (Phillips et al. 1993, Lee etal. 1996). These losses will
contribute to pollution and affect the sustainable yield of crops.
Although plant productivity may rise with increases in atmospheric C02 and,
consequently, offset some erosion, the overall effect of C02 increases in
conjunction with changes in other stresses, including nutrients, temperature, and
moisture availability, is uncertain and crop specific (Phillips etal. 1996). However,
increases in plant production could increase soil carbon storage and ameliorate
erosion losses to some degree so long as nutrients and water do not become
limiting to crop growth. In fact, agricultural soils could become a small sink for
atmospheric CC^ if conservation tillage is practiced (Kern and Johnson 1993).
Ecological effects
EPA research on ecological effects was initiated in 1990 to assess the effects of
global climate change on aquatic and terrestrial ecosystems as an integral part of
the USGCRP. Early research at NHEERL assessed the impacts of climate
change on fresh water fish and changes in the distribution of major vegetation
types. In the early 1990's, policy makers became interested in the global carbon
cycle, particularly in the sources and sinks of atmospheric carbon in the
terrestrial biosphere. At that time, strategies were being formulated for removing
carbon compounds from the atmosphere, and for managing the terrestrial
biosphere to increase carbon sequestration. In particular, the large carbon pools
in forests and soils were seen as potential sinks for atmospheric carbon. At
NHEERL, research was initiated to assess forest management practices as a
means to increase carbon sequestration. At the same time scientists were
debating whether or not increased levels of atmospheric C02 would increase the
productivity of crops and forests. In response, NHEERL scientists initiated long-
term experimental research on the effects of increased temperature, elevated
atmospheric C02, and air pollution on the carbon balance of forested
ecosystems. In1998, the USGCRP was refocused; ORD's primary ecological
responsibility became watershed and aquatic ecosystem assessments. NHEERL
research is currently addressing global change effects on coral reefs.
In the following sections, we summarize the research findings of the NHEERL
scientists within the context of related research. While the research on thermal
tolerance in freshwater fish, vegetation redistribution, and carbon sequestration
has, largely, been completed and published, much of the experimental research
on carbon cycling is not yet published. With the experiments completed and the
data collected, scientists are in the process of analyzing and publishing their
findings on multiple stress effects—publications will continue over the next
several years. The research on coral reef decline was initiated in the late 1990's
-------
13. Synthesis 13-5
and is continuing, consequently, the research plans and early findings are
reported here.
Thermal tolerance in fish
Water temperature has long been recognized as one of the most important
environmental variables influencing the distribution offish species. NHEERL
scientists have investigated the thermal requirements of freshwater organisms;
especially fish, since the 1960's and 1970's when water quality research started
to focus on requirements of aquatic organisms. NHEERL scientists provided
some of the first assessments of climate change effects on North American fish
species in support of the USGCRP. They assembled data on fish species, river
characteristics (Poff and Allen 1995), and air-water temperature relationships (Stefan
and Preud'homme 1993, Eaton and Scheller 1996) to predict the impacts of climate
change on fish distributions (Eaton etal. 1995).
The effect of air temperatures on stream temperatures was determined based on
field studies (Stefan and Preud'homme 1993, Eaton and Scheller 1996). The effect of
climate warming was assessed for 57 North American fish species (Eaton etal.
1995). Results suggest that cold or cool water fish species could be lost from a
large part of their range. Habitat losses were predicted to be greatest for species
with limited distributions and in areas of the country anticipated to warm the most
(e.g., the central Midwest). Results for warm water fish species were less certain
because of a relative paucity of data on summer and winter thermal tolerances
for species.
Effects of global warming on habitable stream reaches based on temperature
changes can be modified near groundwater or tailwater discharges from
reservoirs or lakes (Sinokrot et al. 1995). Empirical models were developed by
NHEERL scientists to predict groundwater inputs to stream reaches based on
watershed slope and hydraulic conductivity (Baker ef al. 2001), and to predict
modifications to stream thermal regimes based on stream shading from
topography or riparian vegetation and groundwater inputs. These efforts will help
fine-tune model predictions of the effects of global change on fish species
distributions.
Global change effects on fish communities will depend not only on stream
temperature, but also on flow regimes. Altered flow regimes resulting from
climate change could be particularly pronounced in the western US. Research
funded by NHEERL (Lettenmaier ef al. 1992), and subsequent assessments (Gleick
2002) predict that the western US will experience a substantial reduction in the
natural storage of water as snow pack with climate warming despite potential
increases in precipitation. Loss of snowpack will result in higher stream flows in
winter and lower water levels in summer (Lettenmaier and Sheer 1991).
Consequently, aquatic ecosystems will experience substantial changes in flow
-------
13. Synthesis 13-6
regimes and sediment loads in streams and rivers, which will impact fish species
to varying degrees.
Global climate change could profoundly affect freshwater lakes because they are
sensitive to a wide array of changes in climate. NHEERL research suggested
that cold water fish are likely to disappear from southern Minnesota lakes, and
experience habitat losses of 41% in northern Minnesota lakes. Largest gains in
suitable habitat for cool and warm water species will occur in lakes with low
production—oligotrophic (Stefan etal. 1996). The recent US National Assessment
summarized possible climate change effects on water resources (Gieick2002); the
effects on lakes include:
• Small changes in climate can produce large changes in lake levels and salinity.
• With higher air temperatures, fewer lakes and streams in high-latitude areas will freeze to
the bottom and the number of ice-free days will increase, leading to increases in nutrient
cycling and productivity.
• Increased lake temperatures could result in higher thermal stress for cold-water fish,
improved habitat for warm-water fish.
• Higher temperatures will increase lake productivity and lower dissolved oxygen, and
degrade water quality.
Vegetation redistribution
Of the predicted global warming consequences, widespread changes in the
distribution of forests, grasslands, and deserts are perhaps the most striking. The
prospect of the pole-ward migration of temperate forests, the loss of tundra and
boreal forests, and the desertification of grasslands could impact much of the
world. The effects of world-wide changes in vegetation zones over a relatively
short time period would have dramatic effects on fish and wildlife species, on
forest health, on water quality, and on agriculture. Moreover, such changes in
vegetation would have significant consequences for carbon storage and loss in
the terrestrial biosphere.
The fundamental concept of vegetation redistribution is complex and occurs over
time scales from years to centuries and at spatial scales from back yards to
continents. Weeds can appear and spread in a new region within years or
decades, but the climate-induced appearance of forest tree species new to a
region requires centuries to millennia in the absence of human intervention. In
contrast, the death of extant vegetation from climate stresses can occur relatively
quickly, sometimes in only a few years or a decade.
NHEERL scientists conducted research to address vegetation redistribution
using models which predict regional vegetation patterns. Precise data bases for
climate and vegetation were critical to the modeling, and much of the early work
was dedicated to their development (e.g., EPA/NOAA 1992,1993). The modeling
research followed two approaches. One used life form classifications (e.g., Sedjo
and Solomon 1989, King and Neilson 1992) in conjunction with climate correlations to
-------
13. Synthesis 13-7
define the climate space occupied by vegetation types (Neilson etal. 1992). A
physiology model was then applied which calculated the uptake of C02 by
photosynthesis and emission of C02 by respiration in each vegetation type
(Neilson I993a, 1995). The other approach used known climate thresholds to
assemble different plant functional types in each % X % degree of latitude and
longitude (Prentice etal. 1992). Both approaches used climate projections
calculated by global climate models to define new vegetation distributions.
The redistribution of global vegetation in response to changing climate and land
use remains a major uncertainty in predicting carbon sequestering in the
terrestrial biosphere. Regional changes in temperature, precipitation, and
consequently, soil moisture, are the driving forces that will alter the distribution of
natural and managed vegetation as climate changes (Marks etal. 1993). The
NHEERL modeling results indicated that the capacity of the terrestrial biosphere
to remove and store atmospheric carbon would increase with a warmer global
climate (Solomon etal. 1993,1996; Solomon 1996, 1997). The direct effects of
increasing atmospheric C02 on biomass were simulated at a global scale and
found to increase carbon sequestration (Neilson 1993b, 1998; Neilson and Marks 1994).
Subsequent work has suggested that increases in vegetation density and carbon
storage will increase with climate warming to a threshold of approximately 4.5 C
above which vegetation density and carbon storage will diminish (Bachelet etal.
2001).
Climate-induced forest dieback and changes in the distribution of land used for
agriculture could generate a pulse of CC^from the biosphere into the atmosphere
lasting several decades (Neilson I993b, 1998). The size of such a pulse could be
15-20% of that from anthropogenic emissions over the same time period (Solomon
and Kirilenko 1997, Kirilenko and Solomon 1998). While not considered in recent
estimates of future carbon releases from the biosphere (Falkowski etal. 2000; Hurttet
ai. 2002), a carbon release of this magnitude would amplify any warming effect of
anthropogenic emissions and limit the effectiveness of carbon sequestration
efforts.
In an effort to refine estimates of C02 releases, forest gap models were used to
estimate the dynamic responses of forests to rapid climate change. These
models replicate the death, reproduction, growth, and maturity of trees, and the
development of forest ecosystems (Solomon and Bartlein 1992, Solomon and West 1993,
Bugmann and Solomon 1995, 2000). Although assessment exercises with these
models (Solomon and Bartlein 1992, Bugmann etal. 2001) confirmed the potential for the
long-term carbon pulse, the gap models have not yet been applied on the
globally-comprehensive basis needed to thoroughly evaluate the carbon pulse
phenomenon.
While the timing and magnitude remains uncertain, C02 emissions from
vegetation redistribution will almost certainly occur and will affect greenhouse
gas concentrations in the atmosphere (Solomon 1996,1997). Human population
-------
13. Synthesis 13-8
growth superimposed on climate related changes in human demographics and
agricultural land use will have an effect on the size and timing of these releases.
Analogously, Houghton et al. (1999) estimated that over the period 1700-1990, 25
petagrams (Pg) of carbon was released into the atmosphere from land use
change in the US, largely from the conversion of forests to agricultural land and
cultivation of prairie soils. In comparison, the US emission of C02 equivalents for
the ten year period 1990-1999 was approximately 58 Pg (us Dept.of state 2002). In
a warmer world, the intensity of agriculture is expected to increase at higher
latitudes, thus reducing the capacity of the earth to store carbon and create
potential sources of C02 through soil warming and land conversion (Cramer and
Solomon 1993, Leemans and Solomon 1993, Solomon and Leemans 1997).
Vegetation zones are likely to shift as climate changes over the next century and
beyond, but how they shift within regions and watersheds, over what time period,
and with what ecological effects is still unclear. But that kind of information is
necessary for developing adaptation strategies. Perhaps most limiting to
vegetation modeling is the inability to predict regional precipitation and soil
moisture. Current global and regional climate models cannot predict precipitation,
soil moisture, and runoff on time scales beyond a few days (Hornberger et al. 2001).
Adding to the uncertainty in predicting vegetation patterns, regional vegetation
models are unable to simulate processes which control the redistribution of plant
species—dieback, seed dispersal, and establishment. Global climate change
involves rapidly changing climate, which may exceed the capacity of many plant
species to adapt (Solomon et al. 1996, Etterson and Shaw 2001). Rapid loss of
vegetation assemblages and slow, species-by-species establishment elsewhere
is much more likely than a gradual process which delivers fully developed plant
communities instantaneously. It is unlikely that new vegetation communities will
contain the same species in the same abundances as old ones because
migration and establishment requirements differ from species to species (Solomon
and Kirilenko 1997, Kirilenko and Solomon 1998). Presently, the models do not account
for factors controlling seed dispersal and species migration. Such improvements
are needed before better predictions of species composition and carbon storage
can be made.
Wildfires were not included in the NHEERL vegetation modeling, but they will
affect future redistribution of vegetation and carbon loss from increasing climate
stress. Large areas of essentially undisturbed forests in the US have been
protected by fire suppression during the last century, permitting dangerous levels
of fuels to accumulate and increasing the likelihood of severe, uncontrollable
fires. Globally, the drought conditions over continental areas projected by most
climate models (Solomon and Leemans 1997) will increase wildfire occurrences. Only
recently have dynamic vegetation models included fire factors based on
vegetation types, climatic conditions, and fuel characteristics (e.g., Bachelet et al.
2001). Currently, methods to include fire intensities and distributions in regional
vegetation models based on wildfire characteristics, climate conditioning of
vegetation, land use distributions, soils and topography are being developed by
-------
13. Synthesis 13-9
EPA and USGS scientists. Once tested, these models will provide improved
predictions of vegetation redistribution and carbon cycling. They will also be
valuable in predicting health-related effects of wildfire emissions.
Carbon sequestration in forests
Sequestration of atmospheric carbon in soils and vegetation could play a key role
in mitigating anthropogenic C02 emissions. Forest systems are a globally
significant terrestrial carbon pool and play a major role in the Earth's carbon
cycle through assimilation, storage, and emission of C02 (Dixon etal. 1994). The
ability of forests to remove carbon from the atmosphere and store it for long time
periods—carbon sequestration—is potentially important in mitigating
anthropogenic emissions of carbon dioxide (Dixon etal. 1999, UNFCCC 2002).
The annual exchange of carbon between forests and the atmosphere, and the
amount of carbon stored in forests, varies with the nature of forest cover, land
use, and climatic constraints. Despite this variation NHEERL scientists showed
that managing forests to maximize growth and biomass retention can significantly
increase the long-term sequestration of atmospheric C02 (Dixon etal. 1994).
Maintaining healthy forests was determined to be the most efficient way to store
carbon, but uncertainties remain.
Most assumptions of how much carbon forests can sequester do not account for
vegetation redistribution, land use change, or changes in human population
density resulting from climate change. These factors can significantly affect
estimates of carbon stored in forests. Changing land use is perhaps the greatest
threat to sequestering carbon in forests (Dixon etal. 1999). Efforts aimed at storing
carbon in the tropics—where the world's largest pools occur—are being
countered by carbon emissions from forest destruction. Moreover, increasing
agriculture in response to the growing human population is impacting forested
regions world-wide. In fact, land use changes may have as large or larger effect
on terrestrial carbon sequestration than direct climate change effects (Schimel etal.
2000).
Currently, the US is pursuing voluntary limitations on C02 emissions (EPA 2003),
but should the US decide to pursue and implement strict limits in the future, EPA
may be asked to regulate sources and sinks (Nature 2003, Samuelsohn 2003, Jeffords
2003). Moreover, many states within the US have passed or are developing
legislation to limit C02 emissions that features sequestration in forests and
agricultural soils (Murphy 2003). Participating countries under the Kyoto Protocol
can receive credit for activities that increase carbon absorption such as planting
forests, although how these credits will be assessed is still vague (Schiermeier
2002).
Carbon trading is being established under the auspices of the Kyoto Protocol in
countries that have ratified the treaty. Among participating countries, large scale
-------
13. Synthesis 13-10
reforestation projects are underway financed by the sale of carbon emission
credits (e.g., Evolution Markets 2002). Driven partly by the expectation of some
future, government-imposed emissions-reduction program, a number of large
American corporations have banded together to make voluntary reductions in
greenhouse gas emissions and trade carbon credits (Patrick 2003).
Despite all the interest and activity, there is no commonly accepted or
scientifically verifiable way to measure carbon sequestration. Without such
procedures, deciding how to calculate emissions and credits is problematical.
Procedural uncertainties exist with the accounting and verification methods (e.g.,
Rypdal and Baritz 2002). Ecological uncertainties surround factors that limit
ecosystem uptake and storage of carbon, particularly nutrient availability and
elevated levels of atmospheric C02 (Pelley 2003, Scholes and Noble 2001).
Multiple stress effects
In conjunction with rising temperatures, the carbon dioxide concentration in the
Earth's atmosphere is expected to double sometime during the second half of the
21st century (IPCC 2001 a). Understanding the response of ecosystems to elevated
atmospheric C02 is central to assessing the effects of global climate change on
ecosystems as well as determining the capability of the biosphere to sequester
anthropogenic carbon. Ecologists have been studying the effects of temperature
and precipitation—the primary drivers of productivity—on ecosystems for many
years. Atmospheric carbon dioxide while essential to ecosystem functioning has
been viewed as a relative constant. The prospect of increasing levels of
atmospheric C02 presents a new paradigm for ecologists trying to predict effects.
Elevated levels of C02 may increase primary productivity and water use
efficiency in plants resulting in increased growth and carbon sequestration—the
fertilization effect (Ceulemans and Mousseau 1994). Based on such experiments, it is
commonly assumed that agriculture and forestry will benefit from future climate
changes. Experimental studies have shown that elevated C02 increased plant
height, stem diameter, leaf area index, and fine root biomass of Pinus ponderosa
(Johnson et al. 1998, Tingey et al. 1996b) and increased P. ponderosa growth (Pushnik
etal. 1995, Surano et al. 1986). Early results from a free air C02 enrichment (FACE)
system in a young North Carolina forest show increased NPP during the first two
years of exposure, however, this may be attributed to the young age of the trees,
and may decline as the forest ages (DeLucia et al. 1999). Reviewing a number of
studies, Morison and Lawlor (1999) and Norby et al. (1999) concluded that
although elevated C02 increases the carbon assimilation rate, it does not mean
that growth will be increased because of possible limiting factors in natural
ecosystems.
In response to the uncertainties surrounding the fertilization effect of elevated
levels of atmospheric C02 and the interacting effects of other stresses, NHEERL
scientists conducted a series of experiments on intact and reconstructed natural
-------
13. Synthesis 13-11
ecosystems to study the interactive effects of climate change, elevated C02,
tropospheric ozone, and soil conditions on important tree species and
ecosystems. A state-of-the-art, environmental exposure facility that controls and
manipulates key climatic and edaphic factors was constructed at NHEERL's
Western Ecology Division (Tingeyefa/. I996a). Located in Corvallis, Oregon, this
facility was used to study the interacting effects of atmospheric C02, tropospheric
ozone, temperature, and soil moisture on forest ecosystem processes. Field
exposure chambers in the Sierra Nevada Mountains near Placerville, California,
were used to examine the effects of elevated C02 and soil nitrogen on the
Ponderosa pine forests (Johnson etal. 2000). A Department of Energy FACE facility
in the Mojave Desert on the Nevada Test Site allowed scientists to study the
direct effects of elevated C02 on intact natural ecosystems (Phillips etal. 2002).
Finally, a series of field sites were established in the western Cascade Mountains
of Oregon to compare experimental research with actual field conditions and to
provide a basis for modeling studies (McKane etal. I997b).
Ecosystems respond to elevated atmospheric C02 and temperature in complex
ways involving interactions between plants, soil processes, and the atmosphere.
A fertilization response is uncertain, particularly in natural ecosystems. Research
by NHEERL scientists (Johnson etal. 2000, Olszykef a/. 1998, Tingey etal. 1996b, 1997,
Rygiewicz etal. 1997) suggests that the response to C02 can be limited by soil
fertility—primarily nitrogen availability. Experiments in the NHEERL
environmental exposure facility used a low nitrogen soil, but if the plants that
were exposed to elevated levels of C02 were grown in a high nitrogen soil or
otherwise fertilized, the results may have been different. A sufficient supply of
nitrogen could increase growth until C02, water, or another resource became the
primary limiting factor. This new level of plant productivity would be maintained to
the extent that nitrogen supplies could be maintained.
Modeling studies support this pattern and further suggest that the commonly
observed increase, and subsequent re-acclimation, of plant growth to elevated
C02 is a consequence of nutrient limitation (e.g., Comins and McMurtrie 1993, McKane
etal. I997a). Applying the General Ecosystem Model (Rastetteref al. 1991) to various
sites in the western Cascade Mountains of the Pacific Northwest led NHEERL
scientists to suggest that soil nitrogen is a primary constraint on the ability of
those forests to sequester carbon (McKane etal. I997a). For a nitrogen-poor site,
model results indicated that total ecosystem carbon storage will increase by less
than 10% during the next 100 years in response to projected increases in
atmospheric C02 and temperature. In contrast, carbon storage at a nitrogen-rich
site was calculated to increase by over 25% during the same period.
Field studies in a variety of ecosystems also support the nutrient limitation
concept. Orem et al. (2001) reported that mature pines grown on soil with poor
fertility did not respond to elevated C02. In grassland ecosystems soil nitrogen
availability appears to limit the capacity of plants to absorb expected increases in
atmospheric C02. Recently published research on grasslands suggests that
-------
13. Synthesis 13-12
there appears to be thresholds of atmospheric C02 above which ecosystems no
longer respond (Gill et ai. 2002). Moreover, increased concentrations of
atmospheric C02 can actually reduce net primary productivity in nutrient-limited
ecosystems (Shaw et al. 2002.), hence the potential for biosphere sequestration of
atmospheric C02 may be limited.
The response of desert ecosystems to elevated C02 is limited by water.
NHEERL's collaborative research with the Desert Research Institute in the
Mojave Desert showed a measurable C02 response only when adequate soil
moisture was available (Smith et al. 2000). With adequate water, elevated C02
increased photosynthetic rates, water use efficiency, and above ground biomass
of vegetation. However, root production and turnover were not affected (Phillips et
al. 2002). Because water is the most limiting resource in this desert ecosystem,
elevated atmospheric C02 increased production by increasing water use
efficiency, but only when adequate water was available.
The fate of carbon in ecosystems that show no biomass increases to elevated
levels of atmospheric C02 remains an enigma. In long term chamber
experiments at NHEERL's Western Ecology Division, elevated levels of
atmospheric C02 increased photosynthetic rates (Lewis et al. 1999, 2001), but tree
biomass was not affected (oiszykef al. 2003). The additional carbon assimilated by
plants exposed to elevated C02was allocated to the below ground biota. But the
movement of carbon into long term storage as soil organic matter could not be
detected as gross changes in total soil carbon. Similar findings were reported for
a loblolly pine forest exposed to elevated C02(Schlesingerand Lichter2001). If plants
are photosynthesizing more with increased concentrations of atmospheric C02,
then where is this carbon going? Increases, if any, found in above ground or
below ground carbon pools are too small to explain where the additionally-fixed
carbon is being allocated—although accelerated rates of carbon cycling by
increased respiration has been suggested by NHEERL scientists and their
collaborators (Lin et al. 1999). It appears that biologically-mediated processes
belowground that transform and acquire nutrients may ultimately determine how
an ecosystem will respond to C02 fertilization.
Further analyses using stable isotope techniques detected a small increase in
soil organic matter over several years (Lin et al. 2001). Although these results are
preliminary, increased allocation of carbon to soil organic matter under elevated
levels of atmospheric C02 could result in a substantial amount of sequestered
carbon over decades to centuries, but it is uncertain if this will be a long term or
transient process. The processing of atmospheric carbon through plants and soil
biota to long term storage as soil organic matter, and how elevated temperature
and C02 associated with global climate change affects this process remains a
major scientific uncertainty.
How ecosystems respond to elevated temperatures and increased levels of
atmospheric C02 is becoming clearer. It is safe to say that the fertilization effect
-------
13. Synthesis 13-13
of C02 is not universal. In fact, it may be rare among unmanaged ecosystems.
Forests, grasslands, and deserts can be expected to respond differently to
climate change. Limiting resources seem to play an important, but uncertain role
in this response. Perhaps the most challenging aspect of predicting how specific
ecosystems respond to climate change is deciphering how multiple, interacting
stress factors—temperature, moisture, elevated C02, air pollution, and
nutrients—combine to affect ecosystem structure and functioning.
In addition to increased temperature and C02, ecosystems will be exposed to
increased air pollution resulting from warmer climates and increases in human
population. The primary cause of air pollution damage to vegetation is
tropospheric ozone (03). Damaging 03 concentrations currently occur over 29%
of the world's temperate and sub-polar forests but are predicted to affect fully
60% by 2100 (Fowler et al. 1999). In multiple stress experiments, elevated levels of
tropospheric ozone tend to cancel the stimulatory effect of C02 on plant growth
(U of Wisconsin 2002, Felzeref al. 2002, Percy et al. 2002). Research in NHEERL's sunlit,
controlled environment chambers suggests that increased levels of C02 may
moderate the detrimental effects of 03 on primary production (oiszyk et al. 2001). In
conjunction with the NHEERL chamber research, Tingey et al. (2001) used a
process-based whole-tree growth model to study the interactions of C02,
temperature, and 03. They found that increasing C02can reduce, but not
eliminate the 03 impact. However, elevated 03 also reduced the stimulant effect
of C02 on plant growth and would be expected to limit carbon sequestration.
Moreover, the interacting effects of 03 and C02 on below-ground processes are
poorly understood, but those processes are critical in determining the responses
of ecosystems to those stresses (Andersen 2003).
With global climate change, ecosystems will be subjected to a changing milieu of
stresses. Elevated C02, higher temperatures and changes in precipitation
patterns combined with the effects of increased air pollution—nitrogen deposition
and increased levels of tropospheric 03—will produce a range of effects on
natural and managed ecosystems. Ollinger et al. (2002) indicate that 03 may
counteract the increases in productivity afforded by elevated C02 and nitrogen
deposition in the northeastern US resulting in little or no altered growth over the
long term. Indirect effects and natural ecosystem processes can also limit the
ability of plants to sequester C02. Changing climatic patterns can alter net
ecosystem productivity (Knappef al. 2002). The ability of forests to sequester
carbon decreases as they age (Finzi et al. 2002, Schimel et al. 2001). The interacting
effects of C02 and air pollution can alter the susceptibility of plants to pest
damage and diseases (Percy et al. 2002). Ultimately, separating climate change
effects from land management and invasive species effects on ecosystems is an
obstacle to developing adaptation and mitigation plans.
Global change research has led us to appreciate the ramifications of multiple
stresses acting in concert, and helped us realize that controlling single pollutants
is not likely to achieve the desired results. While the NHEERL research provided
-------
13. Synthesis 13-14
insights on the interaction between, climate, CC^, and air pollution, the effects of
multiple stresses simultaneously interacting on ecosystems are still major
uncertainty. Comprehensive assessments of climate change effects on
ecosystems need to consider multiple stresses, and projects intended to mitigate
or adapt to climate change should factor in multiple stress effects.
Coral reef ecosystems
Coral reef ecosystems throughout the world are deteriorating at an accelerating
rate. This decline is attributed to multiple stress factors, which include global
changes in atmospheric gases and land use patterns. In the Florida Keys, coral
health is deteriorating at unprecedented levels. The focus of current NHEERL
research is to evaluate coral reef condition, to assess potential consequences of
this decline, and to guide management options.
Bleaching and disease prevalence in the Lower Keys was particularly high in
1998 relative to other years (1998-2002), and was higher than comparison sites
in the Dry Tortugas. A pilot project, comparing only five sites in the Lower Keys
with five sites in the Dry Tortugas, demonstrated a greater percentage of dead
coral in the Lower Keys area. Continued surveys of coral populations in the
Florida Keys will provide information on the species, reefs and regions that are
most at risk, as well as management recommendations.
Controlled laboratory experiments have established temperature and UV
thresholds for important coral species and algal symbionts. Results of early
research suggest that different coral species exhibit different bleaching
responses with exposure to UV radiation. Temperature experiments have
confirmed the adverse effects above 31 °C for coral symbionts. Also, the
interactive effects of high temperature with elevated UV-B have been quantified.
Future research will determine differences in sensitivity among the various
groups (clades) of algal symbionts to temperature and UV radiation, and will
evaluate changes in sensitivity from short (acute) to long (chronic) exposures.
Biomarkers are being developed to aid in determining the physiological
mechanisms underlying the bleaching process, and to determine coral
susceptibility to bleaching. Once the mechanisms are understood, stressor-
response patterns for different coral species and algal clades can then be used
interactively with field studies to identify which stressors are most affecting the
various species, reefs and regions of the Florida Keys.
Better tools for environmental assessments
NHEERL's climate change research program has evolved to meet changing
policy needs. Along with ongoing research, the results of past research, both
published and forthcoming, will continue to support critical policy decisions, but
future assessments may need different analytical tools. The dynamic interactions
-------
13. Synthesis 13-15
between humans and ecosystems require study because climate change
interacts with other forms of human-induced change including land use change,
air and water pollution, and invasive species. Assessments conducted at the sub-
regional and watershed levels can inform the implementation of adaptation and
mitigation strategies by state and local governments.
After more than a decade of assessing the impacts of global climate change in
one manner or another, the basic conclusions and uncertainties about potential
ecological effects remain much the same. We continue to refine our predictions,
but the models and databases needed to make assessments for manageable
parcels of land are still lacking. To some extent this is a result of the relatively
coarse resolution of global climate models from which future patterns of
temperature and precipitation are derived. But from an ecological perspective we
still lack the ability to resolve ecosystem responses to multiple stresses at an
ecologically reasonable scale.
To date, the USGCRP National Assessment has considered effects at national
and regional levels. Comprehensive assessments of the effects of C02 and
temperature changes on ecosystems at a "management" level are needed to
plan mitigation projects and guide land use decisions. Planners in both the public
and private sector will need information at the level of forest stands or
watersheds in order to fully assess effects or to implement adaptation actions.
Carbon sequestration projects will need to be designed at the scale of local land
holders, not regions.
Should C02 controls become mandatory, managing natural ecosystems to
maximize carbon sequestration will require a detailed knowledge of past, present
and future land use, and how those practices affect carbon sources and sinks.
Major questions remain about carbon uptake, translocation, and storage above
and below ground. Social, political, and economic influences on land use and
resource management, and how these forces affect the carbon storage must be
resolved. Ultimately, the data and assessment tools to evaluate actions at the
scale of projects—watersheds, forest plots, and specific crops—will be required.
To address these needs, assessment tools to evaluate land management options
in conjunction with pollution and climate effects at the scale of forest stands, or
sub-watersheds, will be critical. Ecosystem process models working at the
watershed scale will be needed to assess climate change effects on both
terrestrial and aquatic ecosystems. Continued development of spatially
distributed ecosystem models capable of accounting for the interacting effects of
elevated C02, climate change, pollution, and land use along with the supporting
data bases is clearly warranted.
-------
13. Synthesis 13-16
References
Andersen, C.P. 2003. Source-sink balance and carbon allocation below ground in plants
exposed to ozone. Tansley Review. New Phytologist 157: 213-228.
Anderson, A., R. Zepp, J. Machula, D.Santavy, L. Hansen, and E. Mueller. 2001. Indicators of UV
exposure in corals and their relevance to global climate change and coral bleaching. Human and
Ecological Risk Assessment 7:1271-1282.
Bachelet, D., R.P. Neilson, J. M. Lenihan, and R. J. Drapek. 2001. Climate change effects on
vegetation distribution and carbon budget in the United States. Ecosystems 4:164-185
Baker, M.E., M. J. Wiley, and P.W. Seelbach. 2001. CIS-based hydrologic modeling of riparian
areas: implications for stream water quality. JAWRA 37:1615-1628.
Barber, R.T., A.K. Hilting, and M.L. Hayes. 2001. The changing health of coral reefs. Human and
Ecological Risk Assessment 7:1255-1270.
Barnett, J. 2003. Security and climate change. Global Environmental Change 13:7-17.
BBC. 2003. Global warming 'will worsen hay fever.' BBC News [Health}. Tuesday, 4 February,
2003, 00:42 GMT. Retrieved 5 February 2003, from http://news.bbc.co.uk/.
Brauch, H, G., A. Carius, S. Oberthur, and D. Tanzler. 2002. Climate Change and Conflict: Can
climate change impacts increase conflict potentials? What is the relevance of this issue for the
international process on climate change? Federal Ministry for the Environment, Nature
Conservation and Nuclear Safety, Public Relations Division, Alexanderplatz6, 11055 Berlin, E-
Mail: service@bmu.bund.de,Internet: www.bmu.de Editor: The Federal Ministry for the
Environment, Division G II 3.
Bugmann, H.K.M. and A.M. Solomon. 1995. The use of a European forest model in North
America: A study of ecosystem response to climate gradients. J. Biogeography 22:477-484.
Bugmann, H.K.M. and A.M. Solomon. 2000. Explaining forest composition and biomass across
multiple biogeographical regions. Ecological Applications 10:95-114.
Bugmann, H.K.M., S.D. Wullschleger, D.T. Price, K. Ogle, D.F. Clark, and A.M. Solomon. 2001.
Comparing the performance of forest gap models in North America. Climatic Change 51:349-388.
Bunyavanich, A., C.P. Landrigan, A.J. McMichael, P.R. Epstein. 2003. The impact of climate
change on child health. Ambulatory Pediatrics 3(1): 44-52.
CCSP. 2003. About the US Climate Change Science Program, US Climate Change Science
Program, Suite 250, 1717 Pennsylvania Ave, NW, Washington, DC 20006. Tel: +12022236262.
Fax: +1 202 223 3065. Email: information@climatescience.gov. Web: www.climatescience.gov.
Webmaster: WebMaster@climatescience.gov, http://www.climatescience.gov/about/default.htm
CDC. 2000. El Nino Special Report: Could El Nino Cause an Outbreak of Hantavirus Disease in
the Southwestern United States? National Center for Infectious Diseases, Special Pathogens
Branch, All About Hantavirus. www.cdc.gov/ncidod/diseases/hanta/hps/noframes/elnino.htm .
-------
13. Synthesis 13-17
Ceulemans R, Mousseau M. 1994. Effects of elevated atmospheric CO2 on woody plants. New
Phytologist 127: 425-446.
Chivian, E. 2001. Environment and health: 7. Species loss and ecosystem disruption —the
implications for human health. CMAJ 164 (1):66-69.
Comins, H. N. and R. E. McMurtrie. 1993. Long-term response of nutrient-limited forests to CO2
enrichment: equilibrium behavior of plant-soil models. Ecological Applications 3: 666-681.
Cramer, W.P. and A.M. Solomon. 1993. Climatic classification and future distribution of global
agricultural land. Climate Research 3:97-110.
DeLucia, E.H., J.G. Hamilton, S.L. Naidu, R.B. Thomas, J.A. Andrews, A. Finzi, M. Lavine, R.
Matamala, J.E. Mohan, G.R. Hendrey, William H. Schlesinger. 1999. Net primary production of a
forest ecosystem with experimental CO2 enrichment. Science 284:1177-9.
Dixon, R.K., S. Brown, R.A. Houghton, A.M. Solomon, M.C. Trexlerand J. Wisniewski. 1994.
Carbon pools and flux of global forest ecosystems. Science 263:185-190.
Dixon,R.K., J.B. Smith, S. Brown, O. Masera, L.J. Mata, I. Buksha. 1999. Simulations of forest
system response and feedbacks to global change: experiences and results from the U.S.
Country Studies Program. Ecological Modeling 122:289-305.
Eaton, J.G. and R.M. Scheller. 1996. Effects of climate warming on fish thermal habitat in
streams of the United States. Limnol. Oceanogr. 41:1109-1115.
Eaton, J.G., J.H. McCormick, B.E. Goodno, D.G. O'Brien, H.G. Stefany, M. Hondzo, and R.M.
Scheller. 1995. A field information-based system for estimating fish temperature tolerances.
F/sfteries 20(4):10-18.
EPA. 2003. Environmental Protection Agency 2004 Annual Performance Plan and Congressional
Justification. Inside EPA, February 14, 2003. http://insideepa.com.
EPA/NOAA. 1992. Global Change Database: Global Ecosystems Database, CD Disk A., Nat.
Geophys. Data Center, Boulder CO.
EPA/NOAA. 1993. Global Change Database: Global Ecosystems Database, CD Disk B., Nat.
Geophys. Data Center, Boulder CO.
Epstein, P.R. 2001. Climate change and emerging infectious diseases. Microbes and Infection
3(9): 747-754.
Etterson, J.R and R.G. Shaw. 2001. Constraint to adaptive evolution in response to global
warming. Science 294:151-154.
Evolution Markets. 2002. One of the World's largest carbon sequestration projects commences
operations. Press release retrieved January 10, 2003 from http://www.evomarkets.com
Falkowski, P., R. J. Scholes, E. Boyle, J. Canadell, D. Canfield, J. Elser, N. Gruber, K. Hibbard,
P. Hb'gbert, S. Linder, F. T. Mackenzie, B. Moore III, T. Pedersen, Y. Rosenthal, S. Seitzinger, V.
Smetacek, W. Steffan. 2000. The global carbon cycle: A test of our knowledge of Earth as a
system. Science 290:291 -296.
-------
13. Synthesis 13-18
Felzer, B.S., D. W. Kicklighter, J. M. Melillo, C. Wang, Q. Zhuang, and R.G. Prinn. 2002. Ozone
effects on net primary production and carbon sequestration in the conterminous United States
using a biogeochemistry model. MIT Joint Program on the Science and Policy of Global Change,
Report No. 90, November 2002. Joint Program on the Science and Policy of Global Change, MIT
E40-271, 77 Massachusetts Avenue, Cambridge MA 02139-4307 (USA), Fax: (617) 253-9845, E-
mail: globalchange@mi t .edu,Web site: http://mit.edu/globalchange/
Finzi, A.C., E.H. DeLucia, J.G. Hamilton, D.D. Richterand W.H. Schlesinger. 2002. The nitrogen
budget of a pine forest under free airCO2 enrichment. Oecologia 132: 567-578.
Fowler, D., J. N. Cape, M. Coyle, C. Flechard, J. Kuylenstierna, K. Hicks, D. Derwent, C.
Johnson, D. Stevenson. 1999. The global exposure of forests to air pollutants. Water, Air, and
Soil Pollution 116:5-32.
Gill, R. A., H. W. Polley, H. B. Johnson, L. J. Anderson, H. Maherali, and R. B. Jackson. 2002.
Nonlinear grassland responses to past and future atmospheric CO2. Nature 417:279-282.
Gitay, H., A. Suarez, R. T.Watson, and D. J. Dokken (eds.). 2002. Climate Change and
Biodiversity. Technical paper of the Intergovernmental Panel on Climate Change (IPCC), ISBN:
92-9169-104-7, pp 77+ iv.
Gleick, P.H. 2002. Water: The Potential Consequences of Climate Variability and Change for the
Water Resources of the United States. The Report of the Water Sector Assessment Team of the
National Assessment of the Potential Consequences of Climate Variability and Change, for the
U.S. Global Change Research Program. Pacific Institute for Studies in Development,
Environment, and Security, 654 13th Street, Preservation Park, Oakland, CA 94612. 151pp.
Global Change Research Act. 1990. United States of America, Public Law 101-606(11/16/90) 104
Stat. 3096-3104. http://www.gcrio.org/gcact1990.shtml
Haines, A, A.J. McMichael, and P.R. Epstein. 2000. Global climate change and health. CHAJ
163:729-64.
Hornberger et a/., 2001. A Plan for a New Science Initiative on the Global Water Cycle
(Washington, D.C., US Global Change Research Program).
Houghton R. A., J.L. Hackler, and K.T. Lawrence. 1999. The U.S. Carbon Budget: Contributions
from Land-Use Change. Science 285:574-578.
Hurtt, G.C., S.W. Pacala, P.R. Moorecroft, J. Caspersen, E. Shevliakova, R.A. Houghton, B.
Moore III. 2002. Projecting the future of the U.S. carbon sink. Proc. Nat. Acad. Sci. 99:1389-1394.
IPCC. 1995. Climate Change 1995: IPCC Second Assessment. A report of the Intergovernmental
Panel on Climate Change, Synthesis of Scientific-Technical Information Relevant to Interpreting
Article 2 of the UNFCCC- Summaries for Policymakers of the three Working Group reports. IPCC,
Geneva, Switzerland, pp 64. http://www.ipcc.ch/pub/reports.htm
IPCC. 2001 a. Climate Change 2001: Synthesis Report. A Contribution of Working Groups I, II,
and III to the Third Assessment Report of the Integovernmental Panel on Climate Change
[Watson, R.T. and the Core Writing Team (eds.)]. Cambridge University Press, Cambridge,United
Kingdom, and New York, NY, USA, 398 pp.
-------
13. Synthesis 13-19
IPCC. 2001 b. Climate Change 2001: Impacts, Adaptation and Vulnerability. Contribution of
Working Group II to the Third Assessment Report of the Intergovernmental Panel on Climate
Change, J.J. McCarthy, O.F. Canziani, N. A. Leary, D.J. Dokken, and K..S. White (eds.),
Published for the Intergovernmental Panel on Climate Change by GRID Arendal, Arendal,
Norway. Retrieved http://www.grida.no/climate/ipcc tar/wg2/001 .htm
IRRI. 1993. The Rice Almanac 1993-95. International Rice Research Institute, Los Banos, The
Phillipines, 142pp.
IRRI 2002. Rice facts. The International Rice Research Institute. http://www.irri.org/Facts
Jeffords, J. 2003. Senator Jeffords introduces Clean Power Act of 2003. February, 12. Retrieved
February 14,2003, from http://www.senate.gov/~ieffords/press/
Johnson, D.W., R.B. Thomas, K.L. Griffin, D.T. Tissue, J.T. Ball, B.R. Strain, and R.F. Walker.
1998. Effects of carbon dioxide and nitrogen on growth and nitrogen uptake in ponderosa pine
and loblolly pine. J. Environmental Quality 27:414-425.
Johnson, M.G., D.L. Phillips, D.T. Tingey and M.J. Storm. 2000. Effects of elevated CO2, N-
fertilization, and season on survival of ponderosa pine fine roots. Can. J. For. Res. 30:220-228.
Kern, J.S. and M.G. Johnson. 1993. Conservation Tillage Impacts on National Soil and
Atmospheric Carbon Levels. So;7 Science Society of America Journal 57:200-210.
King, G. A. and R. P. Neilson, 1992. The transient response of vegetation to climate change: a
potential source of CO2 to the atmosphere. Water, Air, and Soil Pollution 64:365-383.
Kirilenko, A. P. and A. M. Solomon. 1998. Modeling dynamic vegetation response to rapid
climate change using bioclimatic classification. Climatic Change 38:15-49.
Knapp, A.K., P.A. Fay, J.M. Blair, S.L. Collins, M.D. Smith, J.D. Carlisle, C.W. Harper, B.T.
Danner, M.S. Lett, J.K. McCarron. 2002. Rainfall variability, carbon cycling, and plant species
diversity in a mesic Grassland. Science 298:2202-5.
Koren, H.S. and M. Utell. 1997. Asthma and the environment. Environ. Health Perspect.
105:534-7.
Lee, J.J., D.L. Phillips, and R.F. Dodson. 1996. Sensitivity of the U.S. Corn Belt to climate
change and elevated CO2: II. Soil erosion and organic carbon. Agricultural Systems 52: 503-
521.
Leemans, R. and A.M. Solomon. 1993. The potential change in yield and distribution of the
earth's crops under a warmed climate. Climate Research 3:79-96.
Lettenmaier, D. P., K. L. Brettmann, L. W. Vail, S. B. Yabusaki, and M. J. Scott. 1992. Sensitivity
of Pacific Northwest water resources to global warming. The Northwest Environmental Journal
8:265-283.
Lettenmaier, D.P. and D.P. Sheer. 1991. Climatic sensitivity of California water resources. J.
Water Resources Planning and Management (117)1: 108-125.
-------
13. Synthesis 13-20
Lewis, J.D., D.M. Olszyk and D.T. Tingey. 1999. Seasonal patterns of photosynthetic light
response in Douglas-fir seedlings subjected to elevated atmospheric CO2 and temperature. Tree
Physiol. 19:243-252.
Lewis, J.D., M. Lucash, D. Olszyk and D.T. Tingey. 2001. Seasonal patterns of photosynthesis in
Douglas fir seedlings during the third and fourth year of exposure to elevated CO2 and
temperature. Plant, Cell Environ. 24:539-548.
Lin, G., J.R. Ehleringer, P.T. Rygiewicz, M.G. Johnson, and D.T. Tingey. 1999. Elevated CO2 and
temperature impacts on different components of soil CO2 effluxes in Douglas-fir terracosms.
Global Change Biology 5:157-168.
Lin, G., P.T. Rygiewicz, J.R. Ehleringer, M.G. Johnson and D.T. Tingey. 2001. Time-dependent
responses of soil CO2 efflux to elevated atmospheric [CO2] and temperature treatments in
experimental forest mesocosms. Plant and Soil 229:259-270.
Marks, D., G. A. King, and J. Dolph. 1993. Implications of climate change for the water balance of
the Columbia River Basin, USA. Climate Res. 2:203-213.
Martens, P., T. McMichael, and Jonathan Patz. 2001. Climate, global environmental change and
health: International scientific assessments begin to roll (Editors' foreword). Global Change and
Human Health 2:3-4.
Matthews, R.B., T. Horie, M.J. Kropff, D. Bachlelet,H.G. Centeno, J.C. Shin, S. Mohandass, S.
Singh, Z. Defeng, and M.H. Lee. 1995. A regional evaluation of the effect of future climate change
on rice production in Asia, pp. 95-139, In, Matthews, R.B., M.J. Kropff, D. Bachlelet, and H.H.
Van Laar, eds. Modeling the impact of climate change on rice production in Asia. CAB
International, Wallingford, U.K.
McKane, R. B., E. B. Rastetter, G. R. Shaver, K. J. Nadelhoffer, A. E. Giblin, J. A. Laundre, and
F. S. Chapin, III. 1997a. Climatic effects on tundra carbon storage inferred from experimental
data and a model. Ecology 78: 1170-1187.
McKane, R.B., D. Tingey, P.A. Beedlow, P.T. Rygiewicz, M.G. Johnson, J.D. Lewis. 1997b.
Spatial and temporal scaling of CO2 and temperature effects on Pacific Northwest forest
ecosystems. Amer. Assoc. Adv. Science Pacific Div. Abstracts 16(1):56.
McMichael and Githeko. 2001. Human Health. Chapter 9, Climate Change 2001: Impacts,
Adaptation and Vulnerability - Contribution of Working Group II to the Third Assessment Report of
IPCC, Pp 453-485. Cambridge University Press, Edinburgh, UK., http://www.cambridge.org
McMichael, T. 2001. Transitions in human health: surviving this millennium by learning from the
past one hundred millennia. Global Change and Human Health 2(1):76-77.
Morison, J.L. and D.W. Lawlor. 1999 Interactions between increasing CO2 concentration and
temperature on plant growth. Plant, Cell and Environment 22:659-682.
Moya, T. B., O. S. Namuco, L. H. Ziska, and D. Olszyk. 1998. Growth dynamics and genotypic
variation in tropical, field-grown paddy rice (Oryza sativa L.) in response to increasing carbon
dioxide and temperature. Global Change Biology 4:645-656.
Murphy, K. 2003. States Target Greenhouse Gases. Stateline.org, February 13. Retrieved
February 14 from http://www.stateline.org/
-------
13. Synthesis 13-21
National Assessment Synthesis Team. 2000. Climate Change Impacts on the United States: The
Potential Consequences of Climate Variability and Change, US Global Change Research
Program,Washington DC.
Nature. 2003. Climate come-uppance delayed. News feature, Nature 421:195.
Neilson, R.P. 1995. A model for predicting continental-scale vegetation distribution and water
balance. Ecological Applications 5:362-385.
Neilson, R.P. 1993b. Vegetation redistribution: A possible biosphere source of CO2 during
climatic change. Air Water and Soil Pollution 70:659-673.
Neilson, R.P. and D. Marks. 1994. A global perspective of regional vegetation and hydrological
sensitivities from climatic change. J. Veg. Sci. 5:715-730.
Neilson, R.P., 1993a. Transient ecotone response to climatic change: some conceptual and
modeling approaches. Ecological Applications 3:385-395.
Neilson, R.P., 1998. Simulated changes in vegetation distribution under global warming. Annex
C, pp. 439-456 IN Watson, R. T., M. C. Zinyowera, R. H. Moss and D. J. Dokken, eds., The
Regional Impacts of Climate Change. Cambridge Univ. Press, NY.
Neilson, R.P., G.A. King and G.Koerper. 1992. Toward a rule-based biome model. Landscape
Ecology 7:27-43.
Norby, R.J., S.D. Wullschleger, C.A. Gunderson, D.W. Johnson, and R. Ceulemans. 1999. Tree
responses to rising CO2 in field experiments: implications for the future forest. Plant, Cell and
Environment 22:683-714.
O'Carroll, C.M. 2002. Satellites vs. mosquitoes: tracking West Nile virus in the U.S. NASA,
Goddard Space Flight Center, http://www.gsfc.nasa.gov/topstory/20020204westnile.html
Ollinger, S.V., J.D. Aber, P.B. Reich and R.J. Freuder. 2002. Interactive effects of nitrogen
deposition, tropospheric ozone, elevated CO2 and land use history on the carbon dynamics of
northern hardwood forests. Global Change Biology 8:545.
Olszyk, D., C. Wise, E. Van Ess, and D. Tingey. 1998. Elevated temperature but not elevated
CO2 affects stem diameter and height of Douglas-fir seedlings: results over three growing
seasons. Canadian Journal of Forest Research 28:1046-1054.
Olszyk, D.M., H.G.S. Centeno, L.H. Ziska, J.S.Kern, and R.B. Matthews. 1999. Global Change,
Rice Productivity and Methane Emissions: Comparison of Predicted and Experimental Results.
Agricultural and Forest Meteorology 9,87-101.
Olszyk, D.M., M. G. Johnson, D.L. Phillips, R. Seidler, D.T. Tingey, and L.S. Watrud. 2001.
Interactive effects of O3 and CO2 on a ponderosa pine plant/litter/soil mesocosm. Environ. Pollut.
115,447-462.
Olszyk, D.M., M.G. Johnson, D. Tingey, P.T. Rygiewicz, C. Wise, E. VanEss, A. Bensen and M.
Storm. 2003. Whole-seedling biomass allocation, leaf area, and tissue chemistry for Douglas-fir
exposed to elevated CO2 and temperature for 4 years. Can. J. For. Res. 33:269-278.
-------
13. Synthesis 13-22
Orem, R., D.S. Ellsworth, K.H. Johnson, N. Phillips, B.E. Ewers, C. Majer, H. McCarthy, G.
Hendrey, S.G. McNulty, G.G. Katul. 2001. Soil fertility limits carbon sequestration by forest
ecosystems in a CO2-enriched atmosphere. Nature 411:469-472.
Patrick, K. 2003. Emissions-trading group set to launch. The Globe and Mail, March 31, 2003
retrieved April 1, 2003 from http://www.theglobeandmail.com/
Patz, J.A. 2001. Public health risk assessment linked to climatic and ecological change. Human
and Ecological Risk Assessment 7(5): 1317.
Pelley, J. 2003. Taking credit for forest carbon sinks. February 1, 2003 / Environmental Science
and Technology, pp 59-63.
Percy, K E., C.S. Awmack, R.L. Lindroth, M.E. Kubiske, B. J. Kopper, J.G. Isebrands, K.S.
Pregitzer, G.R. Hendrey, R.E. Dickson, D.R. Zak, E. Oksanen, J. Sober, R. Harrington, and D.F.
Karnosky. 2002. Altered performance of forest pests under atmospheres enriched by CO2 and
03. Nature 420:403-7.
Phillips, D.L., D. White, and C.B. Johnson. 1993. Implications of climate change scenarios for soil
erosion potential in the United States. Land Degradation and Rehabilitation 4: 61-72. Poff, N. L,
and J. D. Allan. 1995. Functional organization of stream fish assemblages in relation to
hydrological variability. Ecology 76:606-627.
Phillips, D.L., D.T. Tingey, M.G. Johnson, C.E. Catricala, and T.L. Hoyman. 2002. Effects of
elevated CO2 on fine root biomass, production, and turnover in a Mojave Desert ecosystem: a
FACE study. Manuscript in preparation.
Phillips, D.L., J.J. Lee, and R.F. Dodson. 1996. Sensitivity of the U.S. Corn Belt to climate change
and elevated CO2: I. Corn and soybean yields. Agricultural Systems 52: 481-502.
Poff, N. L., and J. D. Allan. 1995. Functional organization of stream fish assemblages in relation
to hydrological variability. Ecology, 76: 606-627.
Prentice, I.C., W. Cramer, S.P. Harrison, R. Leemans, R.A. Monserud, and A.M. Solomon. 1992.
A global biome model based on plant physiology and dominance, soil properties and climate. J. of
Biogeography 19:117-134.
Pushnik, J.C., R.S. Demaree, J.L. Houpis, W.B. Flory, S.M. Bauer,and P.O. Anderson. 1995. The
effects of elevated carbon dioxide on a Sierra-Nevada dominant species: Pinus ponderosa. J.
Biogeography 22:249-254.
Rastetter E.B., Ryan M.G., Shaver G.R., Melillo J.M., Nadelhoffer K.J., Hobble J.E., AberJ.D.
1991. A general biogeochemical model describing the responses of the C and N cycles in
terrestrial ecosystems to changes in CO2, climate and N deposition. Tree Physiology 9:101-126.
Roberts, C.M., C.J. McClean, J.E.N. Veron, J.P. Hawkins, G.R. Allen, D.E. McAllister, C.G.
Mittermeier, F.W. Schueler, M. Spalding, F. Wells, C. Vynne, T.B. Werner. 2002. Marine
biodiversity hotspots and conservation priorities for tropical Reefs. Science 295:1280-4.
Rodo, Xavier, Mercedes Pascual, George Fuchs, and A. S. G. Faruque. 2002. ENSO and
cholera: A nonstationary link related to climate change? Proc. Nat'l Academy of Sciences
99(20):12901-12906.
-------
13. Synthesis 13-23
Rygiewicz, P.T., M.G. Johnson, M.J. Storm, D.T. Tingey and L. Ganio. 1997. Lifetime and
temporal occurrence of ectomycorrhizae on ponderosa pine (Pinus ponderosa Laws.) seedlings
grown under varied atmospheric CO2 and nitrogen levels. Plant and Soil 189:275-287.
Rypdal, K. and R. Baritz. 2002. Estimating and managing uncertainties in order to detect
terrestrial greenhouse gas removals. CICERO Working Paper 2002:07. Center for International
Climate and Environmental Research, P.O. Box 1129 Blindern N-0318, Oslo, Norway, Phone:
+47 22 85 87 50,Fax: +47 22 85 87 51, E-mail: admin@cicero.uio.no Web: www.cicero.uio.no
SAB. 1990. Reducing Risk: Setting Priorities and Strategies for Environmental Protection.
Science Advisory Board, United States Environmental Protection Agency, SAB-EC-90-021.
Samuelsohn, D. 2003. Inhofe says Democrats may have the votes to pass CO2 curbs.
Environment & Energy Daily, February 12, 2003.
Santavy, D. L., J. K. Summers, V. D. Engle, and L. C. Harwell (2002). The condition of the coral
reefs in South Florida using coral disease and casual bleaching as an indicator. Environmental
Monitoring and Assessment (in press).
Santavy, D. L., E. Mueller, E.G. Peters, L. MacLaughlin , J. W. Porter, K. L. Patterson and J.
Campbell 2001. Quantitative assessment of coral diseases in the Florida Keys: strategy and
methodology. Hydrobiologia 460:39-52.
Schiermeier, Q. 2003. Cycle studies see carbon sinks rise to prominence. Nature 414:384.
Schimel, D., J. Melillo, H. Tian, A.D. McGuire, D. Kicklighter, T. Kittel, N. Rosenbloom, S.
Running, P. Thornton, D. Ojima, W. Parton, R. Kelly, M. Sykes, R. Neilson, and B. Rizzo. 2000.
Contribution of increasing CO2 and climate to carbon storage by ecosystems in the United States.
Science 287:2004-6.
Schimel, D.S., J. I. House, K. A. Hibbard, P. Bousquet, P. Ciais, P. Peylin, B. H. Braswell, M. J.
Apps, D. Baker, A. Bondeau, J. Canadell, G. Churkina, W. Cramer, A. S. Denning, C. B. Field, P.
Friedlingstein, C. Goodale, M. Heimann, R. A. Houghton, J. M. Melillo, B. Moore III, D.
Murdiyarso, I. Noble, S. W. Pacala, I. C. Prentice, M. R. Raupach, P. J. Rayner, R. J. Scholes, W.
L. Steffen & C. Wirth. 2001. Recent patterns and mechanisms of carbon exchange by terrestrial
ecosystems. Nature 414:169-172.
Schlesinger, W. H. and J. Lichter. 2001. Limited carbon storage in soil and litter of experimental
forest plots under increased atmospheric CO2. Nature 411:466-469.
Scholes, R.J. and I.R. Noble. 2001. Storing Carbon on Land. Science 294:1012-13.
Sedjo, R. A. and A. M. Solomon, 1989. Climate and forests, pp. 105-119 IN Rosenberg, N. J., W.
E. Easterling, P. R. Crosson, and J. Darmstadter, Eds., Greenhouse Warming: Abatement and
Adaptation. Resources for the Future, Washington, D.C.
Shaw, M.R., E.S. Zavaleta, N.R. Chiariello, E.E. Cleland, H.A. Mooney, and C.B. Field. 2002.
Grassland responses to global environmental changes suppressed by elevated CO2. Science
298:1987-90.
Sinokrot, B.A., H.G. Stefan, J.H. McCormick, and J.G. Eaton. 1995. Modeling of climate change
effects on stream temperatures and fish habitats below dams and neargroundwater inputs.
Climatic Change 30:181-200.
-------
13. Synthesis 13-24
Smith, J.B. and D. Tirpak. 1989. The Potential Effects Of Global Climate Change On The United
States. Report to Congress by the United States Environmental Protection Agency, Office of
Policy, Planning and Evaluation, Office of Research and Development, (PM-221) EPA-230-05-89-
050. Retrieved May 28, 2003 from http://vosemite.epa.gov/oar/globalwarming.nsf/
Smith, S.D., T.E Huxman, S.F. Zitzer, T.N. Charlet, D.C. Housman, J.S. Coleman, L.K.
Fenstermaker, J.R. Seemann, and R.S. Nowak. 2000. Elevated CO2 increases productivity and
invasive species success in an arid ecosystem. Nature 408: 79-82.
Solomon, A.M. 1996. Potential responses of global forest growing stocks to changing climate,
land use and wood consumption. Commonwealth. For. Rev. 75:65-75.
Solomon, A.M. 1997. Natural migration rates of trees: Global terrestrial carbon cycle implications.
Pp. 455-468 IN Huntley, B., W.P. Cramer, A.V. Morgan, H.C. Prentice and J.R.M. Allen. Past and
future rapid environmental changes: The spatial and evolutionary responses of terrestrial biota.
Springer-Verlag, NY
Solomon, A.M. and P.J. Bartlein. 1992. Past and future climate change: Response by mixed
deciduous-coniferous forest ecosystems in northern Michigan. Canadian Journal of Forest
Research 22:1727-1738.
Solomon, A.M. and A.P. Kirilenko. 1997. Climate change and terrestrial biomass: What if trees do
not migrate? Global Ecol. and Biogeogr. Let. 6:139-148.
Solomon, A.M. and R. Leemans. 1997. Boreal forest carbon stocks and wood supply: Past,
present and future responses to changing climate, agriculture and species availability. J.
Agricultural and Forest Meteorology 84:137-151.
Solomon, A.M., I.C. Prentice, R. Leemans and W.P. Cramer. 1993. The interaction of climate
and land use in future terrestrial carbon storage and release. Water, Air, and Soil Pollution
70:595-614.
Solomon, A.M. and D.C. West. 1993. Evaluation of stand growth models for predicting
afforestation success during climatic warming at the northern limit of forests, p. 167-188 IN R.
Wheelon, ed. Forest Development in Cold Regions. Proceedings, NATO Advanced Research
Workshop. Plenum Publ. Corp., NY.
Solomon, A.M., N.H. Ravindranath, R.B. Stewart, S. Nilsson and M. Weber. 1996. Wood
production under changing climate and land use. Chapter 15, pp. 487-510. IN Climate Change
1995: Impacts, Adaptations and Mitigation of Climate Change. Working Group II, Second
Assessment Report, Intergovernmental Panel on Climate Change (IPCC), Cambridge University
Press, Cambridge UK.
Speidel J. J. 2000. Environment and health: 1. Population, consumption and human health.
CMA/163(5):551-6.
Stefan, H. G., and E. B. Preud'homme. 1993. Stream temperature estimation from air
temperature. Water Resour. Bull. 29:27-45.
Stefan, H.G., M. Hondzo, X. Fang, J.G. Eaton, and J.H. McCormick. 1996. Simulated long-term
temperature and dissolved oxygen characteristics of lakes in the north-central United States and
associated fish habitat limits. Limnol. Oceanogr. 41:1124-1135.
-------
13. Synthesis 13-25
Surano, K.A., P.P. Daly, J.L. Houpis, J.H. Shinn, J.A. Helms, R.J. Palassou, and M.P. Costella.
1986. Growth and physiological responses of Pinus ponderosa Dougl. ex P. Laws, to long-term
elevated CO2 concentrations. Tree Physiology 2:243-259.
Tingey, D.T., M.G. Johnson, D.L. Phillips, D.W. Johnson and J.T. Ball. 1996b. Effects of elevated
CO2 and nitrogen on the synchrony of shoot and root growth in ponderosa pine. Tree Physiology
16:905-914.
Tingey, D. T., J. A. Laurence, J. A. Weber, J. Greene, W. E. Hogsett, S. Brown, and E. H. Lee.
2001. Elevated CO2 and temperature alter the response of Pinus ponderosa to ozone: a
simulation analysis. Ecological Applications 11:1412-1424.
Tingey, D.T., B.D. McVeety, R. Waschmann, M.G. Johnson, D.L. Phillips, P.T. Rygiewicz and
D.M. Olszyk. 1996a. A versatile sun-lit controlled-environment facility for studying plant and soil
processes. J. Environ. Quality 25:614-625.
Tingey, D.T., D.L. Phillips, M.G. Johnson, M.J. Storm and J.T. Ball. 1997. Effects of elevated CO2
and N-fertilization on fine root dynamics and fungal growth in seedling Pinus ponderosa.
Environmental Experimental Botany 37:73-83.
U of Wisconsin. 2002. Research Shows How Pollutants Affect Tree Growth. University Of
Wisconsin-Madison press release in ScienceDaily Magazine, 13 June 2002, retrieved 23 May
2003 from http://www.sciencedaily.com
U.S. Department of State. 2002. U.S. Climate Action Report 2002, Washington, D.C., May 2002.
UNEP. 2000. The Montreal Protocol on Substances that Deplete the Ozone Layer. Published by
the Secretariat for The Vienna Convention for the Protection of the Ozone Layer & The Montreal
Protocol on Substances that Deplete the Ozone Layer. United Nations Environment Programme,
PO Box30552, Nairobi, Kenya, website: http://www.unep.org/ozone, ISBN: 92-807-1888-6.
UNFCCC. 2002. A guide to the climate change convention and its Kyoto Protocol. The United
Nations Framework Convention on Climate Change, the Climate Change Secretariat, Bonn,
http://unfccc.int/resource/convkp.html
Vitousek, Peter M., Harold A. Mooney, Jane Lubchenco, Jerry M. Melillo. 1997. Human
Domination of Earth's Ecosystems. Science 277:494-499.
Watson, R.T. and A.J. McMichael. 2001. Global climate change -the latest assessment: does
global warming warrant a health warning? Global Change & Human Health 2, (1):64-75.
Wayne, P.W. 1999. Production of allergenic ragweed pollen is increased in CO2 -enriched
atmospheres. Harvard Medical School Quarterly Review Vol.1, No.1, November.
Weerakoon, W. M., D.M. Olszyk, and D.N. Moss. 1999. Effects of Nitrogen Nutrition on
Responses of Rice Seedlings to Carbon Dioxide. Agriculture Ecosystems and Environment 72, 1 -
8.
World Bank. 2002. World Development Report 2003. The International Bank for Reconstruction
andDevelopment/The World Bank 1818 H Street, N.W., Washington, D.C. 20433, U.S.A. ISBN
0-8213-5187-7.
-------
13. Synthesis 13-26
Ziska, L.H., and F.A. Caulfield. 2000. The potential influence of rising atmospheric carbon dioxide
(CO2) on public health: Pollen production of common ragweed as a test case. World Resources
Review 12:449-57.
Ziska, L.H., W. Weerakoon, O.S. Namuco, and R. Pamplona. 1996. The influence of nitrogen on
the elevated C02 response in field-grown rice. Australian Journal of Plant Physiology 23,45-52.
Zizka, L.H., D.E. Gebhard, D.A. Frenz, S. Faulkner, B.D. Singer, and J.G. Straka. 2003. Cities as
harbingers of climate change: Common ragweed, urbanization, and public health. J. Allergy and
Clinical Immunology 111 (2): 290-295.
------- |