Effects of Chronic Exposures to
Gaseous Pollutants on Primary
Production Processes
Photochemical Oxidant Impact on
Mediterranean and Temperate Forest
Ecosystems: Real and Potential
Effects
2
John M. S k e l l y
Abstract: Photochemical oxidants Cprimarily ozone) a s
a i r p o l l u t a n t s pose a more s e r i o u s problem t o f o r e s t s of
t h e United S t a t e s than any o t h e r s i n g l e a i r p o l l u t a n t .
Temperate and Mediterraean f o r e s t s elsewhere have most l i k e l y
been s i m i l a r l y impacted and c u r r e n t i n v e s t i g a t i o n s of such
e f f e c t s a r e being pursued. Ozone Land i t s photochemically
r e a c t i v e precursors) has been demonstrated t o occur a t cons i d e r a b l e d i s t a n c e s downwind of major urban sources. Ozone
has induced p e r t u b a t i o n s t o vegetation over l a r g e a r e a s and
has t h e r e f o r e impacted innumerable and d i v e r s e f o r e s t ecosystems. Direct i n j u r y due t o ozone has been documented t o
occur on numerous i n d i v i d u a l f o r e s t vegetation s p e c i e s but
d i r e c t a l t e r a t i o n s of f o r e s t ecosystems a s r e l a t e d t o ozone
induced e f f e c t s have only been e x t e n s i v e l y documented i n t h e
San Bernardino Mountains of C a l i f o r n i a ; t o a l e s s e r degree
s i m i l a r s t u d i e s have been done i n t h e Blue Ridge Mountains
of V i r g i n i a . Due t o t h e c u r r e n t s u l f u r dioxide (SO?)
problems confronting European f o r e s t s and due t o t h e planned
increased u t i l i z a t i o n of f o s s i l f u e l s i n much of t h e North
American Continent, t h e influence of ozone i n combination
with SO2 must be f u l l y considered. The influence of o t h e r
photochemical oxidants such a s nitrogen oxides and peroxya c e t y l n i t r a t e on f o r e s t vegetation has remained r e l a t i v e l y
unknown.
I
The d i f f i c u l t y of understanding t h e r e a l and
p o t e n t i a l impact of a i r p o l l u t a n t s such a s ozone
(03) on i n d i v i d u a l s p e c i e s within any given p l a n t
community a s compared t o r e l a t i n g d i r e c t o r
i n d i r e c t e f f e c t s of OT, on e n t i r e and complex
p r e s e n t e d a t t h e Symposium on E f f e c t s of A i r
P o l l u t a n t s on Mediterranean and Temperate Forest
Ecosystems, June 22-27, 1980, Riverside,
C a l i f o r n i a , U.S.A.
Professor, Plant Pathology and D i r e c t o r , Labor a t o r y f o r A i r P o l l u t i o n Impact t o Agriculture and
Forestry, V i r g i n i a Polytechnic I n s t i t u t e and
S t a t e University, Blacksburg, VA 24060.
f o r e s t ecosystems must be s e v e r a l o r d e r s of magnitude i n d i f f e r e n c e . Several s t u d i e s have r e l a t e d
dose e f f e c t s t o f u l l - s i b c r o s s e s of various f o r e s t
t r e e s p e c i e s but such s t u d i e s have l i s t e d a
s e r i e s of caveats f o r t h e r e a d e r t o consider
while i n t e r p r e t i n g even t h e most b a s i c r e s u l t s
obtained. Such caveats have taken i n t o account
p o s s i b l e unknown e f f e c t s due t o exposure chamber
systems, physical and b i o t i c f a c t o r i n t e r a c t i o n s ,
and/or r e l a t e d monitoring and d a t a a n a l y s i s
methodologies. A s r e s e a r c h advances from s t u d i e s
of f u l l - s i b crossed p l a n t m a t e r i a l s through h a l f s i b (open p o l l i n a t e d , maternal l i n e s ) through
s p e c i e s and f o r e s t types, t o f o r e s t communities
and complex f o r e s t ecosystems, t h e number of
influencing v a r i a b l e s t o be considered while
i n t e r p r e t i n g t h e r e s u l t s becomes d i s p r o p o r t i o n a l
and d i f f i c u l t t o comprehend.
Most s t u d i e s t h a t have d e a l t d i r e c t l y with 03
e f f e c t s t o any given p l a n t s p e c i e s have not
considered t h e e f f e c t s of p o l l u t a n t combinations
even a t h i g h e r doses. Under n a t u r a l conditions,
f o r e s t ecosystems a r e impacted by a m u l t i p l i c i t y
of atmospheric d e p o s i t i o n s including anthropogenic
p o l l u t a n t s i n gaseous, d r y , and wet formulations.
In a d d i t i o n such d e p o s i t i o n s do n o t occur s i n g l y
a t doses s i m i l a r t o those reported f o r various
exposure chamber s t u d i e s , e . g . , 1-8 hours p e r day
f o r 5 days/week f o r 10 weeks, but r a t h e r t h e y
occur a t low c o n c e n t r a t i o n s , i n various and
c o n s t a n t l y changing combinations and over
extended exposure periods. Thus, ecosystem
s t u d i e s t h a t have n o t considered even t h e s e few
f a c t o r s must be considered of l i m i t e d value f o r
any i n t r i n s i c o r e x t r i n s i c i n t e r p r e t a t i o n .
I t i s a well known concept t h a t a i r p o l l u t a n t
i n c i t e d p e r t u b a t i o n s lead t o s i m p l i f i c a t i o n of
f o r e s t ecosystems. Continued exposures t o SO2
complexes have r e s u l t e d i n s i m p l i f i c a t i o n and
r e v e r s a l o f once f o r e s t e d land t o grassland
communities o r i n some severe c a s e s even t o
s t e r i l i t y of t h e s o i l and accompanying erosion.
However, such severe impacts due t o 0 p o l l u t i o n
have n o t been r e p o r t e d t o occur w i t h t h e p o s s i b l e exception of major f o r e s t v e g e t a t i o n s p e c i e s
d e c l i n e i n t h e San Bernardino Mountains of
Southern C a l i f o r n i a . The complexity of such
s i m p l i f i c a t i o n s c e n a r i o s involving minor changes
i n r e c e p t o r p l a n t physiology and r e l a t e d longterm e f f e c t s on competitive a b i l i t i e s such a s
reproduction, n u t r i e n t c y c l i n g , and r e l a t e d food
chain e v e n t s h a s n o t been well documented.
The main purpose of t h i s paper i s n o t t o p r e s e n t a review of l i t e r a t u r e p e r t a i n i n g t o ozone
impact t o f o r e s t s p e c i e s and r e l a t e d ecosystems.
Several e x c e l l e n t reviews of t h e s u b j e c t have
been p r e v i o u s l y published and due t o t h e s e comprehensive up-to-date a n a l y s i s of t h e t o p i c any
f u r t h e r review would r e s u l t i n a redudancy i n
t h e l i t e r a t u r e (Miller 1973; M i l l e r and McBride
1975; Brown and o t h e r s 1979 and Kozlowski 1980).
Rather t h i s symposium paper w i l l attempt t o r e l a t e
t h e s e review a r t i c l e s and accompanying new l i t e r a t u r e i n t o an a n a l y s i s of t h e r e a l and p o t e n t i a l
long-term e f f e c t s of ozone on f o r e s t ecosystems.
A d d i t i o n a l l y , an e f f o r t w i l l be made t o r e l a t e
e x i s t i n g l i t e r a t u r e i n t o suggestions f o r f u t u r e
c o n s i d e r a t i o n of ecosystem impacts i n t o t h e
National Ambient A i r Q u a l i t y Standards.
BACKGROUND AND ANTHROPOGENIC CONCENTRATIONS
OF OXIDANTS IN FOREST SITUATIONS
A comprehensive review of ozone and o t h e r
ph'o'tochemical oxidants has been published by t h e
National Academy of Sciences (NAS 1977); a
r e c e n t compilation of papers has a l s o been
published (USEPA 1977b). These c o l l e c t i v e s e t s
of papers have provided an e x c e l l e n t review of
t h e o r i g i n , chemistry, t r a n s p o r t , and atmospheric
modeling of t h e s e p o l l u t a n t s .
Background Concentrations
Ozone is a n a t u r a l l y occurring component of
t h e E a r t h ' s atmosphere and concentrations of
0.03-0.05 ppm 03 a r e g e n e r a l l y considered t o be
normal due t o mixing v i a t h e s t r a t o s u h e r i c t r a n s p o r t e f f e c t (Corn and o t h e r s 1975) Cfig.1 ) .
ur,
/
photochemistry
Stratospheric
,-transport effect
Net decay, but effects
from long term
photochemistryand
regional input
\
Natural
photochemicalinput
Loss to ground
and aerosols
-Rural
(upwind)-
-Urban-
-Run1
(downwtnd)-
Figure I--The tropospheric ozone c y c l e .
Corn and o t h e r s 1975).
(from
The emission of oxidant forming p r e c u r s o r s such
a s oxides of n i t r o g e n and hydrocarbons i n t o t h e
lower atmosphere l e a d s t o t h e buildup of photochemically produced ozone and r e l a t e d peroxyacyln i t r a t e s [fig. 2) (NAS 1977).
Figure 2--The normal n i t r o g e n oxide p h y t o l y t i c
cycle [A) and t h e c y c l e a s a l t e r e d by t h e
a d d i t i o n of hydrocarbons leading t o increased
ozone concentrations (B) (from NAS 1977).
PAN has n o t been d e t e c t e d i n non-anthropogenic a l l y p o l l u t e d atmospheres but oxides of n i t r o gen do occur n a t u r a l l y i n t h e atmosphere and
concentrations of 0.02-0.10 ppm NOx have been
reported QNAS 1977). Brennan (Personal
communication) has reported a high PAN concentrat i o n i n t h e Eastern United S t a t e s of 10 ppb but
suggested o v e r a l l concentrations of PAN a r e
well below West Coast observations.
Anthropogenic Concentrations i n
Forested Areas
The long d i s t a n c e t r a n s p o r t of oxidant prec u r s o r s and ozone i n t o remote f o r e s t e d a r e a s has
been well documented (Miller and o t h e r s 1972;
Husar and o t h e r s 1977; Hayes and S k e l l y 1977;
and Cleveland and Kleiner 1975). Concentrations
of ozone above t h e c u r r e n t National Ambient A i r
Q u a l i t y Standard (NAAQS) of 0.12 ppm 03 one hour
average p e r 24-hour p e r i o d ; twice (2 days) p e r
year have r e c e n t l y been r e p o r t e d within t h e
f o r e s t e d a r e a s of Eastern (Skelly and o t h e r s 1979)
and mid-Western United S t a t e s (Wolff and o t h e r s
1977). Numerous r e p o r t s of high ozone concent r a t i o n s have been i s s u e d from t h e extensive San
Bernardino Mountain S t u d i e s (SBM) i n southern
C a l i f o r n i a (USEPA 1977a)
Major episodes of
ozone have developed s p o r a d i c a l l y over t h e summer
months of May through October i n e a s t e r n f o r e s t s
whereas a b e t t e r defined and s t a b l e oxidant season
e x i s t s i n t h e f o r e s t s of southern C a l i f o r n i a .
Galloway and S k e l l y (1978) defined a major a i r
p o l l u t i o n epidose i n J u l y 1977 t h a t involved
high ozone c o n c e n t r a t i o n s and t h e highest ever
recorded l a r g e and f i n e a e r o s o l SO4 c o n c e n t r a t i o n s
( f i g . 3, 4, and 5 ) .
CHAROLETTSVILLE
I
.
By comparing monitoring d a t a from t h e SBM
s t u d i e s with t h o s e of t h e Blue Ridge Mountain
S t u d i e s (BRM) a 3-4 f o l d g r e a t e r c o n c e n t r a t i o n
of ozone i s apparent i n t h e former over t h e
l a t t e r . Peaks of 0.20 t o 0.40 ppm O3 d a i l y onehour maximums have occurred i n t h e SBM f o r e s t
( f i g . 6) but t h e peak one-hour average ever
recorded i n t h e BRM a r e a has been 0.166 ppm O r .
Table 1 p r e s e n t s t h e monthly and peak one-hour
c o n c e n t r a t i o n s of ozone a s monitored a t v a r i o u s
s i t e s i n t h e Blue Ridge Mountains of V i r g i n i a .
PAN and NO have n o t been monitored i n e a s t e r n
f o r e s t s oi^the United S t a t e s and although d e t e c t e d
i n western f o r e s t s l i t t l e has been done t o d i s tinguish differences i n t h e i r respective effects
over t h o s e induced by ozone a l o n e ( f i g . 6 ) .
F
OXIDANT CONCENTRATIONS
Figure 4--Total s u l f a t e (mg/m3) a s monitored a t
C h a r l o t t e s v i l l e , VA during a i r p o l l u t i o n episode
of J u l y , 1977. Note buildup of J u l y 15-20 and
s i m i l a r sharp drop a s i n f i g u r e 3 on J u l y . (From
Galloway and S k e l l y 1978).
JULY, 1977
-SALT POND
MTN.
APPLE ORCHARD MTN.
ROCKY KNOB
........PINNACLES
--
I 2 3 4
5 6 7 8 9 10 11 12 13 14 15 16 17 18 192021 22232425262728293031
DATE
Figure 3--Oxidant c o n c e n t r a t i o n s a s monitored
a t s e v e r a l l o c a t i o n s i n t h e Blue Ridge and
Southern Appalachian Mountains of V i r g i n i a
d u r i n g J u l y , 1977. Daily averages (24 hours)
a r e i n d i c a t e d . Note peak period of J u l y 1520.
Figure 5(A)--A review of t h e Peaks of O t t e r a s
taken on a c l e a r day i n t h e Blue Ridge
Mountains. Photograph taken from Pine Tree
Overlook a t a d i s t a n c e of 11.6 KM from t h e
Peaks. (B) Photo taken on J u l y 20, 1977
during t h e worst a i r p o l l u t i o n s t a g n a t i o n
experienced i n V i r g i n i a . Same view a s
(A)
.
4 i
U
Norway; an a r e a s i t u a t e d c l o s e t o t h e c o a s t and
considered t o be normally unaffected by l o c a l
oxidant producing sources. The h i g h e s t 03 concent r a t i o n observed a t Rorvik was 0.20 ppm (August
1975) and i n Gothenburg t h e h i g h e s t 03 concentrat i o n was 0.13 pprn ( t a b l e 2 ) . They suggested
clockwise a i r movement a s a s s o c i a t e d with high
p r e s s u r e systems and long d i s t a n c e t r a n s p o r t from
Europe t o be r e l a t e d t o t h e ozone episodes.
Skarby (1979) reported t h a t ozone v a l u e s recorded
i n t h e summertime have been too high t o be cons i d e r e d a s normal background concentrations f o r
Swedish c o n d i t i o n s . During t h e summer of 1977
high O3 concentrations (0.20 ppm) were recorded
on 21 out of 92 days. She a l s o suggested longrange t r a n s p o r t t o be involved.
OZONEIpphml UV, OASIBI
TELEMETRY,ONCE HOURLY
1\
l a PAN ( p p b ) 5.C. ELECTRON
CAPTURE
From t h e s e few r e p o r t s it i s q u i t e obvious
t h a t ozone concentrations i n excess of t h e NAAQS
occur f r e q u e n t l y i n t h e temperate and Mediterranean f o r e s t s of t h e world.
Therefore, it i s
a l s o obvious t h a t t h e i n j u r y t h r e s h o l d s f o r
numerous p l a n t s p e c i e s have a l s o been f r e q u e n t l y
exceeded and t h e e f f e c t s of t h e s e exposure doses
a r e discussed below.
DAYS
Figure 6--Comparative d a i l y maximum hourly
averages f o r ozone, t o t a l oxidant, PAN, and NO2
a t Sky Forest August, 1974. (From USEPA 1977).
Ozone concentrations i n European f o r e s t s have
not been e x t e n s i v e l y i n v e s t i g a t e d but i n i t i a l
s t u d i e s i n d i c a t e t h a t ozone appears t o be episodal
i n i t s occurrence i n a manner s i m i l a r t o t h a t
experienced i n Eastern United S t a t e s . Grennfelt
(1979) r e p o r t e d on ozone concentrations a s monit o r e d a t Rorvik about 40 KM south of Gothenburg,
DIRECT EFFECTS TO FOREST SPECIES
The responses of any given f o r e s t ecosystem t o
Table I--Ozone concentrations (pprn) monitored a t Rocky Knob, Floyd Co., Va. (Blue Ridge Parkway)
and a t Pinnacles and Big Meadows, Madison Co., Va. (Shenandoah National Park).
Month
Rocky Knob
4onth
her.
Pinnacles
Peak Month
Hour Aver.
Aver.
Peak
Hour
Aver.
Rocky Knob
Month
Aver.
Peak
Hour
Aver.
Pinnacles
Month
Aver.
January
February
March
Apr i1
May
June
July
August
September
October
November
December
Average
f o r monit o r e d mo.
% i n n a c l e s s i t e moved 14 KM t o Big Meadow CSNP) May 1979.
o n l y 8 days out of t h e month were used f o r t h i s d a t a .
Peak
Hour
Aver.
'
Rocky Knob
Big Meadows
Month
Aver.
Month
Aver.
Peak
Hour
Aver.
1
Peak
Hour
Aver.
Table 2--The number of days with high ozone concentrations in Goth- enburg and Rsrvik, Norway 1972-1978 expressed as days with one hour mean of ozone exceeding indicated values (Grennfelt 1979). >0.08
-
Year
PPm
>0.10
-
>0.12
-
>0.15
-
PPm
PPm
PPm
Maxhourly
mean
(PP~)
Gothenburg 18
17
6
12
5
0
0
1
11
5
0
8
0.20
0.13
0.11
0.15
I
l~ncludesdata only until June 30, 1978. photochemical oxidants must be as a result of the
expression of direct effects to the individual
component species within that ecosystem. The
ability of scientific research to define those
direct effects to individuals and to relate such
defined effects to the whole has been limited.
Three terms have been used somewhat interchangeably to define these effects and for purposes of
this paper they shall be defined as:
Injury - the result of one or more deleterious
alterations of normal physiological processes as
manifested by the presence of chronic or acute visible symptoms and/or growth reductions (growth
reduction may be the only manifestation),.
Damage - injury that results in measurable
economic loss to specific crops e.g. reduced
height or radial increment growth of forest trees
resulting in reduced value of the commerical
forest. Impact - the total influence Qdetrimental or
beneficial) of air pollutants on all aspects of
the forest ecosystem including even minor shifts
towards reduced diversity of species, indirect
effects to watersheds and water quality, or direct effects to recreational values due to
reduced visibility at vistas or overlooks in
National Forests and Parks.
Extensive research has been justifiably done on specific forest species to better define the injury phase of this scenario of increasingly inclusive terminology. However, even within this type of problem definition research a larger endeavor has been made to define visible plant responses over the less easily measured physiolo- gical responses. The latter responses may actual- ly be of more importance to understanding the damage and impact phases of subsequent ecosystem deteriorations. Thus, three additional terms
emerge :
acute injury - involves expresion of clinical
symptoms leading to death of cells, tissues, organs, or entire plants and/or plant communities. Such injury is usually initiated by exposure to
high doses of pollutants (^concentration x <time)_ but may result from exposure to lower concentra- tions of pollutant over extended periods of time. chronic injury - involves non-lethal types of
clinical symptom expressions such as reduced
chlorophyll production and related pigmentation changes, and reduced growth rates. Such injury usually results from still lower dose exposures. functional injury - involves injury to the
functional efficiency of the plant as expressed by reduced growth or other expression of loss without the development of any other clinical symptoms, i.e. injury is only of a physiological and pre-clinical nature. Further visible symptoms do not develop. This form of injury is most difficult to define and measure and is the result of lowest dose exposures at predominantly near background concentrations of pollutants over extended periods of time. An attempt to define the current status of knowledge concerning these various forms of di- rect effects due to ozone has been presented in table 3. A more specific assessment of recent documented studies of chronic pollution effects as induced by all species of air pollutants at the ecosystem level has been presented by Kickert and Miller (1978). It is evident from table 3 that our knowledge of ozone effects following high dose exposures using artificial exposure systems for species level investigations is considered somewhat superior to that of the other levels of activity. However, when the abundance of plant species indigenous to a mixed hardwood-conifer forest *
ecosystem of the Northeastern United States is
taken into account our knowledge is very limited even for the clinical expression of symptoms by most species. Interpretation of available knowledge in the forest community and forest eco- system columns may be somewhat harsh but most probably realistic. A similar table as con- structed for sulfur dioxide related investigations would be much more optimistic thus attesting to the relative ease of working on predominant point sources of pollutants and their related effects. However, our knowledge of SO2 induced pertubations to forest ecosystems located at distances from various sources is relatively poor, e.g. knowledge of the subtle influences of S-related compounds to the productivity of Northeastern United States forests is virtually non-existent. Direct Effects to Forest Trees Davis and Wilhour (1976) have provided the most complete listing of woody plant sensitivities to sulfur dioxide and photochemical oxidants as Table 3--The current status of knowledge concerning ozone induced effects to Temperate and Mediterranean forest tree species, forest communities, and forest ecosystems. Com- parisons of the San Bernardino Mountain Studies (SBM) versus all other investigations (01) have been noted. Effect
Study Forest species2
I
Forest Communities Forest Ecosystems Injury overall 01
SBM moderate moderate poor moderate poor moderate acute 01 SBM abundant abundant moderate moderate poor moderate chronic 01
SBM moderate moderate poor moderate non-existent poor functional 01
SBM poor moderate non-existent moderate non-existent poor 01
SBM moderate abundant poor moderate non-existent poor non-existent moderate non-existent poor Damage Impact 1
In consultation by author with P. R. Miller Cpersonal communication). 2~stimatesin this column include responses obtained in fumigation chamber studies If such information was to be detected poor to non-existent descriptions would be appropriate for each category. ^ B definition
~ not applicable. derived from t h e i r review of United S t a t e s ,
Canadian, and European l i t e r a t u r e .
(c.
Eastern White Pine
The predominant f o r e s t t r e e s p e c i e s s t u d i e d
i n Eastern United S t a t e s has been e a s t e r n white
Pinus s t r o b u s L.; e x t e n s i v e l i t e r a t u r e reviews
by Gerhold (1977) and Nicholson (1977) a r e
a v a i l a b l e . I n t e r e s t i n t h i s s p e c i e s has
remained h i g h s i n c e t h e f i r s t discovery of i t s
somewhat unique s e n s i t i v i t y t o ozone by Berry
(1961). The response of t h i s s p e c i e s t o ozone
c o n c e n t r a t i o n s a s monitored i n t h e Blue Ridge
Mountains of V i r g i n i a ( t a b l e 1) has been t h e
s u b j e c t of s e v e r a l c u r r e n t i n v e s t i g a t i o n s . S k e l l y
and o t h e r s (1979) r e p o r t e d t h a t of 315 white p i n e s
surveyed by u s i n g a modified e v a l u a t i o n scheme a s
adapted from M i l l e r (1973) 17, 80, and 3 percent
were considered t o be t o l e r a n t , i n t e r m e d i a t e and
s e n s i t i v e , r e s p e c t i v e l y , t o ozone. Of t h e 315
t r e e s tagged i n 1977, 10 were reported t o have
d i e d following r e p e a t e d t y p i c a l c l i n i c a l symptoms
of oxidant induced i n j u r y . Subsequent r o o t excav a t i o n s and i s o l a t i o n of fungi has yielded
V e r t i c i c l a d i e l l a p r o c e r a from t h e dying t r e e s .
The growth r a t e of t r e e s i n each c l a s s was a l s o
examined by Benoit (1980) and r a d i a l increment
growth over t h e period 1955-1978 f o r t h e s e n s i t i v e c l a s s was s i g n i f i c a n t l y l e s s (p = . 0 l ) than
t h a t of t h e t o l e r a n t c l a s s ( f i g u r e 7 ) . A general
d e c l i n e i n growth f o r a l l c l a s s e s was noted.
1
9
YEAR 1955
-- - =TOLERANT;53 YRS
-=
AVG AGE
exposed 1.8 c o n i f e r s p e c i e s and found Austrian
n i g r a , Arnold), jack pine
-EPine (Pinus
s i a n a , Lamb.) and V i r g i n i a pine (P.
- virginiana,
M i l l . ) t o be t h e most s e n s i t i v e . However, they
reported v a r i a b l e symptom response among t h e
d i f f e r e n t s p e c i e s , among p l a n t s within s p e c i e s ,
and between branches and needles of i n d i v i d u a l
p l a n t s . In a s e r i e s of exposures, numerous
deciduous t r e e s were a l s o exposed t o s i m i l a r
ozone doses and green ash ( ~ r a x i n u spennsylvanica
Marsh.), white ash (F. americana L.) and t u l i p
poplar ( ~ i r i o d e n d r o n t u l i ~ i f e rLa. ) were r e p o r t e d
t o e x h i b i t f o l i a r i n j u r y by Wood (1970). Jensen
(1973) determined t h e s e n s i t i v i t y of 9 deciduous t r e e s p e c i e s on t h e b a s i s o f height
growth during a 5 month exposure t o 0.30 ppm
03 f o r 8 hours p e r day. He determined t h a t
saccharinum, L.) , green ash,
s i l v e r maple &A(
and sycamore (Platanus o c c i d e n t a l i s , L . ) were t h e
only s p e c i e s determined t o be s e n s i t i v e using
both parameters. Numerous s i m i l a r s t u d i e s u s i n g
high dose exposures have been reviewed by S k e l l y
and Johnston (1979).
Typical oxidant symptoms have been noted by
S k e l l y (unpublished) on s e v e r a l major f o r e s t
t r e e s p e c i e s indigenous t o Shenandoah National
Park of V i r g i n i a [ f i g . 8)
.
\---
INTERMEDIATE.52 YRS AVG AGE
'60
'70
1978
AVERAGE RADIAL INCREMENT GROWTH OF SENSITIVITY CLASSES
Figure 7--The average r a d i a l increment growth
of e a s t e r n white p i n e i n t h r e e ozone s e n s i t i v i t y
c l a s s e s a s found i n t h e Blue Ridge Mountains of
V i r g i n i a . Trees were l o c a t e d i n groups of 3
p e r s i t e with each s e n s i t i v i t y c l a s s represented
i n each of 10 p l o t s (10 t r e e s / c l a s s ) .
Other Eastern Species
F o r e s t t r e e s - - t h e r e l a t i v e 03 s e n s i t i v i t y of
s p e c i e s has been i n v e s t i g a t e d u s i n g high dose
exposures, e . g . 0.25 ppm O3 f o r 8 hour exposure
p e r i o d s . Using such doses Davis and Wood (1972)
Figure 8--Typical oxidant induced s t i p p l i n g
on hickory G a r y a spp.) a s observed i n t h e
Shenandoah National Park of V i r g i n i a . Note
asymptomatic a r e a of covered over p o r t i o n of
lower l e a f i n c e n t e r of photograph (upper
l e a f p u l l e d back).
Very few low dose exposure s t u d i e s have been
conducted t o determine e f f e c t s due t o c l o s e r t o
ambient p o l l u t a n t c o n c e n t r a t i o n o r due t o ambient
exposure c o n d i t i o n s . However, s e v e r a l r e c e n t
s t u d i e s have attempted t o reproduce ambient
concentrations of 03, SO2, and NOx (and v a r i o u s
combinations t h e r e o f ) and t o study t h e i r e f f e c t s
on t h e growth of l o b l o l l y p i n e (P.
- -t a e d a L.)
Kress and S k e l l y (1980a) American sycamore
Kress and S k e l l y (1980b), and s e v e r a l o t h e r
e a s t e r n t r e e s p e c i e s (Kress 1980). I n t h e combined p o l l u t a n t s t u d i e s using 0.05 ppm 03, 0.10
ppm N02, and 0.14 ppm SO2 f o r 6 hours p e r day f o r
28 consecutive days s i g n i f i c a n t height r e d u c t i o n s
were r e p o r t e d a s induced by O x alone t r e a t m e n t s
f o r each s p e c i e s without c l i n i c a l symptoms p r e s e n t on sycamore and with <5 percent f o l i a r
i n j u r y on l o b l o l l y pine. Kress (1980) r e p o r t e d
h e i g h t growth i n c r e a s e s and/or decreases f o r
10 t r e e s p e c i e s following exposure t o 0.05,
0.10, and 0.15 ppm 03 f o r 6 hours/day f o r 28
consecutive days. Lowest dose exposure s i g n i f i c a n t l y reduced t h e h e i g h t of l o b l o l l y p i n e and
0.10 pprn O3 reduced h e i g h t growth i n l o b l o l l y p i n e ,
green a s h , sycamore, p i t c h p i n e (P. r i g i d a M i l l . )
and sweetgum (Liquidambar s t y r a c i f l u a L . )
S l i g h t h e i g h t growth s t i m u l a t i o n s were r e p o r t e d
f o r s e v e r a l s p e c i e s following 0.05 ppm 03 t r e a t ment and sugar maple (A. saccharum Marsh.)
responded p o s i t i v e l y even a t t h e 0.10 ppm 03
t r e a t m e n t (p = 0.05) .
s a r y t o c l i p (to a 1 . 3 cm h e i g h t ) and remove comp e t i n g n a t u r a l v e g e t a t i o n which was t h e n c o l l e c t e d f o r d r y weight measurements ( t a b l e 4 ) .
.
Understory VegetationÑHarwar and Treshow
(1971) have conducted one of few s t u d i e s designed
t o determine ozone e f f e c t s t o u n d e r s t o r y p l a n t s .
They exposed 17 r e p r e s e n t a t i v e s p e c i e s of an
aspen community t o v a r i o u s high and low doses
of 0 5 days p e r week throughout t h e growing
3
season f o r 3 consecutive y e a r s . Several s p e c i e s
were found more s e n s i t i v e t h a n expected and
s e n s i t i v i t y was s o v a r i e d between s p e c i e s t h a t
t h e a u t h o r s suggested major s h i f t s i n community
composition would be probable following only a year
o r two of exposure.
Kohut and Krupa (1978) determined t h e s e n s i t i v i t y of s e v e r a l herbaceous p l a n t s of t h e Northc e n t r a l U.S. f o r e s t s . They l i s t e d a group of
p l a n t s found i n t h e f o r e s t s o f t h e North C e n t r a l
r e g i o n t h a t were a l s o s e n s i t i v e t o 0.08 and 0.15
ppm 0, f o r o n l y 4 hours. These p l a n t s a r e a l s o
n a t i v e t o t h e f o r e s t e d a r e a s of t h e n o r t h and
s o u t h e a s t e r n p o r t i o n s of t h e United S t a t e s .
The s e n s i t i v e p l a n t s l i s t e d were wild buckwheat, c h i c o r y , d a i s y , mustard, and Ribes.
Other work by S k e l l y (1977, unpublished) has
i d e n t i f i e d symptoms t y p i c a l l y induced by 0 on
Clematis s p . i n t h e Shenandoah National Park
of V i r g i n i a .
Figure 9 has been p r e s e n t e d t o f u r t h e r
demonstrate t h e e f f e c t of ambient c o n c e n t r a t i o n s
of ozone on a s p e c i e s t h a t i s widely d i s t r i buted a c r o s s North America i . e . common milkweed (Asclepias spp.) . Duchelle and o t h e r s
(1980) observed s e v e r e , moderate, and
only s l i g h t i n j u r y t o t h i s s p e c i e s t h a t occurred
n a t u r a l l y i n open p l o t s and i n n o n - f i l t e r e d and
f i l t e r e d open t o p chambers, r e s p e c t i v e l y , a s
l o c a t e d i n t h e Shenandoah National Park i n
V i r g i n i a . This s p e c i e s i s being t e s t e d f u r t h e r
f o r i n j u r y t h r e s h o l d s and f o r u s e a s p a r t of a
p l a n t b i o i n d i c a t o r system.
A s a n o t h e r p a r t of t h e Blue Ridge Mountain
S t u d i e s , Duchelle and S k e l l y (1980) e s t a b l i s h e d
4 r e p l i c a t i o n s of open t o p chambers r e c e i v i n g
c h a r c o a l f i l t e r e d a i r o r non-charcoal f i l t e r e d
a i r i n o r d e r t o i n v e s t i g a t e h e i g h t growth of
s e l e c t e d f o r e s t t r e e s . Four open p l o t s were
a l s o e s t a b l i s h e d . By mid-summer it became neces-
F i g u r e 9--Oxidant i n j u r y t o milkweed
~ ~ & l e ~ spp.)
i a s observed i n t h e Shenandoah National Park, VA a s grown i n (A) open
p l o t s , (B) non-f i l t e r e d open t o p chamber and
CC) c h a r c o a l - f i l t e r e d open t o p chamber.
Purple s t i p p l e was only noted on upper
leaf surfaces.
Table 4--The dry weight of foliage of composited clippings as collected from 4 filtered air and 4 non-filtered air open top chambers and 4 open plots established in the Big Meadows Area of the Shenandoah National Park, VA. Exposure
Clipping Dates1 Aug. 14, 1979 Oct. 9, 1979 Dry Weight (Grams) Total
Total
wt2 Average
wt
7263
Filtered
Non-filtered 4937
3128
Open
1816
1234
782
1599
1323
845
Average
fixation and stomatal conductance usually associ- ated with needle aging. Needles of sensitive trees senesced and abscissed prematurely thus contributing to a steady decline in tree vigor and increased vulnerability to other sources of stress. Other Forest Tree Species Miller (1973) ranked the following species for their decreasing sensitivity to ozone following fumigation tests:
Most sensitive
400
331
211
Monterey x Knobcone pine hybrid (P. radiata x P. altenuata) Ponderosa pine [c. ponderosa Laws.)
~ l species
l composited as clipped to 1.3 cm height, 10 foot diameter plots. z
4 replications. Intermediate
Western Species Ponderosa Pine Since the decline of ponderosa pine (P. ponderosa Laws .) during the 1950's (and henceforth into the 1980's) in the South Coast air basin and San Bernardino Mountains of California, this species has become the most intensively investigated of all western forest vegetation species. Declining ponderosa pines have most recently been reported in the southern Sierra- Nevada mountains by Miller and Millecan (1971) and in the Sequoia National Forest and Sequoia- Kings Canyon National Parks by Williams and others (1977). The decline of this species was initially termed "X-diseasev by Parameter and others (1962); further study by Miller and others (1963) eluci- dated ozone to be the direct incitant. Inter-
relationships of foliar symptoms with increased root disease and increased incidences of bark beetle infestations in injured trees have been determined along with significant growth decreases and mortality (Stark and others, 1968; McBride and others, 1975). Several reviews of the major studies that have dealt with ponderosa pine have recently been published by Brown and others (19791, Miller (1973) and Miller and McBride (1975). Most recent investigations by Coyne and Bingham (in press) identified characteristics of ecotypic variation in E. ponderosa which varied in their
clinical symptom response to ozone under field conditions. Light responses, photosynthetic rates, and stomatal conductances were observed and differences among injury classes were mani- fest as acceleration of the normal decline of C02 Western white pine (P. monticola Doug.)
Jeffrey x Coulter pine hybrid
Tolerant
Coulter pine (P.
- coulteri D. Don") Douglas fir (Pseudotsuga menziesii (Mirb.) Franco
Jeffrey pine (P. jeffreyi )Grev. & ~alf.
White fir (Abies concolor (Gord. 6 Glend.1 Lindl.
~i~ cone Douglas fir (Pseudo- tsuga macrocarpa (Vasey) Mayr. Knobcone pine (P.
- attenuata Lemm )
Incense cedar (Libocedrus decurrens Torr.) Sugar pine
lambertiana Doug1 )
Giant sequoia (Sequoia gigantea (Lindl. ) Decne.
.
.
(c.
In one of few low O3 dose exposure studies, 9 western conifer species have been evaluated for foliar injury and growth responses by Wilhour and Neely 0.977).
They found signifi- cant growth reduction in juvenile seedlings of P. ponderosa and P. monticola exposed to 0.10 ppm 03 for 6 hours/day consecutively for up to 22 weeks. They noted no constant association between growth response and foliar injury. DIRECT EFFECTS TO FOREST ECOSYSTEMS A fair number of published reports assessing air pollution induced injury to agricultural crops are available. Damage estimates of yield losses have also been published e.g. air pollution injury to potatoes in the Atlantic Coastal States [Heggestad, 1973). Such evaluations have been based upon extensive knowledge of crop manage- ment practices and abundant information exists concerning expected yields. Therefore, yield losses such as potato tuber number, size, and weight may be easily determined and subse- quently correlated with the degree of foliar injury as induced by photochemical oxidants (Heggestad, 1973) .
Advancing from a relatively simplistic agro- nomic monocultural system of crop management to a mixed hardwood conifer forest ecosystem poses considerably different problems in determining an effect due to any given single stress factor. As noted previously, an abundance of literature describing symptoms has become available for
several major forest species that appear sensi- tive to photochemical oxidants (table 3). However, the overall impact of the more subtle changes in functional efficiency of the plant expressed, for example, as slightly reduced photo- synthetic capability of otherwise asymptomatic foliage or noted trends of slightly shorter pollen tube length in the presence of low doses of 03 remain relatively little understood. There have been no major investigations of oxidant impacts to forest communities or forest
ecosystems with the single well known exception
of the San Bernardino Mountain Studies. The
intensity of the various studies and their related interactions within one of many possible areas of investigation has been illustrated in figures 10 and 11. As noted in figure 10,
oxidant air pollutants are only one of many natural or anthropogenic stress factors important to the forests of the San Bernardino Mountains and if this figure were to be modified for illus- tration of an Eastern U.S. or European forest,
SO2 and other forms of atmospheric depositions would necessarily be added for emphasis. Figure 11 illustrates only a few of the complex inter- actions which may take place within an ecosystem and even a very subtle change in bark characteristics or carbohydrate pools as initially induced by oxidant injury of the foliage may be sufficient to encourage a bark beetle attack of weakened trees. As related in table 3, an evaluation of knowledge concerning injury, damage, and impact to forest species of the San
Bernardino Mountains (primarily E. ponderosa) is
abundant and knowledge is considered to be
moderate for the forest community. However, due to the complexity of any given forest ecosystem,
including that which has been intensively studied in the San Bernardino Mountains, relatively poor information exists as to the subtle influences to the functioning of any given forest ecosystem. CHARACTER-
ISTICS
COMMUNITY STRUCTURE
COMMUNITY
STRUCTURE 5
6
7
8
9
Figure lo--Community-succession interactions in a mixed-conifer forest ecosystem. (From Taylor, 1974). 0
POLLUTANTS
1.
/&-$.A
SYNTHESIS
0;
MOISTURE
BARK
TEXTURE
- PHLOEM THICKNESS
....
.
..- .- - PHLOEM MOISTURE
. - - - .....- - ....
...... ..
THICKMESS
.......- ....
RESIN QUANTITY
- -- -- - -
.... .
FUNGI
FUTURE RESEARCH EMPHASIS AND CONSIDERATIONS Why do we know so little about oxidant induced
injury, damage, or impact to forest communities
or forest ecosystems? Why have only a few tree
species been intensively studied and relatively
few others evaluated for foliar symptom response?
How does the lack of such information influence decisions made regarding the establishment of
National Ambient Air Quality Standards?
Figure 11-411example of tree-level interactions in a mixed-conifer forest ecosystem. Data from these types of studies would be integrated into overall effect illustrated in figure 11. (From Taylor, 1974) .
Intensive management of agronomic crops through selection of tolerant varieties for planting in high oxidant areas and appropriate changes in cultural practices such as withholding irrigation water during oxidant pollution episodes have all served to reduce the immediate injury (and there- fore damage and impact) to such important crops as potatoes, tobacco, soybeans, snapbeans and certain horticultural plants. Through the develop- ment of such practices, the agricultural scientist has assisted the immediate grower (as should be the case) but concurrently the economic cost/bene- fit justifications for pollution abatement enforce- ment have been lessened since overall impact has potentially been greatly reduced. The evaluation of forest tree species for sensitivity to various pollutants has also been attempted and likewise long term growth losses may be averted. Such investigations must be approached with a certain degree of caution since long term subtle changes most undoubtedly are occurring in natural forest ecosystems but as yet most remain undetected. Natural ecosystems usually have a system of checks and balances but the system remains deli- cate and trends towards simplification are easily initiated. Changes in primary productivity, energy resource flow patterns, biogeochemical cycles, and species successional patterns may all be challenged by oxidant air pollution but have remained virtually non-studied.
The difficulties encountered in developing research aimed at isolating, identifying, and subsequently integrating the known effects of oxi- dant air pollutants on the forest ecosystem are too numerous to completely cover in the remaining space available. A partial listing however, must include these important points: 1) Photochemical oxidant is insidious over extremely large areas of diverse forest land and the establishment of control (non- pollution exposed) areas has become virtually impossible. 2) The introduction of charcoal filtration sys- tems into such areas to establish kontrolsw is at best artificial and due to physical restrictions the ability of such systems to define a true ecosystem pertubation is like- wise limited. 3) Long-term investigations must take into account innumerable variables some of which are very transient in their occurrence and others for which relatively little is known even under natural conditions. 4) Modeling and related statistical procedures must take into account the diversity and complexity of a forest ecosystem and statistically probabilities of p = .01, .05,
or .10 must not be the only acceptable limits of "biological significance." The prediction of a biological event with 70 percent accuracy may be valid. Observation of only a 1-5 percent decrease in annual radial increment growth or similar decreases in pollen production and viability may not be statistically significant but may have greater long-term biological significance to the ability of a species to survive over their natural range. The natural forested ecosystems of the temper- ate and Mediterranean regions of the world may serve to provide the most invaluable bioindicator of long-term photochemical oxidant air pollution induced effects. National air quality standards must be reasonably developed to protect these natural resources from even minor change but initially adequate financial support and associ- ated quality research must be continued to ade- quately define the real and potential effect of oxidants to plant species, to plant communities, and to entire forest ecosystems. LITERATURE CITED Benoit, L. F. 1980. Ozone effects on long term radial incre- ment growth and reproduction of eastern white pine. (Abstr.) Proc. Potomac Div. her. Phytopath. SOC., Morgantown, W. Va. Berry, C. R.
1961. White pine emergence tipburn, a physio- genic disturbance. (Sta. Paper No. 130., 8 p.). Southeast For. Exp. Sta., USDA- For. Serv., Athens, Ga. Brown, H. D., P. R. Miller, J. M. Skelly, D. B. Drummond, and C. E. Carlson. 1979. Air pollution effects on forest vege- tation and the analysis of the role of Forest Insect and Disease Management. 134 p. USDA-For. Serv., Washington, D.C. Cleveland, W. S. and B. Kleiner. 1975. Transport of photochemical air pollution from The Camden-Philadelphia urban complex. Environ. Sci. Tech. 9:869-872. Corn, M., R. W. Dunlap, L. A. Goldmuntz and L. H. Rogers. 1975. Photochemical oxidants: sources, sinks and strategies. J. Air Poll. Contr. Assoc. 25 :16-18.
Coyne, P. I. and G. E. Bingham. 1980. Comparative ozone dose response of gas exchange in a ponderosa pine stand exposed to long term fumigations. (Submitted for publication to J. Air Poll. Contr. Assoc.). Coyne, P. I. and G. E. Bingham. 1980. Variation in photosynthesis and stomata1 conductance in an ozone-stressed ponderosa pine stand: Light response. (Submitted for publication to For. Sci.). Davis, D. D. and R. G. Wilhour. 1976. Susceptibility of woody plants to sulfur dioxide and photochemical oxidants. 72 p. USEPA Ecol. Res. Series EPA-600/3- 76-102. Davis, D. D. and F. A. Wood. 1972. The relative susceptibility of eighteen coniferous species to ozone. Phytopathology 62:14-19.
Kohut, R. J. and S. V. Krupa. 1978. Sensitivity of selected species of native vegetation to ozone. (Abstr.). Proc. Am. Phytopathological Soc. 4:88. Duchelle, S. F., J. M. Skelly and L. W. Kress. 1980. The impact of photochemical oxidant air pollution on biomass development of native vegetation and symptom expression Proc.
of Asclepias spp. (Abstr.)
Potomac Div. her. Phytopath. SOC. Morgantown, W. Va. Kozlowski, T. T. 1980. Impacts of air pollution on forest eco- systems. Bio. Sci. 30:88-93. .
Galloway, J. N. and J. M. Skelly. 1978. A pollution episode in Virginia. Virginia Climate Advisory 2(3):4-6. Gerhold, H. D. 1977. Effect of air pollution on Pinus strobus L. and genetic resistance. 45 p. USEPA Rep. No. EPA-600/3-77-002. Cor- vallis, Or. Grennfelt, P. 1979. Ozone monitoring in Scandanavia. In Report from the workshop "Ozone effects on vegetation in Europe." M. Eastmond and L. Skarby Eds. p. 5-8. Swedish Water and Air Res. Inst., Stockholm. Harward, M. R. and M. Treshow. 1971. The impact of ozone on understory plants in the aspen zone. Proc. 64th Ann. Mtg. Air Poll. Contr. Assoc. Atlantic City, N.J. Hayes, E. M. and J. M. Skelly. 1977. Transport of ozone from the northeast U.S. into Virginia and its effect on eastern white pine. Plant Dis. Reptr. 51 :778-782.
Heggestad, H. E. 1973. Photochemical air pollution injury to potatoes in the Atlantic Coastal States. Amer. Pot. J. 50:315-328. Husar, R. B., D. E. Patterson, C. C. Paley, and N. V. Gillani. 1977. Ozone in hazy air masses. Jn- Inter-
national Conference on Photochemical Oxi- dant and its Control. p. 275-282. USEPA Ecol. Res. Series EPA-600/3-77/001b. Research Triangle Park, N.C. Jensen, K. F. 1973. Response of nine forest tree species. to chronic ozone fumigation. Plant Dis. Reptr. 57:914-917.
Kickert, Ronald, N. and P. R. Miller. 1978. Responses of ecological systems. In
Handbook of methodology for the assessment of air pollution effects on vegetation. W. W. Heck, S. V. Krupa, S. N. Linzon, eds. p. 14.1-14.45 Air Poll. Contr. Assoc. Pittsburgh, Pa. Kress, L. W. 1980. Effects of O3 and 0 + NOn on growth
of tree seedlings. Proc. Internatll. Symp. on Eff. of Air Pollutants on Mediterranean and Temperate Forest Eco- systems. June 22-27. Riverside, Ca. Kress, L. W. and J. M. Skelly. 1980. Growth imuact of 07. NO?, and/or SO2 on Pinus taeda. (~ubmi&ed for publication to Atmos. Environ.). --
Kress. L. W. and J. M. Skellv. 1980. Growth impact of o;, NO,, and/or SO2 o Atmos. Environ.). McBride, J. R., V. P. Semino, and P. R. Miller. 1975. Impact of air pollution on the growth of ponderosa pine. Calif. Ag. 29 (12) :8-9. Miller, P. R. 1973. Oxidant-induced community change in a mixed conifer forest. In Air Pollution Damage to Vegetation. J. A. Naegela Ed. p. 101-117. Adv. in Chem. Series 122. Amer. Chem. Soc., Washington, D.C. Miller, P. R. and J.
1975. Effects of
In Response of
B. Mudd and T.
235. Academic
McBride. air pollutants on forests. Plants to Air Pollution. T. Kozlowski, eds. p. 195- Press, New York. Miller, P. R. M. H. McCutchan and H. P. Millegan. 1972. Oxidant air pollution in the central valley, Sierra Nevada foothills, and Mineral King Valley of California. Atmos. Environ. 6:623-633. Miller, P. R. and A. A. Millecan. 1971. Extent of oxidant air pollution damage to some pines and other conifers in Cali- fornia. Plant Dis. Reptr. 55:555-559. Miller, P. R., J. R. Panneter, Jr., O.C. Taylor, and E. A. Cardiff. 1963. Ozone injury to the foliage of Pinus ponderosa. Phytopathology 53:1072-1076. National Academy of Sciences. 1977. Ozone and other photochemical oxidants. Comm. on Med. and Biol. Eff. of Environ. Pollutants. 719 p. NAS, Washington, D.C. Nicholson, C. R. 1977. The response of 12 clones of eastern white pine (Pinus strobus) to ozone and nitrogen dioxide. 141 p. M.S. Thesis, Virginia Polytechnical Institute and State University. Blacksburg, Va. USEPA. 1977. Photochemical oxidant air pollution effects on a mixed conifer ecosystem A progress report. 339 p. USEPA Ecol. Res. Series EPA-600/3-77-104. Corvallis, Or. Parmeter, J. R., Jr., R. V. Bega, and T. Neff. 1962. A chlorotic decline of ponderosa pine in southern California. Plant Dis. Reptr. 46 :269-273.
USEPA. 1977. International Conference on photo- chemical oxidant pollution and its control. 1169 p. Vol. I and 1 1 . USEPA
Ecol. Res. Series EPA-600/3-77-OOla, OOlb. Res. Triangle Park, N.C. ~karby,L. 1979. Elevated ozone levels at the Swedish west coast and in southern Sweden (Skane) using tobacco as an indicator plant. &
Report from the workshop "Ozone effects on vegetation in Europe." M. Eastmond and L. skirby Eds. p. 9-12. Swedish Water and Air Res. Inst., Stockholm. Skelly, J. M., S. F. Duchelle, and L. W. Kress. 1979. Impact of photochemical oxidant air pollution on eastern white pine in The Shenandoah, Blue Ridge Parkway and Great Smoky Mountains National Parks. Proc. I1 Conf. on Sci. Res. in Natll. Parks. San Francisco, CA. Wilhour, R. G. and G. E. Neely. 1977. Growth response of conifer seedlings to low ozone concentrations. In Inter- national Conference on ~hotochemical Oxidant Pollution and Its Control. p .
635-645. USEPA Ecol . Res . Series
600/3-77/OOlb. Williams, W. T., M. Brady and S. C. Wilson. 1977. Air pollution damage to the forests of the Sierra Nevada Mountains of Cali- fornia. J. Air Poll. Contr. Assoc. 27: 230-234. Skelly, J. M. and J. W. Johnston. 1979. Oxidant air pollution impact to the forests of eastern United States - a
literature review 30 p. USEPA Rep. No. EPA-600/3-79-045. Corvallis, OR. Wolff, G. T., P. J. Lioz, G. D. Wight, R. E. Meyers, and R. T. Cederwall. 1977. An investigation of long-range trans- port of ozone across the midwestern and eastern United States. Atmos. Env. 11:797-802. Stark, R. W., P. R. Miller, F. W. Cobb, Jr., D. L. Wood, and J. R. Parmeter, Jr. 1968. Photochemical oxidant injury and bark beetle (Co1eoptera:Scolytidae) infestation of ponderosa pine. I. Inci-
dence of bark beetle infestation in injured trees. Hilgardia 39:121-126. Wood, F. A. 1970. The relative sensitivity of sixteen deciduous tree species to ozone. Phyto-
pathology 50:579. (Abstr.) .
Primary Productivity, Sulfur Dioxide,
and the Forest Ecosystem: an
Overview of a Case study1
Abstract: The objective of the West Whitecourt case study was to determine the consequence of chronic long term ex- posure of a forest ecosystem to low concentrations of sulphur dioxide emissions originating from a "sour gas" processing plant in west central Alberta, Canada. An inter- disciplinary ecological approach was utilized. The vegetation and atmospheric environment were characterized. A concept of ecologically comparable sampling site selec- tion was developed and applied in the West Whitecourt study area. Laboratory and field measurements revealed a reduc- tion in photosynthetic rate in lodgepole pine x jack pine (Pinus contorta x Pinus banksiana) in the field. Reduction of adenosine triphosphate (ATP) concentration in pine tissue during SO2 fumigation in the field followed by complete re- covery after termination of SO2 fumigation and the disruption of mineral nutrient cycling in the forest ecosystem were observed. Basal area increment measurements of 200 lodge- pole x jack pine trees from 5 ecologically comparable sampling sites revealed a decrease in wood production directly related to the presence of sulphur dioxide emissions. It is recommended that the concepts of the assimilatory capacity of the environment for sulphur gas pollutants and irreversible ecological modification be utilized as measures of environmental quality. Many review articles have been written' addressing the problem of air pollutants and forest
ecosystems (Tam and Aronsson, 1972; Smith, 1974;
Miller and McBride, 1975; and Linzon, 1978).
These reviews documented the extreme examples of
acute high concentration long term air pollution
stress on ecosystems and were essentially postmortem studies. Environmental change due to air
pollution stress was clearly visible in these
cases. With the exception of the San Bernardino
Mountain study investigating the effects of
photochemical oxidants on a mixed conifer forest
ecosystem in California (Miller and others, 1977; Kickert and Miller, 19791, very little emphasis has been placed upon integrated research programs concerning the impact of chronic long term low concentration air pollution stress on forest eco- systems. The objective of this paper is to pre- sent an overview of a four-year integrated forest ecosystem case study designed to determine the consequence of chronic long term exposure of a conifer forest ecosystem to low concentrations of sulphur dioxide emissions originating from a ''sour gas" processing plant in Alberta, Canada (Legge and otters 1978). BACKGROUND TO THE CASE STUDY ^presented at the Symposium on Effects of Air
Pollutants on Mediterranean and Temperate Forest
Ecosystems, June 22-27, 1980, Riverside,
California, U.S.A.
2~rofessionalAssociate, Kananaskis Centre for
Environmental Research, University of Calgary,
Calgary, Alberta T2N 1N4 Canada
Potential detrimental environmental impact of sulphur dioxide emissions from the sour gas proc- cessing industry upon the environment in Alberta was a major concern of this industry in the early 1970's. This concern lead to the formation of the Whitecourt Environmental Study Group (WESG) in 1971, a consortium of eight companies involved in the production of saleable natural gas from sour gas (natural gas containing hydrogen sul- phide) in the Whitecourt district of west-central Alberta. It was clear at that time that the assessment of the impact of sulphur dioxide on the forest ecosystem was not a simple cause and effect relationship. A five-year environmental research program therefore was initiated in 1972 and was cooperatively funded by both industry and the Alberta Government. The objective of the re- search program which was called the Whitecourt Environmental Study was to determine the environ- mental consequences of the operation of sour-gas processing facilities on the forest ecosystem in the Whitecourt district occupied by 11 sour gas processing plants and defined as the Whitecourt study area (figure 1). research indicated the potential for environmental change in the field due to sulphur dioxide ex- posure. To resolve these contradictory research results it became clear that a detailed field case study of a forest ecosystem surrounding a sulphur dioxide source was required. The AMOCO Petroleum Company Limited West Whitecourt (Windfall) sour-gas processing plant was chosen for the case study. This gas plant had the longest operational history in the Whitecourt study area beginning operation in 1962. SOURCE OF SULPHUR GAS EMISSIONS The following is a brief outline of the opera- tion of the West Whitecourt sour-gas processing and sulphur recovery plant to familiarize the reader with the origin of sulphur gas air pollu- tion from the sour-gas processing industry in Alberta. Hydrogen sulphide is the principle sulphur com- pound present in sour natural gas and is removed by a series of chemical processes in a sulphur recovery gas plant as elemental sulphur. The H2S not converted to elemental sulphur is incinerated in a high temperature reaction furnace (580' Celcius) in excess air and methane where it is oxidized to sulphur dioxide (SO2) and vented to the atmosphere from a tall (122 meter) "candy- striped" incinerator stack. In addition to an incinerator stack, smaller stacks called flare stacks, generally less than 46 meters in height, Figure 1. Map of western Canada showing in bold outline the province of Alberta and the Whitecourt Study Area. --
-
TOTAL EMISSIONS/MONTH
MAIN STACK/MONTH
... ........,... FLARE STACK 1 MONTH
3200
The Whitecourt study began in 1972 as a remote sensing airborne environmental survey accompanied by assessment on the ground carried out by INTERA Environmental Consultants Limited to determine if there were any visible large scale environmental disturbances. After two years of general re- connaissance no large scale environmental dis- turbance was found (Whitecourt Environmental Study 1972 and 1973).
Controlled SO2 fumigation experiments carried out in the laboratory by the Kananaskis Centre for Environmental Research, University of Calgary, on young lodgepole pine (Pinus contorta Loud.) seedlings, however, re- vealed a direct effect of SO2 on vegetation. These experiments showed that, although plants have the ability to adjust physiologically with- in certain environmental limits, plants were adversely affected when these limits were ex- ceeded (Legge and Harvey 1974). A conflict therefore arose; the general environmental field survey indicated no large scale modification of the vegetation while the preliminary laboratory Figure 2. Monthly sulphur emission history of the West Whitecourt Gas Plant from 1970 through 1976. are used to burn small waste quantities of sulphur recovery gas plant process and compressor gases. Except in the case of a gas plant opera- tional upset, when for short periods the flare stack may contribute more sulphur gas emissions to the atmosphere on a daily basis than the in- cinerator stack, the incinerator stack is the main source of sulphur gas emissions from the West Whitecourt Plant. The monthly sulphur emissions (in long tons) of the West Whitecourt Gas Plant for 1970 through 1976 is shown in figure 2; simply double the sulphur emissions to obtain the SO2 emissions. It is important to note that this gas plant has reduced its sulphur emission output per day an order of magnitude since start-up in 1962 from 150 long tons/day to 18 long tonslday in 1976. This reduction was achieved by enhanced operating procedures and the addition of "tail-gas" re- covery units. SULPHUR:
THE NUTRITIONAL CONTROVERSY Sulphur is an essential nutrient element for normal plant growth and metabolism. It is re- quired in intermediary metabolism and is a con- stituent of many organic compounds such as amino acids and proteins in plant tissue. Sulphur normally enters the plant via the root system in the form of sulphate, which is biochemically re- duced and then converted into numerous organic compounds. Plants, however, can also take-up and utilize SO2 from the atmosphere via the stomates and utilize it as sulphur source for plant nutrition. Faller (1971), for example, has shown that tobacco plants can utilize SOy as a source of sulphur in sulphur deficient soils. This type of information has led many government and industry departments to say that SO2 emitted from industrial sources is actually beneficial as an aerial fertilizer for plants growing on sul- phur deficient soils (Terman 1978; Noggle and Jones 1979).
The situation is not quite -so simple, however. Though a small amount of atmos- pheric SOo can be nutritional to plants in the short term, the large amount and high frequency of uncontrolled application of sulphur such as SOy to an ecosystem by sulphur sources such as smelters, pulp and paper mills, coal-fired power plants, oil sand and oil shale extraction plants and sulphur recovery gas plants can be detri- mental in the long term. Different plant species not only have different nutritional requirements for sulphur, but the rate at which plant species assimilate sulphur is influenced by many other variables, such as physiological status, age, time during the growing season, temperature, soil nutrient availability, and light intensity to name a few. When more sulphur is available than can be assimilated it is accumulated in the tissue (Ulrich and others 1967; Legge and others 1977; Cowling and Koziol 1978; Thompson and Kats 1978). This foliar sulphur accumulation can reach toxic levels and adversely affect plant growth (Katz 1949; Linzon and others 1978). The distinction between the assimilation and the accumulation of sulphur of atmospheric origin by plantsmust be addressed in any ecosystem study. CONCEPTUAL APPROACH TO CASE STUDY To carry out an ecosystem case study one must have a basic understanding of what an ecosystem Is.
The ecosystem is the basic functional unit
of ecology since it includes both the living organism and the non-living environment in which these organisms live. Odum (1971) has defined an ecosystem as "any unit that includes all of the organisms in a given area interacting with the physical environment so that a flow of energy leads to clearly defined trophic structure, bio- tic diversity and material cycling within the system". Due to the inseparable nature and interdependence of the components of ecosystems upon one another, however, any change that occurs in one component of the ecosystem potentially affects all the components of that ecosystem. The higher the diversity of an ecosystem there- fore the more numerous the interrelationships within the ecosystem (Jernelou and Rosenberg 1976). The stability of an ecosystem can be viewed as a function of the balances amongst the components of that ecosystem. An environmental stress such as air pollution can modifiy the stability of an ecosystem by disrupting the balance amongst the ecosystem components. Prior to the initiation of the West Whitecourt case study, it was recognized that an ecosystem study was an interdisciplinary undertaking. The term interdisciplinary in this context means the amalgamation of a set of specific disciplinary talents to work together to address a complex environmental problem. An interdisciplinary re- search team was assembled by the Kananaskis Centre for Environmental Research of the University of Calgary, The University of Alberta, The University of Washington, San Jose State University and the Southern Alberta Institute of Technology. The scientific expertise of the research team was broadly based and ranged from remote sensing, ecology, taxonomy, genetics, plant physiology, analytical chemistry, biochemistry, stable iso- tope physics and meteorology to statistics and electrical engineering. A conceptual model was developed to illustrate the dynamic relationship between the sulphur dioxide "source" and the generalized ecosystem "sink" and is shown in figure 3. For purposes of communication among disciplines, the ecosystem was sub-divided into the following four compart- ments: air, vegetation, soil, and water. The two- way arrows indicate the inter-relationship of the four ecosystem compartments. The expertise of each member of the research team was thus focussed on more than one of the ecosystem compartments at all times. This lead to the formulation of co- operatively designed experiments to evaluate not fir [Abies balsamea (L.) Mill.] (Legge and others VEGETATION
A physiognomic classification of the vegetation communities in the West Whitecourt study area identified 13 major cover types out of 24 com- munity types. Ten climax vegetation associations were recognized. The vegetation of the study area was mapped using a combination of LANDSAT imagery, LANDSAT digital data and conventional false colour infrared aerial photography both of which were accompanied by ground based verifica- tion. With the aerial colour infrared photography of the West Whitecourt study area as a subsample, computer mapping utilizing LANDSAT digital data was completed on 116,000 hectares to place the study area in a regional perspective. The computer mapping of the study area was eight times faster than conventional photography alone and had a comparative accuracy of 93 percent. u WATER
Figure 3. Conceptual model of the forest eco- system in the West Whitecourt case study area. only the interfaces between ecosystem compartments but also the processes within the ecosystem com- partments. Scientists with different areas of expertise were brought into the case study, how- ever, as a function of the needs of the research program. The selection and the timing of inter- action of disciplinary participants were viewed as critically important factors for the success of the program so the case study grew in terms of disciplinary participation from 7 in 1974 to 10 in 1975 and finally to 12 in 1976 and.1977. This evolutionary interdisciplinary approach added a dimension of insight into the fate of sul- phur gas emissions in the forest ecosystem that would not have been possible had the separate disciplines of the research team been operating in isolation. VEGETATION CHARACTERIZATION The vegetation of the Whitecourt area is in- cluded in the predominately forest subregion of the Boreal Forest Region of Canada (Halliday 1937) and is characterized as a transition forest area between the Boreal and Subalpine Forest Regions. The transitional nature of the common species of trees occurring in the area are actually repre- sented by populations of hybrid individuals be- tween lodgepole pine (Pinus contorta Loud.) and jack pine (Pinus banksiana Lamb.), while the true fir in the area represents hybrids between alpine fir [Abies lasiocarpa(Hook.) Nutt.] and balsam ECOLOGICALLY ANALAGOUS SITES One of the principle difficulties encountered by air pollution researchers, before collecting samples in the field for analysis, is the selection of sampling locations. Most sampling locations in air pollution studies are chosen solely on the basis of a gradient which is usually a function of the prevailing wind and the distance from a poll- ution source. Not enough emphasis is placed upon the structure and composition of the plant communi- ties from which samples are taken. Since an eco- system is composed of many interrelated highly variable biological and physical components, the response of these components to a chronic environ- mental stress such as air pollution will also be highly variable. If the range of variability of the responses of ecosystem components to an environmen- tal stress is not considered, the expression of the effect of the environmental stress on the eco- system components may not be detected. There must be a common basis for comparison of ecosystem com- ponents therefore to determine both the gross and subtle effects of an environmental stress along a gradient. The concept and criteria for ecologically analogous sample site selection were developed and applied during the West Whitecourt case study in an attemot to minimize the variability of eco- system components and hence to minimize the varia- bility of the response of the ecosystem components to air pollution stress. The key to this concept of sample site selection is based upon comparable ecological variability of the ecosystem components and comparable environmental variability at the sampling locations chosen along a distance gradient. The criteria for ecologically analogous sample site selection are summarized in Figure 4. When the ecological and environmental variation of ecosystem components at all the sam~lingloca- tions are as similar as possible, the sampling sites are said to be ecologically analogous. The major difference amongst the sampling locations ECOLOGICAL ANALOGUE CONCEPT
ASSUMPTIONS
1 = 2 + 3
1. Ecological Variables (sites A, +An )
slope
aspect
soil type
soil moisture
species density
species diversity
2. Environmental Variables (other than pollutants)
temperature
solar radiation
wind
precipitation
3. Pollutant Variables
composition
location
distance
concentration/conversion
frequency/duration
Figure 4. Summary of criteria utilized for the
selection of ecologically analogous sample sites.
therefore is distance from the pollution source.
The assumption is that the pollutant variables
such as concentration, frequency of fumigation
and duration of fumigation will decrease in
magnitude with increasing distance from the
pollution source. The magnitude of the air
pollution stress on ecosystem components at the
sampling locations will correspondingly decrease
with increasing distance from the pollution
source. This procedure ensures that the expression of the air pollution stress on ecosystem
components will be maximized.
Meteorological and air quality data were
essential in sample site selection. The prevailing winds during the growing season in the study
area were shown to have the highest frequency
of occurrence from the WNW and the second
highest frequency from the ESE. Sulphur dioxide
emissions from the West Whitecourt Gas Plant
therefore occurred with greatest frequency in
S corridor.
E
Although idealized, the
an ~
corridor concept provided an essential point
of reference for the areas chosen for the
selection of sampling locations in the West
Whitecourt study area.
The range of distances at which maximum
ground level concentrations would occur from
sulphur gas emissions from the main incinerator
stack and flare stacks was calculated using the
simple Gaussian plume model under mean wind conditions and a wide range of stability classes.
The maximum ground level concentrations would
occur between 1.6 and 34.0 km downwind of the
incinerator stack and between 0.4 and 2.6 km
downwind of the West Whitecourt Gas Plant. The
intensive experimental site therefore, was principally exposed to sulphur gas emissions from the
flare stacks. Only under short-lived meteorological conditions such as would occur during the
break-up of an inversion would sulphur gas
emissions from the main incinerator stock reach
the intensive experimental site.
It must be emphasized at this point that the
air quality standards for SO2 of 0.2 p p m h hr. /
24 hr. as set by the Alberta Department of the
Environment, were only exceeded on three occasions at the intensive experimental site 1.5 km
east of the West Whitecourt Gas Plant in over
2500 hours of ambient air monitoring during the
1975 and 1976 growing seasons in the West Whitecourt study area.
Five ecologically analogous lodgepole x jack
pine sampling locations were selected in the West
Whitecourt case study area. The five sample
sites were chosen in locations which were progressively downwind in the main path of sulphur
dioxide emission corridor. These sites were
chosen in this manner so that the sulphur dioxide
emission impact gradient would be very steep
across the five sampling locations to maximize
the differences in the responses of the ecological
analogues to pollution stress. The conceptual
ecological model presented in Figure 3 can be
generalized to express the relationships amongst
the five ecological analogues and is shown in
Figure 5. The ecologically analogous sampling
IMPACT GRADIENT
SOURCE
SINK
Figure 5. Replicated conceptual ecological model
illustrating the five ecologically analogous
lodgepole x jack pine sampling locations along
a sulphur dioxide concentration gradient.
sites were located at distances of 1.2 km (A=),
2.8 km (AII), 6.0 km (AII~), 7.5 km (AIv) and 9.6
km (Av) from the Gas Plant. Sampling locations in
the study area other than ecological analogues
were designated by the letter S.
CASE STUDY DATA OVERVIEW Foliar sulphate-sulphur concentration in lodgepole x jack pine trees was found to be a better measure of foliar sulphur accumulation than the foliar total sulphur concentration. The method of Johnson and Nishita (1952) was used to determine foliar sulphate-sulphur concentration while a Leco Furnace was used to determine foliar total sulphur. Figure 6 shows a plot of foliar sulphate-sulphur concen- tration in age-classed lodgepole x jack pine I
I
1
W x t Whilmcourt Study Area
Pinut contort0 a P.banktiam
--
Birch Mountain Firm Tmw
Pinut bonkeiana K R contww
increasing foliar age. The foliar sulphate-sulphur data strongly support the concept of an environ- mental stress gradient presented earlier. The stable sulphur isotopic composition ( s / ratio) of sulphur dioxide emissions from sour gas plants in Alberta have been shown to differ from the natural environmental background stable sulphur isotopic composition (Lowe and others, 1971; Krouse, 1977). This is referred to as the 6 3 4 value.
~
The more positive the 63^S value the
greater the enrichment in s ~ ~The
. background
stable sulphur isotopic composition in the West Whitecourt study area is near 0. s3'
The stable sulphur isotopic composition of sulphur dioxide emissions from the incinerator stack at the West Whitecourt Gas Plant was shown to be +22.2'/00
(per thousand). This difference provided an environmental tracer for sulphur of industrial origin. The mean 6 3 4 value
~ of 1974-1976 foliage from the ecologically analogous sampling locations AI through Av remained close to the mean 6 3 4 ~ value for the incinerator stack at +22.2' l o o
while the mean foliar sulphate-sulphur concentra- tion in 1974-1976 foliage decreased from 422 ppm to 185 ppm. These data clearly show that lodge- pole x jack pine trees were obtaining some of their sulphur directly from the atmosphere from sulphur gas emissions originating from the West Whitecourt Gas Plant. Needles in the upper crowns of many lodgepole x jack pine trees in the West Whitecourt study area, however, displayed foliar @S
values which were greater than those asso- ciated with incinerator stack emissions. These data when compared to the laboratory data of Wilson and others (1978) was suggestive of iso- topically selective metabolic processes function- ing in the lodgepole x jack pine foliage under field conditions
.
100'
, , , ,
, I ,
6
4
2
KILOMETERS WEST
4
KILOMETERS EAST
Figure 6. Plot of foliar sulphate-sulphur con- centration in age-classed lodgepole x jack pine foliage from eight sampling locations in the West Whitecourt study area as a function of distance from the West Whitecourt Gas Plant. foliage as a function of distance from the West Whitecourt Gas Plant. The background foliar sulphate-sulphur concentration was determined from age-classed foliage of jack pine x lodge- pole pine from the Birch Mountain Fire Tower Ill km (69 mi) NNW of Fort McMurray, Alberta. One can clearly see the decrease in foliar sulphate-sulphur concentration with increasing distance from the sulphur gas emission source. The decrease in foliar sulphate-sulphur concen- tration with distance was more pronounced with The 28-meter radio mast tower erected at the intensive experimental site provided a framework for measuring and characterizing SO2 concentration profiles of ambient air above, within and below the lodgepole x jack pine forest canopy. The vertical SO2 profiles revealed that the SO2 concentration minimum measured in the upper crown at 16 meters was orimarily due to an aerodynamic effect and was not due to the trees acting as a biological sink. This aerodynamic effect was described as a splitting of the air flow above and below the crowns of the lodgepole x jack pine trees. The measurements of foliar sulphate- sulphur, foliar total sulphur and foliar S^^S values revealed that the trees, however, were also a biological sink for sulphur gas emissions but that the rate of atmospheric sulphur uptake by the trees was so slow that it was beyond the resolution of the two Thermo Electron Model 43 Pulsed Fluorescent SO2 analyzers used. Photosynthetic rates and leaf resistances of lodgepole x jack pine trees in the West Whitecourt study area were shown to be modified. The amount of this ecological modification was a function of the distance from the West Whitecourt Gas Plant. For example, the seasonal photosynthetic rates of 1976 lodgepole x jack pine foliage were lower and the leaf resistances higher when foliage from S5 (1.5 km east) was compared with foliage from Sin (5.2 km east) (4.38 Â 1.99 mg C02/dry g/hr
versus 6.42 Â 1.28 mg C02/dry g/hr and 11.3 2
6.6 s/cm versus 7.8 5 1.9 s/cm for sample sites
S5 and Sin respectively). This relative reduc- tion in photosynthetic rates, however, was only partially attributable to increased leaf re- sistance. Additional ecological factors there- fore, such as foliar mineral nutrient status and soil pH were considered since these para- meters were known to modify plant response. A detailed analysis of foliar mineral nutrient concentration of N, P, K, Ca, Mg, Mn, Al, Fe and Zn in lodgepole x jack pine foliage from nine sampling locations (including the ecological analogues) in the West Whitecourt study area revealed that the mineral nutrient status of the lodgepole x jack pine trees had been altered. It must be remembered at this point that normal plant growth requires a balance of all essential mineral nutrients within the plant. The foliar concentration of P, K, Fe, Mg, N and Zn tended to increase while the foliar concentration of Ca and A1 tended to decrease with distance from the West Whitecourt Gas Plant and distance from the WN-SE
sulphur dioxide emission corridor. Site type was shown to be a critical factor influencing the concentration of these eight mineral nutrients. Foliar Mn concentration was found to decrease dramatically with distance from the West Whitecourt Gas Plant and distance from the W N W S E sulphur gas emission corridor. Variability of site type, however, did not modify this relationship. A low Fe to Mn ratio was found in foliage from sampling locations within 4 km of the West Whitecourt Gas Plant. The low foliar Fe concentration may contribute to the chlorotic appearance of the foliage at these locations. Foliar mineral nutrient analysis of foliage 82, 85, A1 and Slo revealed that foliar K and P were lower in concentration in foliage from S2, S5 and AT than from Sm. Since foliar K concentration has been linked with stomatal activity, the reduced foliar K concentration may be inhibiting stomatal opening thus increasing leaf resistance which would then limit photosynthetic rate. Reduced foliar P concentration may inhibit phosphorylation and thereby also limit photosynthetic rate. Foliar nutrient deficiencies of either P and K alone or in combination therefore may be partially respon- sible for the reduced photosynthetic rates ob- served in lodgepole x jack pine foliage in the West Whitecourt study area. The alteration of foliar mineral nutrient status in lodgepole x jack pine trees in the West Whitecourt study area therefore is an important ecological factor contributing to the modification of plant response. Soil pH profiles were measured at the same nine vegetation sampling locations where foliar mineral nutrient concentrations were determined since soil pH is known to affect the availablility of mineral nutrients to plants. The general trend or grad- ient in soil pH over all nine sampling locations was an increase in soil pH with depth and with distance from the West Whitecourt Gas Plant and distance from the ~
S sulphur
E
gas emission corridor. The soil pH gradient was most striking when only the ecologically analogous sampling lo- cations were considered. A direct relationship was found between lowered soil pH and the elevated levels of foliar Mn in lodgepole x jack pine trees. The foliar Mn concentration data and the soil pH data suggest that foliar Mn concentration in lodgepole x jack pine trees could be used as a mineral nutrient indicator of modification of the forest ecosystem by sulphur gas emissions. Soil total sulphur concentration in the soil profiles at the nine soil sampling locations also decreased with soil depth, distance and direction from the West Whitecourt Gas Plant. It is impor- tant to note, however, that there was no correla- tion between soil total sulphur concentration and soil pH. There was also no direct correlation between a given soil pH value and the soil f i 3 %
value. These data suggest that the soil S^S value can be used as an indicator of the presence and penetration of sulphur gas emissions into the soil profile while soil pH and soil total sulphur can be used as indicators of sulphur loading of the soil. In terms of plant biochemistry and sulphur gas emissions the most significant observation in the field was a transient metabolic effect; the ATP (adenosine triphosphate) concentration of foliage cells from lodgepole x jack pine trees was found to be directly decreased upon exposure to low-con- centration short duration SO2 fumigation (75% decrease upon fumigation with 0.14 ppm SO2 for 15 minutes).
It is important to note that when the foliage was no longer exposed to SO2 the foliar ATP concentration increased to the pre- SO2 fumigation ATP concentration (see Harvey and Legge, 1979, for details). This decrease and increase in the foliar ATP concentration was also observed with excised lodgepole x jack pine branches from the West Whitecourt study area which were fumigated under controlled conditions at the Kananaskis laboratory. When lodgepole x jack pine trees, which had been grown in the absence of sulphur gas emissions in the laboratory, were fumigated with SO2 no fluctuation in ATP concentration was observed. It is important to note that the laboratory trees had a foliar ATP content which was over twice the foliar ATP content of the lodgepole x jack pine foliage from the West Whitecourt study area (658 nmoles/dry g versus 1460 nmoles/dry g). The lower foliar ATP concentration of field grown trees compared to laboratory grown trees suggests a partial explan- ation for the lowered photosynthetic capacities reported for lodgepole x jack pine trees in the West Whitecourt study area. The photosynthetic rate of lodgepole x jack pine trees grown under controlled conditions in a non-SO2 environment in growth chambers at the Kananaskis laboratory and lodgepole x jack pine trees grown in the sulphur dioxide emission en- vironment in the field at the intensive West Whitecourt study site S5 was measured when both sets of trees were exposed to similar low concen- tration short-duration SO2 fumigations. The photosynthetic rate of the field grown plant material was not depressed by SO2 fumigation while the photosynthetic rate of the laboratory grown material was depressed by the SO2 fumiga- tions. The photosynthetic rate of the laboratory trees was much greater than the trees in the field. There was also no evidence of a plant- water deficit in lodgepole x jack pine trees severe enough to effect photosynthetic rate. Adenosine triphosphate is the major bio- chemical intermediate of energy transfer in biological systems. A decrease in foliar ATP content in lodgepole x jack pine trees caused by SO2 fumigation therefore would also be a decrease in the amount of biochemical energy available for normal metabolic functions. Al- though the ATP content of the lodgepole x jack pine foliage recovered to the pre-SO2 exposure concentration after the SO2 stress was removed, during the SO2 fumigation there would have been a net loss of biochemical energy. The fact that foliar ATP content increased after SO2 fumigation, indicated that the trees were coping with the sulphur gas emissions at the cost of a metabolic energy drain. In summary, the contrast in the biochemical and physiological responses of the lodgepole x jack pine trees fumigated with SO2 in the field and the laboratory strongly indicates that en- vironmental pre-history and acclimation of the trees to ecological modification of components of the forest ecosystem are the critical factors determining plant response to sulphur gas emissions in the West Whitecourt study area. A comparison of the mean photosynthetic capac- ities of 1976 lodgepole x jackpine foliage through the 1976 growing season at sampling loca- tions S2, S5 and Slo revealed that S10 had a positive net C02 fixation balance two to three weeks prior to the foliage at S2 and S5 and is shown in Figure 7. The mean photosynthetic capacity of 1976 Sin foliage was also always higher than the mean photosynthetic capacity measured for 1976 foliage from S2 or S5
Additionally in terms of photosynthetically active needle biomass lodgepole x jack pine branches sampled at Sl, 82, AI and S5 were chlorotic in appearance with premature abscission (needledrop) of the third year needles and poor leader growth while branches sampled at S q and Sinwere compar- atively darker green in color with a needle re- tention of from four to six years and good leader growth. The photosynthetic potential of lodge- pole x jack pine trees based upon needle biomass alone therefore was much greater at S9 and Sin compared to Sl, Sy, A1 or $5. .
Figure 7. Comparison plot of the mean photosyn- thetic capacity of 1976 foliage on lodgepole x jack pine branches from sampling sites S2, S5 and Slo from early in June to mid-September. When the observed ecological modifications of the forest ecosystem such as reduced needle bio- mass, reduced biochemical energy, reduced photo- synthetic rates, reduced soil pH, the disruption of mineral nutrient cycling, foliar sulphur load- ing and the shortened growing season are combined, and considered in the long term time sense the net effect should be measurable as a reduction in forest productivity. This decrease in forest pro- ductivity, however, would be expected to decrease with increasing distance from the sulphur gas emission source. Annual basal area increment measurements were taken from 40 lodgepole x jack pine trees at each of the five ecologically analogous sampling loca- tions AI through Av in 1976 to determine if mod- ification of the forest ecosystem was significant enough in the long term sense to be reflected in reduced wood production since the initial start- up of the West Whitecourt Gas Plant in 1961-1962. Statistical analysis of the basal area increment data shown in Figure 8 revealed that distance from the West Wh'itecourt Gas Plant, time in years, and their interaction had significant effects on the basal area increment of the lodgepole x jack pine trees from the five ecological analogues. An exponential growth curve model was determined for lodgepole x jack pine trees from Airand the growth curve of the lodgepole x jack pine trees fromA1, A1l, AIII and AIv were statistically compared to it. The basic underlying assumption was that sulphur gas emissions had not had a significant effect on the growth of the trees at Av. This analysis statistically revealed that there has been a defi- nite reduction in basal area increment in lodgepole x jack pine trees since 1962 in AI, A,.,, AIII and AIv compared to the basal area increment model for AV which was attributable to sulphur gas emissions from the West Whitecourt Gas Plant. t ions :
1.
sulphur gas emissions r e a c h t h e f o r e s t
ecosystem w i t h i n 17 km. (10.6 mi.) of
t h e source; and
2. t h e impact of sulphur g a s emissions i s
r e s t r i c t e d t o a r e a s NW and SE of t h e
West Whitecourt Gas P l a n t .
The a r e a a f f e c t e d by sulphur d i o x i d e e m i s s i n s ,
t h e r e f o r e , i s approximately 454 km 2 (175 m i )
o r 45,373 h e c t a r e s (112,130 a c r e s ) . This a r e a l
e x t e n t e s t i m a t e of impact i s c o n s e r v a t i v e because t h e 17 km d i s t a n c e i s o n l y one-half t h e
d i s t a n c e range c a l c u l a t e d u s i n g t h e simple
Gaussian plume model under a l l s t a b i l i t y c l a s s e s f o r maximum ground l e v e l c o n c e n t r a t i o n of
sulphur d i o x i d e emissions from t h e main i n cinerator stack.
It i s important t o b e a r i n mind a t t h i s
p o i n t , however, t h a t t h i s p r o j e c t e d impact
a r e a h a s n o t been uniformly modified by s u l phur gas emissions b u t r a t h e r h a s been modi f i e d i n terms of an impact g r a d i e n t extending
NW and SE from t h e West Whitecourt Gas P l a n t .
I n o t h e r words, t h e e x t e n t of ecosystem component m o d i f i c a t i o n w i l l d e c r e a s e w i t h d i s t a n c e from t h e sulphur g a s emission source.
Another f a c t o r must be considered a t t h i s
p o i n t . Sulphur emissions from t h e West Whitec o u r t Gas P l a n t have been reduced almost a n
o r d e r of magnitude s i n c e 1970 ( r e f e r t o F i g u r e 2 ) . This s i g n i f i c a n t r e d u c t i o n i n emissions
w i l l n o t o n l y g e n e r a l l y d e c r e a s e t h e magnitude
of t h e i m p a c t , o f sulphur emissions on t h e f o r e s t ecosystem, i t w i l l a l s o d e c r e a s e t h e a r e a l
e x t e n t of t h e a r e a impacted by s u l p h u r emissions
i n t h e p a s t thus allowing a p o r t i o n of t h e f o r e s t ecosystem t o recover from t h e previous
sulphur gas emission s t r e s s .
When one uses f o l i a r s u l p h a t e - s u l p h u r conc e n t r a t i o n i n lodgepole x j a c k p i n e t r e e s a s a
measure of sulphur accumulation from exposure
t o t h e c u r r e n t l e v e l of sulphur g a s emissions,
i t appears t h a t a t o l e r a b l e c o n c e n t r a t i o n i s
reached by 9-12 km (5.6-7.5 mi) of t h e West
Whitecourt Gas P l a n t . This i s i n d i c a t e d by a
decrease i n f o l i a r sulphate-sulphur concentration
w i t h n e e d l e age which i s w i t h i n t h e range o f
t h e background f o l i a r s u l p h a t e - s u l p h u r conc e n t r a t i o n . The f o l i a r &^s v a l u e s , however,
could be used t o provide a more e x a c t measure
of t h e d i s t a n c e a t which t h e presence of s u l phur gas emissions become n e g l i g i b l e t o components of t h e f o r e s t ecosystem.
5
ll
1950
I
1955
I
1960
I
1965
I
1970
I
1975
YEAR O F GROWTH
Figure 8.
Comparative p l o t s of t h e mean b a s a l
a r e a increments from 40 lodgepole
X jack pine t r e e s a t each of t h e
f i v e e c o l o g i c a l l y analagous sampling
s i t e s i n t h e West Whitecourt study
area.
The maximum r e d u c t i o n i n b a s a l a r e a increment
occurred a t A 1 and A 1 1 and p r o g r e s s i v e l y dec r e a s e d t o z e r o a t Ay. The e f f e c t of sulphur
gas emissions on b a s a l a r e a increment growth
i n lodgepole x j a c k pine t r e e s s i n c e 1961 a t
AI, AII, AIII,
and AIv r e l a t i v e t o Av i s thus
a gradient with the reduction i n basal area
increment r e s u l t i n g from sulphur gas emission
f a l l i n g t o z e r o a t Av o r 9.6 km. I f t h e t o t a l
b a s a l a r e a increment r e d u c t i o n of AT r e l a t i v e
t o Av i s averaged over t h e f o u r t e e n y e a r s s i n c e
t h e s t a r t - u p of t h e West Whitecourt Gas P l a n t ,
t h i s would correspond t o approximately a one
t o two p e r c e n t r e d u c t i o n i n b a s a l a r e a i n c r e ment growth of AI r e l a t i v e t o Av.
The a r e a l e x t e n t of p o s s i b l e m o d i f i c a t i o n of
components of t h e f o r e s t ecosystem by sulphur
g a s emission from t h e West Whitecourt Gas P l a n t
can be e s t i m a t e d u s i n g t h e following assump-
CONC LUS I O N
It i s c l e a r from t h i s c a s e study t h a t s u l phur gas emissions from t h e West Whitecourt
Gas P l a n t have modified t h e f o r e s t ecosystem
i n a number of ways. The main e c o l o g i c a l proc e s s which has been d i r e c t l y and i n d i r e c t l y
a f f e c t e d by sulphur d i o x i d e emissions i s mine r a l n u t r i e n t c y c l i n g . By p r o g r e s s i v e l y a l t e r i n g t h e mineral n u t r i e n t b a l a n c e s of ecosystem
components f o r example, t h e b i o l o g i c a l r e l a t i o n s h i p s amongst t h e components and t h e
p h y s i o l o g i c a l and biochemical f u n c t i o n s of t h e
components a r e modified. It i s t h e s e ecosystem
component modifications which are the ex- pressions of environmental deterioration re-
sulting from chronic exposure to sulphur di- oxide over time. Despite this measurable deterioration of the forest ecosystem, however, it does not appear at this time that sulphur dioxide emissions from the West Whitecourt Gas Plant have caused irreversible ecological de- gradation. With the significant reduction in sulphur emissions from the West Whitecourt Gas Plant (See Figure 2) it is not antici- pated that there will be significant irre- versible ecological modification of the forest ecosystem in the remaining 10 to 20 years of operation of the West Whitecourt Gas Plant. One philosophical dilemna has resulted from the West Whitecourt case study. There is no relationship between air quality stan- dards and the maintenance of environmental quality since the term environmental quality excludes environmental modification. No effort to date has been made to address or to quantify acceptable limits of environmental modification resulting directly or indirectly from air pollution stress despite the fact that the presence of air pollutants in the atmosphere implies that a certain amount of environmental modification is acceptable. Since, at the present time it is techno- logically and economically impossible to re- move all air pollutants from industrial pro- cesses, it is suggested that irreversible ecological modification of the environment be used as an additional criteria for limiting pollutant emissions to the atmosphere. The as- similatory capacity of the environment, in other words, must be taken into account by both industry and regulatory agencies. The uni- form application and enforcement of fixed air quality standards over a geographical area the size of the p ovince of Alberta (661,183 km2 or 255,285 mi ) with its physiographically
complex terrain, heterogeneous vegetation and diverse climatology is clearly not enough to maintain environmental quality. Future research will be required to determine the assimilatory and accumulatory capacity of the environment to pollutants and to provide the biological monitoring techniques to assure that the assimilatory and accumulatory capacity of the environment is not exceeded. After the assimilatory and accumulatory capacity of the environment have been con- sidered, flexible air quality standards may be possible. These standards could be ad- justed regionally and seasonally in order to minimize pollutant impact on the environment. All emission sources, however, would have to be viewed in the context of their regional location, projected longevity of their op- erations, composition of their emissions, the proximity of neighboring emission sources as well as regional land use priorities since it is the total pollutant load to the environment which must be considered when one uses assimilatory capacity as a measure of environmental quality. 5
The conceptual interdisciplinary nature of the West Whitecourt case study has proven to be the basis for the success in unravelling the very complex interrelated consequences of the chronic exposure of the forest ecosystem to sulphur gas emissions from the West White- court Gas Plant. It is suggested that fu- ture air pollution research on forest eco- systems follow a similar experimental design if the environmental perturbations caused by air pollution stress are to be understood. Direct extrapolation of the data summarized in this paper to other areas would be mis- leading unless local environmental factors, vegetation and pollutant parameters, are taken into consideration prior to interpretation. ACKNOWLEDGMENTS The West Whitecourt Case Study could not have been completed without the enthusiasm and cooperation of the following interdisci- plinary team members: D.R. Jaques, G.W. Harvey, H.R. Krouse, H.M. Brown, E.C. Rhodes, and M. Nosal of the University of Calgary; H.U. Schellhase of the Southern Alberta In- stitute of Technology; J. Mayo and A.P. Hartgerink of the University of Alberta; P.F. Lester from San Jose State University; and R.G. Amundson and R.B. Walker of the University of Washington. The majority of the financial support for this research was in the form of a grant-in- aid of research to the Kananaskis Center for Environmental Research of the University of Calgary from the Whitecourt Environmental Study Group. Additional financial support was received from the Research Secretariat of Alberta Environment, the Oil Sands En- vironmental Study Group (OSESG) , the Alberta
Oil Sands Environmental Research Program (AOSERP), and the University of Calgary Inter- disciplinary Sulphur Research Group (UNISUL)
A special note of thanks is in order for Mr. Ron Findlay and Mr. E. Baraniuk of AMOCO Canada Petroleum Company Limited and the rest of the Whitecourt study group members companies who had the foresight to initiate the White- court Environmental Study and the patience to see it through. Finally I wish to thank my air pollution colleagues throughout North America for their genuine interest and support during the re- search program. .
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1978. Growth of Ryegrass (Lolium perenne L.) I. Effects on photosynthesis and respi- ration. Journal of Experimental Botany 29(112):1029-1036 Faller, N. 1971. Plant nutrient sulphur- SO2 vs. So&. The Sulphur Institute Journal 7(2):5-6 Halliday, W. E. D. 1937. A forest site classification for Canada. Canadian Forest Service Bulletin 89. 50 p. Harvey, G. W., and A. H. Legge. 1979. The effect of sulfur dioxide upon the metabolic level of adenosine tri- phosphate. Canadian Journal of Botany 57(7) :759-764. Jernolov, A., and R. Rosenberg. 1976. Stress tolerence of ecosystems. Environmental Conservation 3:43-46 Johnson, C. M., and H. Nishita. 1952. Microestimation of sulfur in plant materials, soils and irrigation waters. Analytical Chemistry 24(4) :736-742. Katz, M. 1949. Sulfur dioxide in the atmosphere and its relation to plant life. Industrial and Engineering Chemistry 41(11):2450-2465. Kickert, R. N., and P. R. Miller. 1979. Responses of ecological systems. 2
Handbook of methodology for the assessment of air pollution effects on vegetation. W. W. Heck, S. V. Krupa, and S. N. Linzon, eds. fc. 14-1 to 14-45. Air Pollution
Control Association. Krouse, H. R. 1977. Sulphur isotope abundances elucidate uptake of atmospheric sulphur emissions by vegetation. Nature 265:45-46. Legge, A. H., and G. W. Harvey. 1974. Sulphur dioxide and environmental pre- conditioning of vegetation. In Whitecourt Environmental Study Report 1974. Section IV 1-29. Whitecourt Environmental Study Group AMOCO Canada Petroleum Company Limited, Calgary, Alberta. Legge, A. H., D. R. Jaques, R. G. Amundson, and R. B. Walker. 1977. Field studies of pine, spruce, and aspen periodically subjected to sulphur gas emissions. Water, Air, and Soil Pollution 8(l) :lO5-129. Legge, A. H., D. R. Jaques, H. R. Krouse, H. M. Brown, E. C. Rhodes, H. U. Schellhase, J. Mayo, A. P. Hartgerink, P. F. Lester, R. G. Amundson, G. W. Harvey, and R. B. Walker. 1978. Sulphur gas emissions in the boreal forest: the west whitecourt case study. 11. final report. Submitted to the Whitecourt Environmental Study Group. Kananaskis Center for Environmental Research Report Number 78-10. 615 p. Linzon, S. N., P. J. Temple, and R. G. Pearson. 1978. Sulfur concentrations in plant foliage and effects. Presented at the 71st Annual Meeting of the Air Pollution Control Association, Houston, Texas June 25-30, 1978. 15 p. Linzon, S. N. 1978. Effects of airborne sulfur pollutants on plants. In Sulphur in the environment. part 11: ecological impacts. J. 0. Nriagu ed. p. 110-162. John Wiley & Sons, N. Y.
Lowe, L. E., A. Sasaki, and H. R. Krouse. 1971. Variations in sulphur-34: sulphur-32 ratios in soil fractions in western Canada. Canadian Journal of Soil Science 51:129-131. Miller, P. R., and J. R. McBride. 1975. Effects of air pollutants on forests. In Responses of plants to air pollution.
J. B. Mudd and T. T. Kozlowski, eds. p. 192-235. Academic Press, New York. Miller, P. R., R. N. Kickert, 0. C. Taylor, R. J. Arkley, F. W. Cobb Jr., D. L. Dahlsten, P. J. Gersper, R. F. Luck, J. R. McBride, J. R. Parmeter Jr., J. M. Wenz, M. White, and W. W. Wilcox. 1977. Photochemical oxidant air pollutant effects on a mixed conifer forest ecosystem. A progress report 1976. Ecological Re- search Series EPA-600/3-77-104. U. S. Environmental Protection Agency, Corvallis, Oregon. 339 p. Noggle, J. C., and H. C. Jones. 1979. Accumulation of atmospheric sulfur by plants and sulfur-supplying of soils. Interagency ~nergy/~nvironment
R &
D
Program Report. TvA/oNR-~~/~O.
EPA-600/7-
79-109. U. S. Environmental Protection Agency. Washington, D.C. 37 p. Odum, E. P. 1971. Fundamentals of ecology. W. B. Saunders Company, Toronto. 574 p. Smith, W. H. 1974. Air pollution-effects on the structure and function of the temperate forest eco- system. Environmental Pollution 6:111-129. .
Tamm, C O., and A. Aronsson.
1972. Plant growth as affected by sulphur compounds in polluted atmosphere. A literature survey. Research Notes Number 12. Department of Forest Ecology and Forest Soils. Royal College of Forestry. Stockholm, Sweden. 53 p. Tel-man, G. L. 1978. Atmospheric sulphur-the agronomic as- pects. Technical Bulletin Number 23. The Sulphur Institute. Washington, D.C. 15 p. Thompson, R. C . , and G. Kats.
1978. E f f e c t s of continuous H2S fumigation
on c r o p and f o r e s t p l a n t s . Environmental
Science and Technology 12(5):550-553.
U l r i c h , A . , M. A . Tabatabai, K. Ohki, and C . M.
Johnson.
1967. S u l f u r c o n t e n t of a l f a l f a i n r e l a t i o n
t o growth i n f i l t e r e d and u n f i l t e r e d a i r .
P l a n t and S o i l 26(2):235-252.
Wilson, L. G . , R. A . Bressan, and P. F i l n e r .
1978. Light dependent emission of hydrogen
s u l f i d e from p l a n t s . P l a n t Physiology
61:184-189.
Effects of Airborne F on Forest
Ecosystems'
Robert G. Amundson and Leonard H. Weinstein
A b s t r a c t : Although t h e r e a r e many r e p o r t s of f l u o r i d e (F)
i n j u r y t o f o r e s t s , t h e r e have been no s y s t e m a t i c s t u d i e s on
t h e f o r e s t ecosystem. I n t h i s p a p e r , we have reviewed t h e
p r e s e n t s t a t e of o u r knowledge on F p o l l u t i o n and e f f e c t s
on p h y s i o l o g i c a l p r o c e s s e s , t r e e growth, F accumulation
and p l a n t i n j u r y , community s t r u c t u r e , i n t e r a c t i o n w i t h
pathogens and i n s e c t s , and d i s t r i b u t i o n of F i n t h e environment. The p r e p a r a t i o n of t h i s review i n d i c a t e d t h e many
a r e a s of t h e F-plant i n t e r a c t i o n on which t h e r e i s no i n f o r n a t i o n , where i t i s poorly understood, o r where a v a i l a b l e
i n f o r m a t i o n i s h i g h l y c o n t r o v e r s i a l . I n some c a s e s , we
have j o i n e d t h e c o n t r o v e r s y .
I n j u r y t o f o r e s t t r e e s p e c i e s by a i r b o r n e
f l u o r i d e (F) h a s been r e p o r t e d i n many p a r t s o f
t h e world ( e . g . , Adams and o t h e r s , 1952; Horntvedt
and Robak, 1975; Niklfeld.1975; EPA, 1973; F l i i i l e r
and o t h e r s , 1979), b u t many F-emitting s o u r c e s a r e
i n a g r i c u l t u r a l o r urban a r e a s and r e p o r t s of
i n j u r y t o agronomic c r o p s , ornamental and urban
t r e e s ( e . g . , Bolay and Bovay, 1965; Facteau and
M e l l e n t h i n , 1976; de Ong, 1946; Leonard and Graves,
1966) o r on f l u o r i d e accumulation and p r o d u c t i o n
of f l u o r o s i s i n l i v e s t o c k and o t h e r h e r b i v o r e s
( S u t t i e , 1977) a r e a l s o common.
The p r i n c i p a l i n d u s t r i a l s o u r c e s of a i r b o r n e
F a r e primary aluminum s m e l t i n g ; s t e e l manufacture;
conversion of f l u o r a p a t i t e t o phosphate and phosphorus; and g l a s s , ceramic and b r i c k p r o d u c t i o n .
N a t u r a l s o u r c e s of a i r b o r n e F a r e p r i n c i p a l l y
from s o i l p a r t i c l e s , fumaroles, and volcanoes.
The a s h from t h e r e c e n t e r u p t i o n of Mount S t .
Helens c o n t a i n e d 8 ppm s o l u b l e F ( S t o i b e r and
o t h e r s , 1980) and 400 ppm t o t a l F and i t s impact
on f o r e s t s i n t h e n o r t h w e s t e r n U.S. w i l l b e
p r e s e n t e d a t t h e Symposium on E f f e c t s of A i r
P o l l u t a n t s on Mediterranean and Temperate F o r e s t
Ecosystems, J u n e 22-27, 1980, R i v e r s i d e ,
C a l i f o r n i a , U.S.A.
z
Research A s s o c i a t e and Program D i r e c t o r ,
Environmental Biology, r e s p e c t i v e l y . Boyce
Thompson I n s t i t u t e a t C o r n e l l U n i v e r s i t y , I t h a c a ,
New York.
watched c a r e f u l l y .
R e s u l t s of o n l y a few f i e l d s t u d i e s made n e a r
F-emitting s o u r c e s a r e a v a i l a b l e i n t h e s c i e n t i f i c l i t e r a t u r e . One r e a s o n f o r t h e absence of
more r e p o r t s i s t h a t t h e s t u d i e s were o f t e n rout i n e and n o t q u a n t i t a t i v e , making p u b l i c a t i o n i n
r e f e r e e d j o u r n a l s d i f f i c u l t . A second r e a s o n i s
t h a t r e s u l t s of a s t u d y performed f o r a n i n d u s t r y
may b e s e q u e s t e r e d from p u b l i c a t i o n o r o t h e r u s e
because of a c t i v e , pending, o r p o t e n t i a l l i t i g a t i o n . Often, f i e l d s t u d i e s t h a t have been d i s t r i b u t e d were i n a form t h a t was n o t s u b j e c t e d t o
p e e r review, was c a r e l e s s l y assembled, a n d / o r
r e f l e c t e d t h e p e r s o n a l b i a s e s of t h e a u t h o r s .
Because of t h e s e problems, we have n o t confined
t h i s review t o works p u b l i s h e d i n j o u r n a l s , b u t
we have t r i e d t o judge t h e r e p o r t s t h a t we have
c i t e d i n terms of t h e i r p e r t i n e n c e a n d / o r a v a i l a b i l i t y , and o u r p e r s o n a l views a r e o f t e n pres e n t e d . Host i n t e r n a l r e p o r t s were avoided, b u t
t h e l a c k of p u b l i s h e d i n f o r m a t i o n o f t e n l e f t no
r e c o u r s e b u t t o c i t e them. We hope t h a t we have
s t a t e d o u r c r i t i c i s m s of some s t u d i e s a s f a i r l y
a s possible.
LABORATORY STUDIES ON PLANT PRODUCTIVITY
The p r o d u c t i v i t y of t h e p l a n t depends upon t h e
c o o r d i n a t i o n and r a t e o f CO-; a s s i m i l a t i o n , resp i r a t i o n , t r a n s p i r a t i o n , t r a n s l o c a t i o n of photos y n t h a t e , m i n e r a l n u t r i t i o n , growth, and reprod u c t i o n . The amount of i n f o r m a t i o n a v a i l a b l e on
t h e impact of a i r b o r n e F on t h e s e p r o c e s s e s
ranges from v i r t u a l l y none, e . g . , on t r a n s l o c a t i o n
of p h o t o s y n t h a t e s , t o a moderate amount, e.g., on
C02 a s s i m i l a t i o n (apparent p h o t o s y n t h e s i s ) and
respiration.
There a r e few d a t a on t h e chemical composit i o n , d i s t r i b u t i o n , and p a t t e r n s and frequency
of exposure of atmospheric F i n t h e f i e l d . One
reason f o r t h i s is t h a t a i r monitors with
s h o r t a v e r a g i n g times have n o t been g e n e r a l l y
a v a i l a b l e . Because F c o n c e n t r a t i o n s i n t h e amb i e n t a i r have n o t been c h a r a c t e r i z e d and f l u c tuating F concentrations a r e d i f f i c u l t t o control,
t h e d e s i g n of meaningful l a b o r a t o r y o r c o n t r o l l e d
f i e l d experiments i s formidable. The i n f o r m a t i o n
t h a t i s a v a i l a b l e i s g e n e r a l l y f o r a v e r a g i n g times
of 1 2 o r 24 h o u r s (McCune and o t h e r s , 1976) and
t h e peak F c o n c e n t r a t i o n s t h a t occur n e a r s o u r c e s
a r e n o t known. T h i s i n f o r m a t i o n would b e v e r y
u s e f u l s i n c e i t h a s been shown f o r o t h e r a i r
p o l l u t a n t s , such a s S02, t h a t s h o r t - t e r m peak
exposures a r e more i m p o r t a n t i n e x p l a i n i n g p l a n t
damage t h a n a v e r a g e c o n c e n t r a t i o n s (McLaughlin
and o t h e r s , 1979). U n f o r t u n a t e l y , most l a b o r a t o r y
s t u d i e s have employed continuous exposures a t
c o n s t a n t c o n c e n t r a t i o n s t h a t do n o t s i m u l a t e
f i e l d exposures. For t h e s e r e a s o n s t h e d a t a
a v a i l a b l e a r e of l i m i t e d v a l u e i n p r e d i c t i n g t h e
impact of a i r b o r n e F on f o r e s t ecosystems.
Gas Exchange
Apparent P h o t o s y n t h e s i s
Given t h e problems o u t l i n e d above, i t i s n o t
s u r p r i s i n g t h a t t h e r e have been s o few s t u d i e s on
t h e e f f e c t s o f F on a p p a r e n t p h o t o s y n t h e s i s (AP)
of f o r e s t tree s p e c i e s (Table 1 ) . Consequently,
we have i n c l u d e d i n Table 1 n o t o n l y s t u d i e s on
f o r e s t t r e e s b u t a l s o t h o s e on h o r t i c u l t u r a l
s p e c i e s exposed t o hydrogen f l u o r i d e (HF) o r
s u p p l i e d w i t h sodium f l u o r i d e (NaF). We have
a r b i t r a r i l y s e p a r a t e d experiments w i t h HF i n t o
a c u t e exposures (over 1 0 pg m 3 f o r a few 'days o r
l e s s ) and c h r o n i c exposures (ca. 5 \E HF m 3 o r
l e s s f o r a few days t o more t h a n a growing s e a s o n ) ,
a l t h o u g h we r e c o g n i z e t h a t many exposures c l a s s i f i e d a s c h r o n i c could more r e a l i s t i c a l l y b e
c l a s s i f i e d a s a c u t e . Exposures t o s o l u t i o n s cont a i n i n g NaF have v a r i e d from s e v e r a l h o u r s t o
months and w i l l b e d i s c u s s e d i n d i v i d u a l l y .
Acute exposures -- With t h e e x c e p t i o n of c o t t o n ,
where h i g h c o n c e n t r a t i o n s of HF had no e f f e c t
(Thomas, 1 9 5 8 ) , a c u t e exposures have c o n s i s t e n t l y
reduced AP (Thomas and Hendricks, 1956; Thomas,
1958; H i l l , 1969; Bennett and H i l l , 1973).
Bennett and H i l l (1973) exposed a l f a l f a t o HF f o r
2 h o u r s and found t h a t (1) approximately 120 yg m-3
HF were needed t o produce f o l i a r n e c r o s i s ; (2)
about 40 pg m-3 were n e c e s s a r y t o c l e a r l y i n h i b i t
AP; (3) t h e d e p r e s s i o n of AP and subsequent recove r y a f t e r exposure were slower f o r HF t h a n f o r t h e
o t h e r major a i r p o l l u t a n t s t e s t e d (S02, 03, N02,
NO and Cl2).
They a l s o noted t h a t of t h e p o l l u t a n t s t e s t e d , HF p r o d u c e d - t h e g r e a t e s t r e d u c t i o n
i n AP f o r an e q u i v a l e n t p o l l u t a n t dose, b u t s t a t e d
t h a t t h e occurrence i n the f i e l d of a concentrat i o n t h a t would produce a 1 0 p e r c e n t r e d u c t i o n i n
AP would b e r a r e . One can conclude t h a t a s i g n i f i c a n t i n f l u e n c e of a n a c u t e exposure on p l a n t
community p r o d u c t i v i t y would l i k e l y b e preceded
by l e s i o n s and a b s c i s s i o n o f f o l i a g e .
Chronic exposures -- S e v e r a l i n v e s t i g a t o r s
have r e p o r t e d t h a t c h r o n i c exposure t o HF had no
e f f e c t on AP i f t h e r e was no v i s i b l e i n j u r y ( H i l l ,
1969; H i l l and o t h e r s , 1958; Thompson and o t h e r s ,
1967), and when f o l i a r i n j u r y o c c u r r e d , t h e red u c t i o n i n AP was p r o p o r t i o n a l t o ( H i l l , 1969;
Thomas and Hendricks, 1956; Thomas, 1958) o r
g r e a t e r t h a n t h e amount of f o l i a g e i n j u r e d (Thomas,
1958, f o r f r u i t t r e e s ; and Woltz and Leonard, 1964,
f o r c i t r u s ) . Thomas (1958) proposed t h a t t h e r e i s
a t h r e s h o l d of F c o n c e n t r a t i o n and d u r a t i o n o f exposure f o r each s p e c i e s above which AP i s reduced
more t h a n can b e accounted f o r by c h l o r o s i s and
necrosis.
McCune and o t h e r s (1976) d e s c r i b e d experiments
i n which field-grown sorghum was exposed f o r 14
days t o t h r e e c o n c e n t r a t i o n s of HF (0.7, 1 . 7 and
3.5 t o > 5 yg m-3) and AP of t h e whole p l a n t
canopy was measured t h r e e t i m e s d a i l y b e f o r e ,
d u r i n g , and a f t e r t h e exposure p e r i o d s . The l o w e s t
HF c o n c e n t r a t i o n had no e f f e c t on AP; t h e i n t e r mediate c o n c e n t r a t i o n reduced AP d u r i n g t h e expos u r e p e r i o d , b u t immediate recovery o c c u r r e d upon
c e s s a t i o n o f t h e exposures. P l a n t s s u b j e c t e d t o
t h e h i g h e s t c o n c e n t r a t i o n a l s o had reduced r a t e s
of AP f o r t h e f i r s t week. But when t h e HF concenm-3 on t h e
t r a t i o n was r a i s e d t o g r e a t e r t h a n 5
e i g h t h day, s e v e r e f o l i a r i n j u r y o c c u r r e d , t h e
r a t e s of AP dropped d r a s t i c a l l y , and t h e r e was no
recovery i n t h e post-exposure p e r i o d .
I n an e x t e n s i v e s e r i e s o f experiments, K e l l e r
(1977) p l a c e d 11 d i f f e r e n t t r e e s p e c i e s ( s e e
Table 1 ) a t v a r y i n g d i s t a n c e s from a s o u r c e of a i r borne F f o r s e v e r a l months and measured r a t e s of AP
on t h e whole p l a n t s r e t u r n e d t o t h e l a b o r a t o r y .
Exposure t o F produced f o l i a r i n j u r y and a b s c i s s i o n ,
and reduced t h e r a t e o f AP of t h e whole p l a n t .
The
r e d u c t i o n i n AP o f t h e whole p l a n t was due p r i m a r i l y
t o t h e l o s s of f o l i a g e , because t h e r a t e of AP of
n e e d l e s remaining on t h e p l a n t s was a s h i g h a s t h o s e
on c o n t r o l p l a n t s .
Sodium f l u o r i d e -- Navara (1963) r e p o r t e d b o t h
d e p r e s s i o n and s t i m u l a t i o n of AP of beans grown i n
s o l u t i o n c u l t u r e f o r 16 days w i t h 0.03 o r 0.3 ppm
NaF, w h i l e t h o s e s u p p l i e d w i t h 3 ppm had d e p r e s s e d
r a t e s of AP. When P i c e a e x c e l s a Link. c u t t i n g s were
watered p e r i o d i c a l l y through t h e w i n t e r and s p r i n g
w i t h d e i o n i z e d w a t e r c o n t a i n i n g 100 ppm NaF, t h e
AP r a t e s were n o t o n l y reduced b u t n e c r o s i s was
produced on t h e newly f l u s h e d f o l i a g e . The F conc e n t r a t i o n s i n t h e new f o l i a g e t h a t e x h i b i t e d
i n j u r y contained o n l y 3.7 t o 8 ppm when i n j u r y
f i r s t o c c u r r e d . By t h e end of J u l y , t h o s e n e e d l e s
t h a t s u r v i v e d c o n t a i n e d from 31.5 t o 52.2 ppm F
( K e l l e r , 1980).
McLaughlin and Barnes (.I9751 exposed c u t
b r a n c h l e t s of t h r e e p i n e s p e c i e s and l e a v e s of s i x
deciduous t r e e s t o 0 , 1 . 9 , 1 9 , and 190 pprn NaF f o r
24 hours and then measured t h e r a t e s of APT With
1 . 9 pprn NaF, t h e r a t e s of AP of o l d e r n e e d l e s of
e c h i n a t a M i l l . were
Pinus t a e d a L. and
-reduced w h i l e t h e o t h e r s p e c i e s were u n a f f e c t e d
(s-ee Table 1 f o r s p e c i e s used).
Needles
w i t h reduced r a t e s of AP contained l e s s than 1 0
pprn F. Although low c o n c e n t r a t i o n s of f o l i a r F
reduced AP and s t i m u l a t e d r e s p i r a t i o n , t h e a u t h o r s
warn of t h e l i m i t a t i o n s of e x t r a p o l a t i n g laborat o r y d a t a t o t h e f i e l d s i t u a t i o n . However, t h e i r
d a t a r a i s e d s e v e r a l q u e s t i o n s : (1) What concent r a t i o n of HF would be necessary t o i n c r e a s e t h e
f o l i a r F c o n c e n t r a t i o n 4-8 pprn i n a 24-hour p e r i o d
a s d i d t h e comparable dose of NaF? (2) I f upon
exposure t o HF, a branch on a t r e e accumulated F
a t t h e same r a t e , would t h e r e d u c t i o n i n AP be
permanent o r would i t recover t o t h e pre-exposure
r a t e ' a f t e r t h e exposure? (3) Would t h e 4-8 pprn
increase i n f o l i a r F associated with the reduction
i n AP produce v i s i b l e i n j u r y ? One could view t h i s
kind of exposure a s a c u t e , because t h e comparable
dose of HF t o accumulate t h i s amount of F i n 24
assuming an accumulahours could be 4-8 -ng m--,
t i o n c o e f f i c i e n t of 1 pprn p g l m3 daym1.
and a p r i c o t exposed t o 70 pg mV3 HF. But Thompson
and o t h e r s (1967) d i d n o t f i n d s i g n i f i c a n t d i f f e r ences i n water use of c i t r u s exposed over a growing
season t o e i t h e r ambient l e v e l s of F o r f i l t e r e d
a i r w i t h added F (both < 0.5 v& m-3) compared t o
c o n t r o l p l a n t s . Amundson and o t h e r s ( i n review)
exposed corn t o 1 . 5 lie mF3 HF continuously f o r
one week and found an i n c r e a s e d r a t e of t r a n s p i r a t i o n over c o n t r o l s . The d a t a a v a i l a b l e on F
e f f e c t s on t r a n s p i r a t i o n a r e v a r i a b l e and i n s u f f i c i e n t t o p r e d i c t p o s s i b l e e f f e c t s on p l a n t comun i t y water r e l a t i o n s . However, s i n c e F can e l i c i t
changes i n stomata1 a p e r t u r e , t h e s e e f f e c t s may b e
important i n a f o r e s t ecosystem where water
d e f i c i t s l i m i t AP a t c e r t a i n times of t h e day o r
y e a r (Larcher, 1975; Kramer and Kozlowski. 1979).
Respiration
Since F a l t e r s normal p l a n t metabolism,
e f f o r t s have been made t o i d e n t i f y m e t a b o l i t e s
t h a t could be used a s i n d i c a t o r s of i n c i p i e n t F
i n j u r y . Yee-Meiler (1975) found t h a t non-specific
e s t e r a s e a c t i v i t y i n young Norway s p r u c e (Picea
a b i e s [L.] K a r s t . ) and European w h i t e b i r c h
(Betula verrucosa Ehrh.) exposed t o a i r b o r n e F
was i n c r e a s e d l a t e i n t h e growing season without
t h e appearance of i n j u r y symptoms. Needles of
c o n i f e r s placed a t varying d i s t a n c e s from an i n d u s t r i a l F source had s i g n i f i c a n t i n c r e a s e s i n
phenols i f they came from t r e e s w i t h F i n j u r y
(Yee-Meiler, 1977). The r e s u l t s were v a r i a b l e
f o r deciduous t r e e s . K e l l e r and Schwager (1971)
found i n c r e a s e d peroxidase a c t i v i t y i n l e a v e s of
seven t r e e s p e c i e s exposed t o an i n d u s t r i a l source
of HF and noted t h a t t h e enzyme a c t i v i t y i n c r e a s e d
b e f o r e o r i n t h e absence of development of F
i n j u r y symptoms. Unfortunately, many environmental
s t r e s s e s and l a b o r a t o r y manipulations can i n c r e a s e
pei-oxidase a c t i v i t y , l i m i t i n g t h e u s e f u l n e s s of
t h i s a s s a y (Endress and o t h e r s , 1980).
P.
R e s p i r a t i o n (measured a s oxygen uptake) was
s t i m u l a t e d i n i n t a c t p l a n t s (Applegate and Adams,
1960a; Applegate and o t h e r s , 1960) o r i n t i s s u e s
from i n t a c t p l a n t s fumigated w i t h HF, i n t h e
absence (Weinstein, 1961; Applegate and Adams,
1960b; Yu and M i l l e r , 1967; M i l l e r and M i l l e r ,
1974) o r presence of f o l i a r l e s i o n s ( H i l l and
o t h e r s , 1959). F l u o r i d e i n h i b i t i o n of oxygen
uptake h a s a l s o been r e p o r t e d and was dependent
on p l a n t t i s s u e age (Bejaoui and P i l e t , 1975)
d u r a t i o n of exposure (Applegate and Adams, 1960a),
n u t r i e n t s t a t u s (Applegate and Adams, 1960b), and
t i s s u e F c o n c e n t r a t i o n s (Applegate and o t h e r s ,
1960). However, t h e r a t e of r e s p i r a t i o n of some
t i s s u e s i s r e l a t i v e l y i n s e n s i t i v e t o F ( H i l l and
o t h e r s , 1959; Givan and Torrey, 1968). I n t h e i r
experiments w i t h c u t b r a n c h l e t s of p i n e s and hardwoods s u p p l i e d w i t h 1 , 9 , 19 o r 190 pprn NaF i n
s o l u t i o n f o r 24 h o u r s , McLaughlin and Barnes (1975)
found t h a t t h e lower two c o n c e n t r a t i o n s g e n e r a l l y
s t i m u l a t e d r e s p i r a t i o n (measured a s C02 e v o l u t i o n )
while the highest concentration both stimulated
and i n h i b i t e d r e s p i r a t i o n , depending on t h e
species.
T r a n s p i r a t i o n and Water Use
There a r e few r e p o r t s on t h e e f f e c t s of F on
t r a n s p i r a t i o n . Navara (1963) grew beans i n
s o l u t i o n c u l t u r e s c o n t a i n i n g 0.03, 0.3, and 3.0
pprn F and found reduced r a t e s of t r a n s p i r a t i o n
a f t e r 12 and 16 days i n p l a n t s s u p p l i e d w i t h t h e
two h i g h e s t c o n c e n t r a t i o n s of F. Soybeans fumig a t e d w i t h 12 -ng m-- HF had d r a m a t i c a l l y reduced
r a t e s of t r a n s p i r a t i o n w i t h i n 4 hours (Poovaiah
and Wiebe, 1973). This a g r e e s w i t h Navara and
Kozinda (1967) who found s i m i l a r r e s u l t s i n bean
p l a n t ' Metabolism
F has long been used a s a metabolic i n h i b i t o r
and t h e l i s t of published r e p o r t s of F e f f e c t s on
enzyme systems and metabolic p r o c e s s e s i s e x t e n s i v e .
Many of t h e e f f e c t s of F on p l a n t metabolism have
been reviewed (McCune and Weinstein, 1971; Chang,
1975) and Horsman and Wellburn (1976) have comp i l e d a u s e f u l l i s t of F-induced metabolic responses.
Mineral N u t r i t i o n
Wide d i f f e r e n c e s i n t h e response of peaches
t o HF l e d t o t h e f i r s t s t u d y of t h e i n f l u e n c e of
mineral n u t r i t i o n on HF s u s c e p t i b i l i t y (Brennan
and o t h e r s , 1950). With low o r d e f i c i e n t amounts
of N , Ca, and P i n tomato f o l i a g e , t h e r e was reduced uptake of NaF by r o o t s o r HF by l e a v e s ;
s i m i l a r r e s u l t s were found w i t h e x c e s s i v e amounts
of N and Ca (Brennan and o t h e r s , 1950). Other
s t u d i e s have r e s u l t e d i n i n c r e a s e d f o l i a r F i n
P-, K-, o r Fe-deficient beans (Applegate and Adams,
1 9 6 0 ~ ) ;reduced f o l i a r F i n Mg-deficient tomato
p l a n t s (MacLean and o t h e r s , 1969); s m a l l e r f r u i t s
i n Ca-deficient tomato p l a n t s (Pack, 1966); and
i n c r e a s e d t o l e r a n c e t o HF exposure i n tomato p l a n t s
Table 1.
Reported e f f e c t s o f f l u o r i d e (HF and NaF) on a p p a r e n t p h o t o s y n t h e s i s (as measured by changes i n
C02 u p t a k e ) o f h i g h e r p l a n t s .
Genus o r S p e c i e s
Concentration
p g m-3 HF
Gladiolus
0.8
Hordeum
Medicago
Fruit trees
-
2 hours
2 hours
AP reduced d u r i n g exposure w i t h
r e c o v e r y a f t e r exposure
Bennett &
Hill
1973
4 weeks
3 weeks
no e f f e c t
no e f f e c t
Hill &
others
1959
14 p e t . r e d u c t i o n i n AP 1 0 p e t . i n j u r y
Thomas
1958
2.1 av.
3.1
Gossypium
-
5.2
13.6
Citrus
.32 -.77
Gladiolus
0.8
1.2
2.3
183 h o u r s
30-205 days
growing s e a s o n
no e f f e c t
0.7
2.2 t h e n 1.7
3.5 t h e n 5+
1 4 days
1212 days
717 days
Pinus s y l v e s t r i s
P.
nigra
P.
strobus
Larix l e p t o l e p i s
1
Quercus b o r e a l i s
Pseudotsuga m e n z i e s i i
Picea excelsa
Ainus incana
Sorbus A r i a
-Acer p s e u d o p l a t a n u s
L a r i x decidua.
ambient
near
source
p e t . r e d u c t i o n i n AP = p e t . l e a f i n j u r y
no e f f e c t
38
5.1112
1.6
7.7
Lycopersicon
Prunus
Zea
t o t a l i n t e r r u p t i o n i n AF' w i t h
r e c o v e r y i n few h o u r s t o days
138 h o u r s
39 days
27 days
6 3 days
1 day
1 7 / 2 1 days
42 days
1 6 days
Fragaria
Thomas &
Hendricks 1956
32
32
F r u i t trees
Gladiolus
p e t . r e d u c t i o n i n AP = p e t . i n j u r y
4-8 h o u r s
4-8 h o u r s
4-8 h o u r s
1.4 - 5.2
0.9 -11.2
Lycopersicon
7 days
Reference
32
200
16-40
Hordeum
Medicago
Sorghum
8.0
Response
Duration
Nov- A p r i l
no
3
no
50
no
no
no
Thompson o t h e r s 1967
Hill
effect
pet. reduction over i n j u r y
effect
pet. reduction
effect
effect
effect
1969
no e f f e c t
reduced w i t h r e c o v e r y a f t e r exposure
reduced d u r i n g 3.5 exposure t h e n
severely injured l i t t l e recovery
McCune &
o t h e r s 1976
reduced AP of whole p l a n t due t o l o s s
o f f o l i a g e w i t h v A s i b l e i n j u r y on
remaining f o l i a g e
Keller
1977
McLaughlin
others
1975
I
--
1
Cornus f l o r i d a
1.9 ppm
Liquidambar S t y r a c i f l u a
NaF
Plantanus occidentalis
Acer rubrum
1 9 PPm
-I
Liriodendron t u l i p i f e r a
NaF
O x y d e n d r s arboreurn
Pinus s t r o b u s
1 9 0 ppm
P.
taeda
P.
echinata
Picea excelsa
100 ppm
24 h o u r s
AP reduced i n o l d e r n e e d l e s of
t a e d a and P. e c h i n a t a
--
24 h o u r s
AP reduced i n a l l s p e c i e s
24 h o u r s
AP reduced i n all s p e c i e s
winter- spring
2.
AP reduced i n o l d f o l i a g e l n e w i n j u r e d
&
K e l l e r 1980
grown with excess Mg (MacLean and others, 1976). There is little information on the effects of F on forest tree nutrition, but there is a con- siderable amount of information on mineral cycling in forest ecosystems (Grier and Cole, 1972; Bormann and Likens, 1979), and airborne F can influence this cycling in forest vegetation (see "Tree Growth"). sources. Thirdly, the source strength is often known and can be applied to dispersion modelling. Fourthly, F is not very mobile in plants and tends to accumulate along the margins and distal end of the leaf. Consequently, most of the F that enters a leaf remains, except for that lost by weathering and perhaps a small amount by trans- location. But, as mentioned earlier, one major drawback is the difficulty of monitoring ambient concentrations. Growth and Production Effects of F on the physiology and metabolism of plants are ultimately manifested as changes in the height, diameter, dry weight, and reproduction of the plant. But most of the available litera- ture describes studies with agronomic crops. Relatively low concentrations of F have been reported to stimulate growth, but growth can be inhibited by amounts of foliar F that do not pro- duce chlorosis or necrosis in the same species (Treshow and Harner, 1968). The effects of F on reproduction have been demonstrated and its possible implications dis-
cussed by Pack and Sulzbach (1976). They hypoth- esized that lowered seed production was a result of inhibition of pollen germination or pollen tube growth, inhibiting or preventing, fertilization. Growth of pollen tubes in apricot (Facteau and Rowe, 1977) and sweet cherry (Facteau and others, 1973) was reduced by HF fumigation during flower- ing, but Dinh and others (1973) found no effect on sweet cherry pollen tube growth after exposure to 97 pg F m-3. Joint Action with Other Pollutants Experiments on the joint action of HF with other pollutants have emphasized effects on F accumulation (Matsushima and Brewer, 1972; Mandl and others, 1975, 1980), foliar lesions (Solberg and Adams, 1956; Hitchcock and others, 1962; Mandl and others, 1975, 1980); and growth and yield (Hatsushima and Brewer, 1972; Mandl and others, 1980). Field studies that attempt to determine the response of plants or plant connnuni- ties to F emissions must consider not only environ- mental and edaphic factors (Treshow and others, 1967), but also the presence of other pollutants (Bunce, 1978; McClenahen, 1978; Carlson, 1978) that complicate assessment of the impact of F alone. McCune (1980) has discussed published and unpublished results of experiments with HF in combination with S02, 03, and N02. FIELD STUDIES F has many characteristics that make it an ideal toxicant to study in an ecosystem. Firstly, it is an apparently non-essential element that normally occurs in foliar tissues at a concentra- tion of <10 ppm; thus, the presence and amount of airborne contamination can be measured. Secondly, F is easily identified with specific emission Smith (1974) recognized three broad classes of air pollutant-dose relationships with respect to potential impacts on forest ecosystems. The Class I relationship pertains to a very low dose where the forest acts as a sink for the pollutant and the impact may be immeasurable or stimulatory. A moderate dose relationship (Class 11) is ex- pected to cause significant direct and indirect physiological impairment to individuals resulting in reduced growth, reproduction and/or increased morbidity. With a high dose (Class 111), there is acute morbidity resulting in ecosystem simplifica- tion with drastic changes in primary productivity, mineral cycling, succession, etc. All three pollutant-dose relationships have been described in one form or another around F sources (Bunce, 1978; Treshow and others, 1967; Carlson and Dewey, 1971; Wheeler, 1972). Fluoride Accumulation in Soils The amount of total F in soils that has been reported ranges up to 8300 ppm but is generally from 20-500 ppm (Weinstein, 1979). In general, plants are poor accumulators of soil F (Hansen, 1958; MacIntire and others, 1949; Merriman and Hobbs, 1962; McClenahen, 1976), but there are some exceptions, notably species of Theaceae, such as tea and camellia (Zimmerman and others, 1957; Zimmerman and Hitchcock, 1956), hickories and flowering dogwood (McClenahen, 1976). The deposition of fluoride in soils near sources of emission has been the subject of several in-
vestigations. McClenahen (1976) examined the geo- graphic distribution of total F in soils at two seasons and at different distances from an alumina reduction smelter. Of course, the highest accumu- lations occurred in the direction of the prevail- ing winds and extended about 10 km. In areas where F deposition was lowest, total F increased with depth of the soil profile, but the opposite was true in areas where deposition was heaviest. There was a lower concentration of F in the soil profile in outlying areas than near the source. The total F in the soil profile in low and high
impact areas over the two-year study period was consistently different. No attempt was made to correlate soil F with the amount of F accumulated by plants. Relatively large amounts of F-containing amendments are necessary to increase the accumula- tion of 7 in plants (Weinstein, 1977), and Israel (1974) has estimated that each 120 vg/g increment i n s o i l F r e s u l t e d i n a gain i n f o r a g e F of 1 ?~g/g.
The accumulation of F i n c o n i f e r n e e d l e s and i n
l'soil-humus" samples n e a r a phosphorus p l a n t i n
Canada h a s been s t u d i e d (Thompson and o t h e r s , 1979;
Sidhu, 1977). S e v e r i t y of damage t o v e g e t a t i o n was
r e p o r t e d t o be c o r r e l a t e d w i t h F c o n c e n t r a t i o n of
f o l i a g e and of "soil-humus".
Because t h e d i s t r i b u t i o n of a i r b o r n e F i n s o i l s would be expected t o
follow t h e same p a t t e r n a s i n v e g e t a t i o n , i t would
be d i f f i c u l t t o e s t i m a t e t h e p r o p o r t i o n of F prese n t i n f o l i a g e t h a t was accumulated from t h e atmosphere and t h a t from t h e s o i l . Water-soluble F from
t h e "soil-humus" was p o s i t i v e l y c o r r e l a t e d w i t h
f o l i a r F and because t h e s o i l s were h i g h l y a c i d i c ,
r o o t uptake could have been an important pathway
i n t o t h e vegetation.
The s o i l a s a s o u r c e of F t o p l a n t s has n o t been
adequately i n v e s t i g a t e d and t h e long-term e f f e c t
of a c i d i c p r e c i p i t a t i o n i n making s o i l F a v a i l a b l e
t o p l a n t s , especially i n a c i d i c , non-agricultural
s o i l s should be i n v e s t i g a t e d .
There a r e many
o t h e r gaps i n our understanding of t h e c y c l i n g
of F i n f o r e s t ecosystems, such a s t h e e f f e c t s of
F accumulation on l i t t e r decomposition,on changes
i n n u t r i e n t a v a i l a b i l i t y , and on s o i l s t r u c t u r e .
F Accumulation and Occurrence of I n j u r y
I n many r e p o r t s , t h e a u t h o r s have p r e s e n t e d
v a l u e s f o r t h e F c o n t e n t of v e g e t a t i o n a t d i f f e r e n t d i s t a n c e s (and sometimes, d i r e c t i o n s ) from a
s o u r c e , b u t o f t e n they d i d n o t provide information
on t h e s o u r c e s t r e n g t h , ambient a i r c o n c e n t r a t i o n ,
o r t h e forms of a i r b o r n e F t h a t were p r e s e n t .
Often, q u a l i t a t i v e o r s e m i - q u a n t i t a t i v e e s t i m a t e s
of i n j u r y a r e given and t h e r e i s l i t t l e o r no cons i d e r a t i o n t o o t h e r p o s s i b l e causes of i n j u r y ,
such a s i n s e c t s , pathogens, environmental s t r e s s e s ,
o r even t h e presence of o t h e r p o l l u t a n t s . These
d a t a a r e most u s e f u l i n e v a l u a t i n g t h e r e l a t i v e
s e n s i t i v i t y of d i f f e r e n t s p e c i e s , t h e i n t e r s p e c i f i c
d i f f e r e n c e s i n s e n s i t i v i t y , t h e most s e n s i t i v e
s t a g e s of p l a n t o r f o l i a r development, t h e compon e n t s of t h e f o r e s t ecosystem most v u l n e r a b l e t o
an e f f e c t , and, i f e v a l u a t e d c a r e f u l l y , t h e dose
of atmospheric F o r t h e amount of t i s s u e F
accumulated t o produce a measurable e f f e c t , whether
i t i s r e g i s t e r e d a s a metabolic o r p h y s i o l o g i c
change o r a s a c h l o r o t i c o r n e c r o t i c l e s i o n .
As one would e x p e c t , t h e atmospheric concent r a t i o n of F and t h e amount accumulated i n vegetat i o n d e c r e a s e s w i t h d i s t a n c e from t h e s o u r c e
(Treshow and o t h e r s , 1967; Sidhu, 1977, 1978;
Thompson and o t h e r s , 1979; Roberts and o t h e r s ,
1979; Bunce, 1978, 1979; Wheeler, 1972; Carlson
and Dewey, 1971). The amount of F accumulated i n
f o l i a g e , however, w i l l depend upon many f a c t o r s
i n c l u d i n g t h e dose and form of F, t h e s p e c i e s ,
a c c e s s i b i l i t y of t h e p o l l u t a n t t o t h e p l a n t (e.g.,
s c r e e n i n g of u n d e r s t o r y by o v e r s t o r y s p e c i e s ) ,
plant-to-plant v a r i a b i l i t y , e t c . I n g e n e r a l ,
b r o a d l e a f s p e c i e s w i l l accumulate more F than
c o n i f e r s when they occur t o g e t h e r (Sidhu, 1977,
1978); and g r e a t d i f f e r e n c e s can occur between
c o n i f e r s p e c i e s , c e t e r u s parabus, w i t h t h e most
t o l e r a n t ones accumulating t h e most F (Weinstein,
1 9 7 7 ) . A l i k e l y e x p l a n a t i o n f o r t h i s is t h a t when
t h e most s e n s i t i v e s p e c i e s a r e i n j u r e d (metabolic a l l y o r p h y s i o l o g i c a l l y ) by a given dose of F,
continued a b s o r p t i o n and accumulation a r e reduced.
Not only a r e t h e most t o l e r a n t s ~ e c i e st h e most
e f f i c i e n t accumulators, b u t t h e amount of accumulat i o n and t h e t h r e s h o l d f o r i n j u r y w i t h i n a genus
( o r even s p e c i e s ) may b e v a s t l y d i f f e r e n t i n
d i f f e r e n t f o r e s t ecosystems. For example, Treshow
and o t h e r s (1967) d i d n o t f i n d n e e d l e i n j u r y i n
Douglas-fir (Pseudotsuga m e n z i e s i i [Mirb.] Franco)
i n Idaho a t F c o n c e n t r a t i o n s i n n e e d l e s t h a t
averaged 150 ppm (composite v a l u e f o r t h e c u r r e n t
y e a r , 2-year-old, and 3-year-old n e e d l e s ) , w h i l e
Carlson and o t h e r s (1979) r e p o r t e d t h a t "mottling
o r c h l o r o s i s was p r e s e n t a t 6-8 ppm" ( n e e d l e s of
u n c e r t a i n a g e ) . Obviously, t h i s d i f f e r e n c e is
r e f l e c t e d i n p a r t by t h e environmental d i f f e r e n c e s
between t h e s t u d y a r e a s (Idaho and Montana) b u t
o t h e r d i f f e r e n c e s between t h e r e s u l t s of t h e two
s t u d i e s should be considered. F i r s t l y , Carlson
and o t h e r s (1979) analyzed a number of n e e d l e
c h a r a c t e r i s t i c s a t d i f f e r e n t d i s t a n c e s from t h e
source of f l u o r i d e e m i s s i o n s i n Montana. The most
common n e e d l e i n j u r y observed was m o t t l i n g (presumably c h l o r o t i c m o t t l i n g ) and, although s i g n i f i c a n t i t was a weak a s s o c i a t i o n t h a t d i d n o t correl a t e very c l o s e l y w i t h F c o n t e n t of n e e d l e s . The
~2 v a l u e s f o r F c o n t e n t of n e e d l e s and n e e d l e
m o t t l e i n Douglas-fir, lodgepole p i n e (Pinus
c o n t o r t a v a r . l a t i f o l i a Engelm.) and w h i t e p i n e
(Pinus monticola Lamb.) were 0.0266, 0.0445, and
0.1604, r e s p e c t i v e l y (Carlson, 1980). But one
might conclude from t h e o r i g i n a l r e p o r t t h a t t h e
occurrence of m o t t l i n g on t h e s e c o n i f e r n e e d l e s
was i n c r e a s e d g r e a t l y by F. The p o s s i b i l i t y t h a t
o t h e r p o l l u t a n t s a s s o c i a t e d w i t h t h i s symptom, such
a s ozone o r another o x i d a n t , would be d i s t r i b u t e d
i n t h e same a i r mass a s F was n o t considered.
Carlson and o t h e r s (1979) a l s o concluded t h a t t h e r e
i s no t h r e s h o l d c o n t e n t of F i n n e e d l e s above
which i n j u r y w i l l occur, and t h a t any d e t e c t a b l e
amount of atmospheric F i s d e t r i m e n t a l t o c o n i f e r s .
This i s a s i m p l i s t i c e x p l a n a t i o n and i t i g n o r e s
s e v e r a l f a c t s . The f i r s t i s t h a t a l l c o n i f e r
needles a r e not equally s e n s i t i v e t o F injury, a s
i s noted i n many compilations ( e . g . , Weinstein,
1977; F l u o r i d e s , 1971; Thomas and A l t h e r , 1966).
Secondly, s e n s i t i v i t y t o F i s r e l a t e d t o t h e age
of t h e n e e d l e a t t h e time of exposure.
It would
b e absurd t o a s s e r t t h a t "adverse e f f e c t s were
v i s i b l e o n n e e d l e s when t h e i r f l u o r i d e c o n c e n t r a t i o n
reached 8-10 ppm" (Carlson and o t h e r s , 1979) of t h e
F accumulated a f t e r t h e c o n i f e r n e e d l e s had comp l e t e d t h e i r e l o n g a t i o n . T h i r d l y , t h e form of F
t o which n e e d l e s a r e exposed and whether i t i s
i n t e r n a l o r s u p e r f i c i a l would a l s o determine t h e
kind of e f f e c t produced. F i n a l l y , i f t h e r e i s no
t h r e s h o l d f o r i n j u r y then t h e r e a r e no mechanisms
of d e t o x i f i c a t i o n i n p l a n t s and p h y s i o l o g i c o r
metabolic p r o c e s s e s , such a s p h o t o s y n t h e s i s o r
enzyme a c t i v i t y , t h a t have been a l t e r e d by I? should
evidence no recovery. There i s ample proof t h a t
once a fumigation c e a s e s , o r i f t h e periodsbetween
--
-
successive fumigations are sufficiently separated, recovery processes (repair mechanisms) are active (see Dinman, 1972; McCune and Weinstein, 1971; Thomas and Alther, 1966). Carlson and others (1979) appear to have equated injury from F with such destructive agents as ionizing radiation. Another interesting contrast in the sensitivity of conifers to F is exemplified by the conditions near a phosphorus plant at Long Harbour, Newfound- land and an alumina reduction smelter at Kitimat, B.C. The Long Harbour area is classified as belonging to the Boreal Forest. Its productive forests are 8-12 m tall and are composed princi- pally of dense stands of balsam fir (Abies balsamea [L.] Mill.) and black spruce (,Picea mariana [Mill.] B.S.P.).
Non-productive scrub forests are less than 5 m tall and are composed of larch (Larix laricina IDuRoi] K. Koch), black spruce, and balsam fir. Rock-barrens and peat- lands are common (Thompson and others, 1979). Soils are generally shallow, precipitation is heavy, and the forests are exposed to high winds containing saline aerosols. Kitimat is in the Pacific Coastal Rain Forest area. The forest is an uneven-aged, overmature, decadent, and stable climax forest. Logging is an important commercial activity. The forest consists of about 60% western hemlock (Tsuga heterophylla [Raf.] Sarg.), 25% balsam fir (Abies amabilis [Dougl.] Forb.), 7% western red cedar (Thuja plicata Lamb.), 6% yellow cedar (Chamaecy- paris nootkatensis [Lamb.] Spach.), and 2% sitka spruce (Picea sitchensis [Bong.] Carr.).
The average age of fir and hemlock is more than 300 years, and it is not unusual to observe trees of 1 or 2 m dbh. Total annual precipitation is about 115 inches and occurs on 53% of the days. The site lies in a wide trough that runs north and south, and bisects the Coast Mountains (Reid, Collins, 1976). other objective criteria related to the intended use of the tree. There is insufficient information to develop these kinds of lists because existing compilations are based primarily on field and laboratory observa- tions of foliar injury. Sensitivity lists based on foliar injury (Weinstein 1977, 1979) are only a guide iind do not provide evidence of relative effects on plant processes. Tree Growth Many studies have identified F as the cause of tree mortality around industrial sources (Adams and others, 1952; Scurfield, 1960; Jung, 1968; Robak, 1969). The determination of F as the causal agent usually entailed determination of foliar F concentrations and, occasionally, air quality moni- toring. In these class 111 relationships (Smith, 1974), determination of the area of impact is normally easy to identify. This is not true for class I1 relationships for several reasons: (1) environmental factors (mainly weather patterns) change from year to year and not only distribute the pollutants randomly but also produce more or less favorable growing conditions for the impacted vegetation; (2) normal biotic factors (insects and pathogens) and abiotic factors (soils) also account for variability in growth; (3) stage of development of the stands of trees also dictate growth rates and the degree of competition between individuals; and (4) all of these factors combined with pollutant exposure produce a given effect. Therefore, to quantify the reduction in growth caused solely by the pollutant, the variability due to the other parameters must be accounted for. Treshow and others (1967a) measured radial growthyneedlelength, needle dry weight, and foliar fluoride concentrations in Douglas-fir (Pseudot- menziesii [Mirb.] Franco) located at differ- ent distances from a fluoride source (also see Emissions at the Long Harbour phosphorus plant 'F Accumulation and Occurrence of Injury"). They are not known, but are certainly lower than those classified the study plots into three groups based at Kitimat, which have ranged from 2.5 to 6.6 tons on foliar F concentrations of composite samples of gaseous F/day between 1955 and 1977 (Alcan o f four age-classes of needles. The groups were
Surveillance Committee, 1979). F concentrations cpntrol (average 24 ppm F), intermediate fluoride in conifers were frequently higher than 100 ppm (average 150 ppm F), and high fluoride (average in late summer without evidence of any foliar 225 ppm and with some needle necrosis). Signifi-
lesions. This can be contrasted to the published cant reductions in radial growth were found in threshold value for needle injury in balsam fir both groups subjected to elevated F concentration at Long Harbour of as low as 14 ppm (Sidhu, 1978). There was a significant negative correlation of Although the same species do not occur in the two needle length with radial growth, but there were areas, the different responses of conifers are so no significant effects on needle dry weights. striking that one must conclude that (1) it is Thus, they found that (1) radial growth reduction not possible to generalize from one site to another, can occur without foliar lesions and (2) Douglas- fir needles can average as much as 150 ppm F (2) foliar F contents alone may be a poor deter- minant of injury, and (3) environmental stresses without foliar injury. (such as wind, salt, nutrient, or water) are as important predictors of an effect as is F content.. A study of the impact of F on nutrient cycling in stands of loblolly (Pinus taeda L.) and slash It is difficult to classify conifers and other pines (Pinus elliotti Engelm.) and the impact on tree species into groups based upon their relative tree growth was made by Wheeler (1972). No tolerance to airborne F because most compilations injury symptoms attributable to F exposure were are based upon foliar injury, and not according noted in the sample plots but trees at the edge to effects on timber volume, fruit production, or of some stands did show some "burning of needles". Increased foliar F concentrations (from 13 to 49 ppm in pooled samples) were correlated with in- creased return rates of Ca and K from greater leaf leaching and of Ca, K, and Mg by greater litterfall. This altered nutrient cycling pre- sumably should alter productivity but no relation- ship was found between needle concentrations of F, Ca, Mg, and K and productivity as measured by amount of bole wood. Wheeler (1972) concluded that either these fluctuations in needle status did not affect growth or that the sampling was insufficient to detect differences that were present. Extensive studies on growth and F accumulation have been made at Kitimat, B.C. (Bunce, 1978) and Columbia Falls, MT (Carlson, 1978). Both areas were subjected to F for many years before any scientific assessment of growth reduction due to F were made and each area was subjected to insect infestation (see section "Insects"), Bunce (1978) used "foliage analysis, observa- tions of lichens, air flow patterns and topographic features" to estimate the area of impact and to establish the distribution of his sample plots. Tree ring cores were taken from western hemlock, the dominant species, from all sample locations, and were used to determine the amount of growth reduction due to F emissions. After variability in growth rates due to weather, insect infesta- tion, and another pollutant (SO2) were accounted for, Bunce (1978) reported the annual loss of wood production to be 950 cunits (95,000 cu. ft.) per year compared to the 800,000 cunits attributed to insect damage. Obviously the cause of the insect outbreak is fundamental to the assessment of the magnitude of the F-related effects on growth and is discussed elsewhere. Although the primary and secondary (bark beetles) insect out- breaks ended by 1968, F emissions have continued at a lower rate since 1975 and trees in the insect damaged zone are regenerating satisfactorily. The question ofwhether there is a cause-and-effect relationship between F emissions and insect in- festation has not yet been answered for reasons discussed elsewhere. F from an aluminum reduction plant in Columbia Falls, MT caused growth reductions in Douglas-fir fir, lodgepole pine, and western pine (Carlson, 1978, 1979). However due to questionable assump- tions and miscalculations, an overestimate of the loss of usable timber due to F pollution was made. Statistically, the data (Carlson, 1978) showed only a weak correlation between foliar F concen- trations and reduced radial growth. The area of growth reduction was substantially smaller than reported previously (Carlson, 1980). It has also been stated (Carlson, 1978) that any increase in foliar F above background concentrations is detrimental to tree growth. This assumption was generated by the implied growth reduction of trees located in areas designated as having reduced growth; but upon closer examination of the data, no growth reduction could be demonstrated (Carlson, 1980). Consequently, the original assumption, which implies that'^thereg no thres- hold concentration of foliar F below which injury does not occur, cannot be substantiated. This is not meant to imply that F is not phytotoxic, because it is the most toxic of the common atmos- pheric pollutants. But an understanding of its effects in the ecosystem, requires much research and the synthesis of an enormous amount of information. ~och'sPostulates were not written
frivolously.
Community Structure
Large areas of the Eastern United States are subjected to a complex mixture of air pollutants from urban centers and industrial sources. Most of the Eastern Deciduous Forests are subjected to at least moderate air pollution (Class 11). McClenahen (1978) studied the effects of a mix- ture of pollutants derived from industrial sources (containing F, SO?, NOx, chloride, and oxidant) on changes in structure and composition of a mixed deciduous forest in the Ohio River Valley. The study sites were arbitrarily divided into over- story, subcanopy, shrub and herb layers and the stands were measured for diversity (Pielou, 1975), evenness (Williams, 1977), and species composition. In genera1,the average total stand densities of the overstory and herb layers were found to decrease in proximity to the F source while the subcanopy and,shrub layer increased with the shrub layer being the only layer thatshoweda significant correlation to F exposures. Chloride from another source had a greater influence in the other layers. Murray (1979) conducted a study of plant comun- ity structure around an aluminum smelter in Australia. Although a number of study sites were lost by fire, he was able to ordinate species associations with F stress. More of these kinds of studies are needed to provide data to predict the risk of an effect when an ecosystem is exposed to airborne F. Incidence and Severity of Diseases and Insects There is evidence, from laboratory and field experiments or observations, that airborne F may alter the plant-pathogen and plant-insect rela- tionships. The exact relationships between F and these biotic stresses and their underlying mech- anisms are only beginning to be understood. --
Plant pathogens
Although there are many industrial sources of F, we are not aware of any field or laboratory reports that link airborne F with incidence or severity of forest tree diseases. It is necessary, therefore, to discuss some labora- tory research on the effects of HF on diseases of crop plants in order to evaluate possible forestry effects and to establish research needs. The plant-pollutant-pathogen interaction was reviewed by Heagle in 1973 and Laurence in 1978. For the kinds of effects that have been found, McCune and others (1973) provided three possible e x p l a n a t i o n s : (1) t h e r e could be a d i r e c t e f f e c t
of t h e p o l l u t a n t on growth and development of t h e
organism; (2) t h e p o l l u t a n t could a f f e c t t h e susc e p t i b i l i t y of t h e p l a n t t o t h e pathogen; and (3)
t h e p o l l u t a n t could a f f e c t t h e microbiota o r microenvironment of p l a n t s u r f a c e s and thereby a f f e c t
t h e pathogen.
Tobacco l e a v e s i n f e c t e d with tobacco mosaic
v i r u s and c o n t a i n i n g 200-300 ppm F had a higher
t i t e r of v i r u s than c o n t r o l l e a v e s when a l o c a l
l e s i o n assay was used. The t i t e r was lower a t 500
ppm F (Dean and Treshow, 1966; Treshow and o t h e r s ,
1967b). But perhaps t h e b e s t evidence f o r a
d i r e c t e f f e c t of a i r b o r n e F on growth and development of a pathogen was t h e c o n s i s t e n t reduction
i n bean powdery mildew (Erysiphe polygoni DC.)
found a s a r e s u l t of HF fumigation, i n d i c a t i n g
t h a t HF was a f f e c t i n g t h e i n f e c t i v i t y of t h e pathogen i t s e l f , because reduction i n d i s e a s e was prop o r t i o n a l t o t h e l e n g t h of t h e exposure p e r i o d ,
i n f e c t i o n was continuous throughout t h e exposure
p e r i o d , and t h e pathogen i t s e l f i s e p i p h y t i c .
The most l i k e l y mechanism f o r an e f f e c t of F on
p l a n t pathogenic d i s e a s e s would be an a l t e r a t i o n
i n t h e s u s c e p t i b i l i t y of t h e h o s t p l a n t t o t h e
pathogen. The r e d u c t i o n i n t h e numbers of bean
r u s t (Uromyces p h a s e o l i [ P e r s . ] Wint.) u r e d i a by
pre- and post-inoculation exposures t o HF may have
been due t o a change i n h o s t metabolism by t h e
accumulation of F (McCune and o t h e r s , 1973). The
b e s t evidence a v a i l a b l e t h a t s u g g e s t s an i n d i r e c t
e f f e c t of F was found i n halo-blight of bean
(Pseudomonas p h a s e o l i c o l u s [Burkh. ] Dows ) where
stem c o l l a p s e was a f f e c t e d , b u t f o l i a r symptoms
were n o t . Thus, t h e s i t e a f f e c t e d was s p a t i a l l y
removed from t h e s i t e of F accumulation, t h e l e a f
(McCune and o t h e r s , 1973).
.
There is no reason t o b e l i e v e t h a t crop p l a n t s
should respond d i f f e r e n t l y than f o r e s t s p e c i e s t o
a i r b o r n e F and p l a n t pathogens, and l a b o r a t o r y and
f i e l d s t u d i e s a r e needed t o determine and e v a l u a t e
e f f e c t s on t h e incidence of d i s e a s e and p o s s i b l e
epidemiological consequences.
--
The c o n t r o v e r s i e s a s s o c i a t e d w i t h
Insects
t h e e f f e c t s of F on p l a n t s i n g e n e r a l , and ecosystems i n p a r t i c u l a r , a l s o extend t o t h e p o s s i b i l i t y t h a t F a l t e r s t h e r e l a t i o n s h i p between p l a n t s
and d e s t r u c t i v e i n s e c t s , t h a t F k i l l s b e n e f i c i a l
i n s e c t s , o r t h a t accumulation of F i n i n s e c t s makes
them a v e h i c l e f o r t h e t r a n s f e r of F i n ecosystems.
There i s ample evidence t h a t an a s s o c i a t i o n can
e x i s t betwen F-contaminated y e g e t a t i o n and i n s e c t s ,
but t h e r e l a t i o n s h i p i s n o t understood and i t does
n o t occur under a l l c o n d i t i o n s o r with a l l i n s e c t s .
P f e f f e r (1962-1963) r e p o r t e d t h a t a t t a c k by
bark b e e t l e s , snout b e e t l e s , and f i r l e a f r o l l e r s
were a s s o c i a t e d w i t h F emissions i n a f i r f o r e s t
i n Czechoslovakia. Carlson and Dewey (1971) and
Carlson and o t h e r s (1974) have r e p o r t e d t h a t F
accumulation i n c o n i f e r f o l i a g e i s c l o s e l y r e l a t e d
t o i n f e s t a t i o n s by s e v e r a l d e s t r u c t i v e i n s e c t s :
p i n e needle s c a l e (Phenacapsia p i n i f o l i a e F i t c h ) ,
pine needle s h e a t h miner ( Z e l l a r i a haimbachi
Busck), needle miner (Ocnerostyma strobivorum
[ Z e l l e r ] ) , and sugar p i n e t o r t r i x (Choristoneura
lambertiana [Busck] ) t h a t ranged from no s i g n i f i c a n c e ( l a r c h casebearer) t o a non-significant
trend (pine needle s c a l e ) t o s t r o n g evidence of a
weak c o r r e l a t i o n (needle miners). Only about 6%
of t h e v a r i a t i o n i n needle damage by needle miners
was a s s o c i a t e d with f o l i a r F concentration. There
was an even more remote a s s o c i a t i o n between needle
miner population and f o l i a r F concentration.
Edmunds and Allen (1956) and Compton and o t h e r s
(1961) found no a s s o c i a t i o n between ~ i n eneedle
& a l e (Nuculopsis c a l i f o r n i c a [ ~ o l e m k ] )and t h e
e x t e n t of F i n j u r y o r F content of needles of
ponderosa p i n e (Pinus ponderosa Laws) and Edmunds
(1973) questioned t h e r e s u l t s of Carlson and Dewey
(1971). Thalenhorst (1974) and Wentzel (1965)
found p o s i t i v e r e l a t i o n s h i p s between spruce g a l l s
induced by Adelges a b i e t e s (L.) and F. But Temple
(personal communication) could f i n d no c o r r e l a t i o n
between t h e F content of washed s i l v e r maple f o l i age and g a l l s induced by t h e bladder-gall mite
(Vasates quadripes [deshimer]).
-
7
One of t h e most i n t e r e s t i n g examples of a possib l e F-plant-insect a s s o c i a t i o n was observed n e a r
an alumina reduction s m e l t e r i n Kitimat, B.C. ( s e e
s e c t i o n on "F Accumulation i n P l a n t s and Occurrence
Between 1960 and
of Injury" and "Tree Growth").
1963, an e p i z o o t i c of saddleback l o o p e r s ( E c t r o p i s
c r e p u s c u l a r i a [Denis & S c h i f f . ] ) and spruce budworms ( C h o r i s t m e u r a 9Free.) occurred t h a t
k i l l e d many t r e e s over a l a r g e a r e a t h a t coincided
w e l l w i t h t h e p a t t e r n o f f u m e d i s p e r s i o n . I n 1961,
balsam bark b e e t l e s (Pseudohylesinus g r a n d i s
[Swaine] and P. nebulosus [Lee.]) appeared a s
secondary p e s t s throughout t h e a r e a a t t a c k e d by
t h e looper and t h e budworm. We used t h e word
' p o s s i b l e " above i n r e f e r r i n g t o F as t h e c a u s a l
agent i n t h i s outbreak because (1) t h e r e i s no way
now t o e s t a b l i s h a cause-and-effect r e l a t i o n s h i p ;
(2) t h e emissions were a l s o high i n p a r t i c u l a t e
m a t e r i a l s , s u l f u r compounds, p i t c h v o l a t i l e s , and
even CO2; (3) t h e problem was n o t s t u d i e d a t t h e
time t h a t t h e outbreaks occurred; and (4) o t h e r
p o s s i b l e e t i o l o g i e s have been suggested by entomolo g i s t s from t h e Canadian F o r e s t r y Service. Several
of t h e t h e o r i e s t h a t might e x p l a i n t h e i n s e c t
a t t a c k s a t Kitimat a r e : (1) F absorbed by t h e
f o l i a g e of t h e t r e e a l t e r s i t s metabolism and inc r e a s e s i t s a t t r a c t i v e n e s s t o i n s e c t s ; (2) F weakens
t h e t r e e , rendering i t l e s s a b l e t o r e s i s t i n s e c t
a t t a c k ; (3) gaseous o r p a r t i c u l a r emissions a r e
t o x i c t o p a r a s i t i c and/or predaceous i n s e c t s t h a t
provide important c o n t r o l s of t h e population of
d e s t r u c t i v e i n s e c t s ; (4) t h e emissions have a
"blanket" e f f e c t t h a t r e s u l t s i n a s l i g h t temperat u r e a l t e r a t i o n and gives t h e l a r v a e of t h e l o o p e r s
and budworm a competitive advantage over p a r a s i t e s
and p r e d a t o r s ; (5) loopers and budworm moths were
c a r r i e d on winds i n t o t h e Kitimat a r e a and dispersed i n t h e same p a t t e r n a s s m e l t e r emissions;
and (6) t h e r e were an unusually l a r g e number of
l i g h t s i n t h e v a l l e y above t h e smelter i n t h e
e a r l y 1960's and they provided l i g h t of wavelengths
t h a t a t t r a c t e d moths (Alcan S u r v e i l l a n c e Committee,
Although the primary and secondary insect attacks were extremely destructive, amounting to a total net loss of mature timber estimated at 800,000 cunits (80,OOQOOO cu. ft.) (Reid, Collins, 1976) a considerable number of trees were not damaged and regrowth has been extensive. In some areas near the smelter, F-induced injury was a prominent feature on young hemlock, Sitka spruce, black cottonwood, and even western red cedar (Weinstein, unpublished field reports for 1971 and 1974 cited in Alcan Surveillance Committee, 1979). In the intervening years, especially since 1975, there has been a substantial reduction in total emissions from the smelter (more than 50% between 1975 and 1977), accompanied by greatly reduced foliar injury. Nevertheless, vegetation exhibiting no foliar symptoms often contains 100 ppm F or more, and the incidence of insect attack is no-greater than in nearby areas not exposed to the smelter emissions. Because any reduction in emissions would include gaseous F, particles, and other components of the fumes, no cause- and effect-relationship can be made. From subjective observations, however, particulate emissions have been reduced strikingly, at least since 1971, and we feel that this fraction of the emissions was perhaps of great significance in the original out- breaks. Certainly, the indirect relationship be- tween an increase in insect colonization and particles has been known for many years (Bartlett, 1951). Even before Carlson and his colleagues were attempting to demonstrate a relationship between F and insects on U.S. Forest Service land and in Glacier National Park, an enormous outbreak of mountain pine bark beetle (Dendroctonus ponderosae [Hopkins]) was beginning on the Canadian border many km to the north. It extended through- out the entire Flathead National Forest and the western part of Glacier National Park, and has destroyed many thousands of lodgepole, ponderosa, and white pines. Although there is little doubt that an associa- tion exists between airborne contaminants and insect outbreaks, the evidence for a cause-and- effect relationship with F in unconvincing, and at times it appears that some investigators have forced a relationship. Insect outbreaks occur in unpolluted as well as polluted areas. The question to be resolved is not whether there is or isn't a relationship between airborne substances and in- sects, but to determine the nature of this rela- tionship and the features it has in common with other stresses. Evaluation of F Injury in the Field The most common measures of F injury to forests include (1) assessment of the presence and amount of foliar injury, especially of indicator species; (2) loss or depletion of sensitive receptors and community changes; (3) measurement of biomass pro- duction; and (4) the accumulation of F in plant tissues that might produce foliar injury or render the plant unsuitable for indigenous herbivores. Regardless of the approaches used, the path to useful information can be a difficult and confusing one, as is well-known for other atmospheric pollu- tants. Some of these problems have been discussed by Weinstein and McCune (1970). There are a number of indigenous plant species that are sensitive to atmospheric F, including goat- weed (Hypericum perforaturn L.), common barberry (Berberis vulgaris L.), Oregon grape (Mahonia repens [Lindl.] Don. and g. nervosa [Pursh.] Nutt.), blue-
berry (Vaccinium spp.), and young needles of many conifers (see Table 2 for a list of F-sensitive One general conclusion can be made: higher plants).
field observations of plants can be a good qualita- tive but is usually a poor quantitative indicator of effects. In many cases of F pollution, there has been a severe depletion of lichen populations (reviewed by Gilbert, 1973). In areas nearest the F source, a lichen desert may exist, but they appear and in- crease in frequency and diversity with increasing distance from the source (LeBlanc and others, 1972). Nash (1971) and LeBlanc and others (1971) trans- planted several species of lichens into the field in areas of F-emitting industries and found that the species used were injured near the source (but sometimes up to 10 km away) and were effective F accumulators. Corticolous lichens accumulate F more rapidly than saxicolous species, and consequent- ly, demonstrate accelerated damage and reduced abundance (Perkins and others, 1980), but much research remains to characterize and classify the sensitivity of the different lichen types growing on their many kinds of habitats. Problems associated with the measurement of biomass have been discussed in many treatises on forest mensuration, and Bunce (1978, 1979) and Parker and others (1974) have discussed the problems associated with discriminating between effects of F, insects, and environmental stresses in evaluating effects on tree growth. The relationship between F accumulation and production of foliar lesions or other effects, is discussed elsewhere, and fluorosis in indigenous herbivores is beyond the scope of this review. F Distribution in the Environment In its most elementary form, the transfer of F to and from the atmosphere, waters, soils and rocks, and living organisms, due to natural or anthro- pogenic causes, has been described (Fluoride, 1971; Weinstein, 1977). F that is accumulated in plants enters the food chain through herbivores and passes into the soil in their wastes. The transfer from one animal to another is possible in the case of insects that have accumulated F on or in their bodies and are eaten by birds or other carnivores, but this has not beenstudied. It is also not known if increased levels of F associated with a variety of insects was due to accumulation by ingestion or by surface contamination. Hughes and others (in preparation) cultured cabbage loopers (Trichoplusia ni [Hubner]) on two kinds of diets. One contained -
i n c r e a s i n g amounts of F a s NaF o r KF and equival e n t amounts of c o n t r o l cabbage. The o t h e r cont a i n e d F from HF-fumigated l e a v e s and was combined w i t h c o n t r o l l e a v e s t o g i v e t h e same dose
curve. Analyses of prepupae and pupae showed
t h a t F accumulated i n t h e b o d i e s of t h e l o o p e r s
1 0 p e t . of t h e concens u p p l i e d w i t h F s a l t (G.
t r a t i o n of t h e d i e t on a dry weight b a s i s ) ; no
F accumulated i n l o o p e r s grown w i t h t h e fumigated
cabbage d i e t . There was evidence t h a t l o o p e r s
grown w i t h t h e l a t t e r d i e t developed f a s t e r and
grew l a r g e r than t h o s e on t h e c o n t r o l cabbage
NaF o r KF d i e t s . These r e s u l t s s u g g e s t t h a t t h e
F r e p o r t e d a s having accumulated i n i n s e c t s proba b l y was due t o s u r f a c e contamination of p a r t i c l e s
(Carlson and Dewey, 1971; Dewey, 1973). Ingest i o n of surface-contaminated i n s e c t s by c a r n i v o r e s ,
however, s t i l l t r a n s f e r s t h e F t o t h e n e x t t r o p h i c
l e v e l , b u t t h e amount of accumulation t h a t might
occur a t t h a t l e v e l i s n o t known.
There a r e g r e a t d i f f e r e n c e s i n t h e c a p a c i t i e s
of p l a n t s growing i n t h e same s o i l s t o accumulate
F. Most p l a n t s accumulate low c o n c e n t r a t i o n s of
F (0
1 0 ppm), b u t some s p e c i e s can accumulate
hundreds of ppm from t h e same s o i l . I n any
s p e c i e s , s o l u b l e F i n t h e s o i l s o l u t i o n can b e
r e a d i l y absorbed by p l a n t s (Romney and o t h e r s ,
1969). When d e p o s i t e d upon p l a n t s u r f a c e s , t h e
r e l a t i v e l y i n s o l u b l e forms of F have low phytot o x i c i t y (McCune and o t h e r s , 1977), b u t t h e i r
i n g e s t i o n can b e harmful t o h e r b i v o r e s . Conseq u e n t l y , t h e main s o u r c e of p h y t o t o x i c a i r b o r n e
F i s HF.
-
Once i t e n t e r s a l e a f , F moves i n t h e t r a n s p i r a t i o n s t r e a m t o t h e t i p s o r margins of t h e l e a f
and s t a y s i n a form t h a t can be leached from many
l e a v e s (Leone and o t h e r s , 1956; L e d b e t t e r and
o t h e r s , 1960; Jacobson and o t h e r s , 1966). Cons e q u e n t l y , f o l i a r c o n c e n t r a t i o n s of F need n o t
s t e a d i l y i n c r e a s e (Knabe, 1970). Twigs of deciduous s p e c i e s can accumulate F i n t h e w i n t e r ,
presumably through t h e l e n t i c e l s , and e l e v a t e d
c o n c e n t r a t i o n s have been found i n young f o l i a g e
i n t h e s p r i n g ( K e l l e r , 1974, 1978). A s m a l l prop o r t i o n of F e n t e r i n g a l e a f can a l s o be t r a n s l o c a t e d t o o t h e r p a r t s of t h e p l a n t (Kronberger
and o t h e r s , 1978).
F a l r e a d y p r e s e n t i n most s o i l s i s i n an i n s o l u b l e form and h a s l i t t l e i n f l u e n c e on v e g e t a t i o n ,
The f a t e of F leached from f o l i a g e and of F dep o s i t e d d i r e c t l y from t h e atmosphere h a s n o t been
s t u d i e d e x t e n s i v e l y . Any e f f e c t w i l l depend upon
t h e n a t u r e and chemistry of t h e s o i l . F l i i h l e r
and o t h e r s (1979) have shown t h a t l e a c h i n g of
p a r t i c u l a t e F depends upon i t s w a t e r s o l u b i l i t y
(NaF > powdered p i n e n e e d l e s c o n t a i n i n g F >
c r y o l i t e > CaFy). The F i n powdered p i n e n e e d l e
l i t t e r leached n e a r l y a s r a p i d l y a s d i d NaF.
When NaF s o l u t i o n s were a p p l i e d t o s o i l columns,
o r g a n i c m a t t e r , aluminum, and i r o n were l o s t ,
b u t t h e amount depended upon t h e s o i l t y p e ,
E f f e c t s of F on s o i l composition and s t r u c t u r e ,
m i n e r a l c y c l i n g , and l i t t e r decomposition a r e
important a s p e c t s of t h e impact of F on f o r e s t
ecosystems and r e s e a r c h i n t h e s e a r e a s should
have a h i g h p r i o r i t y .
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and L. K. Mann. 1979. The effects of SO2 dosage kinetics and exposure frequency on photosynthesis and transpiration of kidney beans (Phaseolxs vulgaris L.).
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Bull. Torrey Bot. Club 98:103-106. Navara, J. 1963. Zur Frage des Einflusses von Fluor in Substrat auf die Intensitat der Stomatar- Kutikularen Transpiration und auf die Photo- synthese. Biologia, Bratislava 18(1):15-22. Navara, J. and V. Kozinka. 1967. Wasserhaushalt der Pflanzen in gegenwart gasf6rmiger Fluorverbindungen in der Atmos- phzre. Biologia, Bratislava 22(3):210-220. -
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Plants Animals. 1st. 27-31 p. Roberts, B. A., L. K. Thompson, and S. S. Sidhu. 1979. Terrestrial bryophytes as indicators of fluoride emissions from a phosphorus plant. Long Harbour, Newfoundland, Canada. Can. J. Bot. 57:1583-1590. Romney, E. M., R. A. Wood, and P. A. T. Wieland. 1969. Radioactive fluorine 18 in soil and plants. Soil Science 108(6):419-423. Niklfeld, H. 1967. Pflanzensoziologische Beobachtungen tin Rauchschadensgebiet eines Aluminiumwerkes Centralbl. Gesamte Forstwest. 84:318-329. Scurfield, G. 1960. Air pollution and tree growth. For. Abstr. 339-347 and 517-528. Pack, M. R. 1966. Response of tomato fruiting to hydrogen fluoride as influenced by calcium nutrition. J. of A.P.C.A. 16(10):541-544. Sidhu, S. S. 1977. Fluoride levels in air, vegetation and soil in the vicinity of a phosphorus plant. Paper 77-30.2. 16p. 70th Annual Meeting, Air Pollution Control Assoc., Toronto, Canada. Pack, M. R., and C. W. Sulzbach. 1976. Response of plant fruiting to hydrogen fluoride funigation. Atmos. Environ. 10: 73-81. Parker, M. L., H. W. F. Bunce, and J. H. G. Smith. 1974. The use of x-ray densitometry to measure the effects of air pollution on tree growth near Kitimat, British Columbia. p. 185-204. Internat. Cong. Air Pollut. and Forestry, Marianske Lazne, Czechoslovakia. Sidhu, S. S. 1978. Patterns of fluoride accumulation in forest species as related to symptoms and defoliation. Paper 78-24.7 16 p. 71st Annual Meeting, Air Pollution Control Assoc., Houston, Texas. Smith, W. H. 1974. Air pollution-Effects on the structure and function of the temperate forest eco- system. Environ. Pollut. 6:111-129. Perkins, D. F., R. 0. Millar, and P. E. Neep. 1980. Accumulation of airborne fluoride by lichens in the vicinity of an aluminum reduction plant. Environ. Pollut. 21:155-168. Solberg, R. A. and D. F. Adams. 1956. Histological responses of some plant leaves to hydrogen fluoride and sulfur dioxide. her. J. Bot. 43:755-760. .Pfeffer,A. 1962-1963. Insectenschadlinge an Tannen im Bereich der Gasexhalationen. 2. Angew.
Entomol. 51:203-207. Stoiber, R. E., S. N. Williams, and L. L. Malinconica
1980. Mount St. Helens. Washington, 1980 volcanic eruption: Magmatic gas component during the first 16 days. Science 208:1258-1259. Peilou, E. C. 1975. Ecological Diversity. John Wiley and Sons, New York. Poovaiah, B. W. and H. H. Wiebe. 1973. Influence of hydrogen fluoride fumigation on the water economy of soybean plants. Pit. Phys. 51:396-399. Reid Collins and Associates, Ltd. 1976. Fluoride emissions and forest growth. Aluminum Co. of Canada, Kitlmat, B.C. 112 p. Report of Alcan Surveillance Committee. 1979. Environmental effects of emissions from the Alcan smelter at Kitimat, B.C. 151 p. Ministry of Environment, Province of British Columbia. Robak, H. 1969. Aluminum plants and conifers in Norway. .
Suttie, J. W. 1977. Effects of fluoride on livestock.
Occup. Med. 19:40-48. J. Thalenhorst, W. 1974. Untersuchungen liber den Einfluss fluor- haltiger Abgase auf die Disposition der Fichte fiir den Befall durch die Gallenlaus Sacchiphan- tes abietis (L.).
A. Pflanzen Krankh. und Pflanzenschutz 81(12):717-727. Thomas, M. D. 1958. Air pollution with relation to agronomic crops: I. General status of research on the effects of air pollution on plants, Agron. J. 50:545-550. Thomas, M. D., and E. W. Alther. 1966. The effects of fluoride on plants. Hand-
book of Experimental Pharmacology. Vol. 20.
Part 1, p. 231-306. Springer-Verlag, New York. Thomas, M. D., and R. H. Hendricks. 1956. Effect of air pollution on plants. In: Air Pollution Handbook. P. L. Magill, F.R.
Holden, and C. Ackley, eds. McGraw-Hill Co., N.Y. Thompson, L. K., S. S. Sidhu, and B. A. Roberts. 1979. Fluoride accumulations in soil and vege- tation in the vicinity of a phosphorus plant. Environ. Pollut. 18:221-234. Thompson, C. R., 0. C. Taylor, M. D. Thomas, and J. 0. Ivie. 1967. Effects of air pollutants on apparent photosynthesis and water use by citrus trees. Environ. Sci. & Technol. 1:644-650.
Treshow, M., F. K. Anderson, and F. Harner. 1967a. Responses of Douglas-fir to elevated atmospheric fluorides. For Sci. 13(2): 114- 20. Treshow, M., G. Dean, and F. Harner. 1967b. Stimulation of tobacco mosaic virus- induced lesions in bean by fluoride. Phytopath. 57:756-758. Treshow, M., and F. M. Harner. 1968. Growth responses of Pinto bean and al- falfa to sub-lethal fluoride concentrations. Can. J. Bot. 46:1207-1210. Weinstein, L. H. 1961. Effects of atmospheric fluoride on meta- bolic constituents of tomato and bean leaves. Contrib. Boyce Thompson Inst. 21~215-231. Weinstein, L. H. 1977. Fluoride and plant life.
Med. 19 (1) :49-78. J. of Occup. Weinstein, L. H., and D. C. McCune. 1970. Field surveys, vegetation sampling, and air and vegetation monitoring. p. GI-G4. In: Recognition of Air Pollution Injury to Vegetation: A Pictorial Atlas. J. S. Jacobson and A. C. Hill, eds. Air Pollution Control Assoc., Pittsburgh, Pa. Wentzel, K. F. 1965. Insekten als Immissionsfolgesch~dlinge. Naturwissenschaften 52:113. Wheeler, G. L. 1972. The effects of fluorine on the cycling of calcium, magnesium, and potassium in pine plantations of eastern North Carolina. Dissertation. North Carolina State Univ. at Raleigh. 71 p. Williams, F. M. 1977. Model-free evenness: an alternative to diversity measures. Satellite Program in Statistical Ecology of the International Statistical Ecology Program. The Pennsylvania State University, University Park, Pa. Woltz, S. S., and C. D. Leonard. 1964. Effect of atmospheric fluorides upon certain metabolic processes in Valencia orange leaves. Proc. Fl. State Hort. Soc. 77:g-15. Yee-Meiler, D. 1975. Uber die Eignung von Phosphatase-und ~steraseaktivitats-bestimmungen an Fichtenna- deln und Ritkenblattern zum Nachweis 'unsichtbarer physiologischer" Fluorimmis- sionsschadigungen. Eur. J. For. Path. 5: 329-338. Yee-Meiler, D. 1977. Phenole als Indikatoren metabolischen St'orungen bei fluorexponierten Waldbkmen. Mitteilungen eidg. Anst. forstl. Vers wes. 53(4) :203-229.
Yu, M. H. and G. W. Miller. 1967. Effect of fluoride on the respiration of leaves from higher plants. Plant Cell Physiol. 8:483-493. Zimmerman, P. W., and A. E. Hitchcock. 1956. Susceptibility of plants to hydrofluoric acid and sulfur dioxide gases. Contrib. Boyce Thompson Inst. 18:263-279. Zimmerman, P. W., and A. E. Hitchcock, and J. Gwirtsman
1957. Fluorine in food with special reference to tea. Contrib. Boyce Thompson Inst. 19: 49-53. .
Air Pollution-a 20th Century Allogenic
Influence on Forest ~cosystems'
W i l l i a m H. smith2
Abstract: Chronic doses of ozone, s u l f u r d i o x i d e ,
nitrogen oxides, hydrogen f l u o r i d e and other primary or
secondary gaseous a i r contaminants may cause subtle effects on
forest ecosystems. Air pollutants may influence reproduction,
n u t r i e n t cycling, photosynthesis, predisposition t o
entomological or pathological s t r e s s or q u a n t i t y of healthy
f o l i a r tissue. Forest ecosystem response t o chronic a i r
p o l l u t i o n may i n c l u d e a l t e r a t i o n s i n growth r a t e s and
successional patterns. The establishment of comprehensive
f i e l d and laboratory investigations t o systematically examine
chronic a i r p o l l u t i o n s t r e s s on f o r e s t ecosystems i n those
p a r t s of t h e world s u b j e c t t o atmospheric contamination is
concluded t o be of top priority. In the United States, forest
ecosystems judged t o be a t particular risk and i n need of more
intensive investigation include the Northern Hardwood f o r e s t ,
C e n t r a l Hardwood f o r e s t and Western Montane f o r e s t .
The interactions between a i r contaminants
and f o r e s t ecosystems a r e extremely complex,
but can be conveniently divided i n t o - t h r e e
major c l a s s e s (Smith 1980). Under conditions
of low dose
Class I r e l a t i o n s h i p - t h e
vegetation and s o i l s of f o r e s t ecosystems
function a s important sources and sinks for a i r
pollutants. When exposed t o intermediate dose
Class I1 r e l a t i o n s h i p - i n d i v i d u a l t r e e
s p e c i e s o r individual members of a given
species may be subtly and adversely affected by
n u t r i e n t s t r e s s , i m p a i r e d metabolism,
predisposition t o entomological or pathological
s t r e s s , or d i r e c t disease induction. Exposure
-
-
%?resented a t the Symposium on Effects of Air
Pollutants on Mediterranean and Temperate Forest
Ecosystems, June 22-27, 1980, Riverside, California, U.S .A.
p r o f e s s o r of Forest Pathology, School of
Forestry and Environmental S t u d i e s , Yale
University, New Haven, Conn., U.S.A.
t o high dose - Class I11 r e l a t i o n s h i p - may
induce acute morbidity or mortality of specific
trees. A t t h e ecosystem l e v e l t h e impact of
these various i n t e r a c t i o n s would be v e r y
variable.
In t h e Class I relationship,
pollutants would be exchanged between the atmos p h e r i c compartment, a v a i l a b l e n u t r i e n t
compartment, other s o i l compartments and
various elements of the biota. Depending on the
nature of the pollutant, the ecosystem impact
of this t r a n s f e r could be undetectable (innocuous e f f e c t ) or s t i m u l a t o r y ( f e r t i l i z i n g
e f f e c t ) . I f t h e e f f e c t of a i r p o l l u t i o n dose
on some component of the biota is inimical then
a Class I1 r e l a t i o n s h i p is established. The
ecosystem impact i n t h i s c a s e could include
reduced productivity or biomass, alterations i n
species composition or community s t r u c t u r e ,
increased insect outbreaks or microbial disease
epidemics and increased morbidity.
Under
conditions of high dose and Class I11 relationship, ecosystem impacts may include gross
simplification, impaired energy flew and biogeochemical cycling, changes i n hydrology and
erosion, climate alteration and major impacts
on associated ecosystems.
This paper is s p e c i f i c a l l y concerned with
Class I1 i n t e r a c t i o n s r e s u l t i n g from f o r e s t
ecosystem exposure t o chronic doses of ozone,
s u l f u r dioxide, nitrogen oxides, hydrogen
fluoride or other primary or secondary gaseous
a i r contaminants. It s p e c i f i c a l l y addresses
the relationship between these gases, and t h e i r
mixtures, on f o r e s t r e p r o d u c t i o n , f o r e s t
metabolism and direct forest s t r e s s as detailed
by previous c o n t r i b u t o r s t o t h i s s e c t i o n and
attempts t o examine resulting perturbations i n
ecosystem structure and function.
FOREST REPRODUCTION
Sexual reproduction of f o r e s t t r e e s is
c r i t i c a l l y important for maintenance of genetic
f l e x i b i l i t y and the persistence of most species
i n n a t u r a l f o r e s t communities. Reproductive
s t r a t e g i e s , however, a r e t y p i c a l l y b e s e t by a
v a r i e t y of "weak points" and reproductive
growth of many f o r e s t t r e e s is, a t best,
irregular and q u i t e unpredictable. Generally
t h e r e i s a very good c o r r e l a t i o n between t r e e
vigor and t h e capacity f o r flowering and
f r u i t i n g (Kramer and Kozlowski 1979). A
v a r i e t y of environmental c o n s t r a i n t s impose
r e s t r i c t i o n s on t r e e reproductive processes.
Because a i r contaminants may reduce t r e e vigor
and i n view of the f a c t t h a t numerous potential
p o i n t s of i n t e r a c t i o n have been i d e n t i f i e d
between a i r p o l l u t a n t s and r e p r o d u c t i v e
elements (Smith 19801, it has been hypothesized
t h a t a i r c o n t a m i n a n t s may i m p a c t f o r e s t
e c o s y s t e m s by i n f l u e n c i n g r e p r o d u c t i v e
processes.
Considerable evidence has been presented
i n d i c a t i n g a p o t e n t i a l a d v e r s e i m p a c t of
numerous g a s e o u s p o l l u t a n t s on p o l l e n
metabolism. Other p a p e r s have i n d i c a t e d
reduced cone and f r u i t production under f i e l d
conditions (Smith 1980). I f one o r more of
these various reproductive stress mechanisms is
o p e r a t i v e i n n a t u r a l f o r e s t ecosystems, it is
p o s s i b l e t h a t changes i n s p e c i e s composition
may ultimately occur. In their study of ozone
impact on t h e understory vegetation of an aspen
ecosystem, Harvard and Treshow (1975) concluded
t h a t only one or two y e a r s of ozone exposure
m i g h t be s u f f i c i e n t t o c a u s e s h i f t s i n
community c o m p o s i t i o n because of s e e d
production responses t o ozone exposure.
FOREST METABOLISM
Photosynthesis i s t h e most fundamental
metabolic process of forest ecosystems and is
the primary determinant of growth and biomass
accumulation. The r a t e of net photosynthesis
of mature t r e e s frequently is within the range
of 10-200 mg of carbon dioxide taken up per
gram of dry weight per day.
The r a t e is
extremely variable, however, and influenced by
genetic, c l o n a l and provenance differences,
season of t h e year, time of day, p o s i t i o n
w i t h i n t h e crown of t h e t r e e , age of f o l i a g e ,
climate and edaphic factors.
Studies with a wide variety of agricultural
and herbaceous s p e c i e s , under c o n t r o l l e d
environmental conditions, have i n d i c a t e d t h a t
a i r contaminants must be added t o t h e list of
environmental v a r i a b l e s t h a t can p o t e n t i a l l y
a l t e r the r a t e of photosynthesis.
B e c a u s e of e a s e of h a n d l i n g a n d
experimental design, investigators studying the
r e l a t i o n s h i p between a i r p o l l u t a n t s and t r e e
photosynthesis have p r i m a r i l y employed t r e e
seedlings f o r research material and controlled
environmental f a c i l i t i e s for growth. Evidence
has been provided, under t h e above
circumstances, f o r photosynthetic suppression
caused by s u l f u r dioxide, ozone, f l u o r i d e ,
heavy metals and coal dust. The thresholds of
photosynthetic toxicity for tree seedlings vary
w i t h i n d i v i d u a l s p e c i e s and i n d i v i d u a l
pollutants.
For s e v e r a l s e e d l i n g s t h e
threshold of s u l f u r dioxide photosynthet' c
influence may approximate 1 ppm (2620 pg m-3
o r l e s s f o r an exposure of s e v e r a l hours. For
ozone, the threshold of photosyn e t i c response
may approximate 0.5 ppm (980 g m or l e s s f o r
an exposure of several days (Smith 1980).
9
Considerable r i s k i s associated with
extrapolation of seedling photosynthetic d a t a
accumulated i n c o n t r o l l e d e n v i r o n m e n t a l
f a c i l i t i e s t o older t r e e s i n n a t u r a l f o r e s t s .
Excised l e a f and s m a l l chamber techniques,
theref ore, have been employed t o assess the a i r
pollutant influence on photosynthetic rates of
t r e e s f ive-years-old and older. The use of
sapling-age experimental material avoids t h e
unique characteristics of seedling metabolism.
Evidence for f o r e s t t r e e sapling photosynthetic
suppression has been presented f o r s u l f u r
dioxide, ozone and cadmium. For sulfur dioxide
and ozone exposure, t h e s a p l i n g e v i d e n c e
suggests t h a t t h e threshold of photosynthetic
reduction may approximate 0.5 t o one ppm f o r 510 hours for one or two days (Smith 1980).
Much of the seedling and sapling evidence
suggests t h a t t h e photosynthetic i n h i b i t i o n
caused by s u l f u r d i o x i d e and ozone i s
reversible i f the pollutant s t r e s s is removed.
Under t h e circumstance of v a r i a b l e p o l l u t a n t
concentration i n ambient atmospheres, photosynthetic recovery might be common. Synergism,
o r g r e a t e r s t r e s s resulting from simultaneous
pollutant exposure relative t o either pollutant
alone, appears f r e q u e n t l y i n t h e seedling and
sapling literature. Evidence f o r s y n e r g i s t i c
photosynthetic suppression by s u l f u r dioxide
and ozone and f l u o r i d e and cadmium has been
presented. Almost a l l of t h e s t u d i e s r e p o r t
photosynthetic depression in the absence, or a t
l e a s t p r i o r to, t h e appearance of v i s i b l e
f o l i a r symptoms.
The evidence f o r a i r pollution induced
photosynthetic suppression i n l a r g e t r e e s i n
n a t u r a l environmentsis extremely meager and
sapling evidence
fragile.
The seedling
however, demonstrates a threshold of e f f e c t
t h a t approaches ambient concentrations i n
numerous temperate environments. Because of
the profound importance of t h e photosynthetic
process and t h e p o t e n t i a l f o r suppression by
widespread a i r contaminants, appropriate f i e l d
s t u d i e s must be conducted i n s p i t e of t h e i r
d i f f i c u l t y and cost. The o p p o r t u n i t y t o
examine t h e i m p a c t of c o n t a m i n a n t s on
r e s p i r a t i o n and t r a n s p i r a t i o n should a l s o be
included i n experimental designs. Inclusion of
one or both of these physiologic processes i n
seedling - sapling s t u d i e s has revealed some
indication for significant alteration.
Increased r e s p i r a t i o n coupled with reduced
p h o t o s y n t h e s i s c o u l d e x a c e r b a t e growth
consequences.
-
FOREST FOLIAGE
Under conditions of s u f f i c i e n t dose, a i r
p o l l u t a n t s d i r e c t l y cause v i s i b l e i n j u r y t o
forest trees. The accumulation of particulate
contaminants on leaf surfaces or the continued
uptake of gaseous p o l l u t a n t s through l e a f
stomata w i l l eventually r e s u l t i n c e l l and
tissue damage that w i l l be manifest i n f o l i a r
symptoms obvious t o t h e trained, but unaided
eye. This direct induction of disease i n trees
by a i r p o l l u t a n t s i s t h e most dramatic and
obvious individual t r e e response of a l l Class
I1 interactions.
I t i s t h e only Class I1
i n t e r a c t i o n t h a t can be detected i n t h e f i e l d
by c a s u a l o b s e r v a t i o n .
Unlike a l t e r e d
reproductive strategy, n u t r i e n t cycling, t r e e
metabolism or insect and disease relationships;
t h e degree of f o l i a r symptoms induced by a i r
p o l l u t a n t s can be r e l a t i v e l y easily observed,
inventoried and quantified. In the presence of
s u f f i c i e n t dose, t r e e damage may be of
sufficient severity t o cause mortality.
Acute f o l i a r disease may be caused i n
f o r e s t v e g e t a t i o n by w i d e s p r e a d a i r
contaminants including; s u l f u r dioxide,
nitrogen oxides, ozone, peroxyacetyl-nitrates,
f l u o r i d e and s e v e r a l t r a c e m e t a l s , and
localized a i r contaminants including acid rain,
ammonia, chlorine, hydrocarbons and hydrogen
sulfide. The response of woody plants t o these
atmospheric p o l l u t a n t s is extremely variable
and dramatically controlled by genetic factors,
p l a n t age and h e a l t h and e n v i r o n m e n t a l
conditions. F i e l d symptoms of a i r p o l l u t i o n
injury a r e not highly specific, are mimicked by
a wide variety of other t r e e s t r e s s factors and
a r e u s e f u l o n l y t o experienced observers
f a m i l i a r w i t h t h e r a n g e of e d a p h i c ,
entomological and pathological s t r e s s factors
c h a r a c t e r i s t i c of a given f l o r a i n a given
location. The dose required t o produce acute
i n j u r y v a r i e s w i d e l y w i t h p o l l u t a n t and
vegetative type. There has been s u f f i c i e n t
work done t o enable a generalized ranking of
r e l a t i v e f o r e s t t r e e s e n s i t i v i t y t o t h e most
important a i r p o l l u t a n t s (Davis and Wilhour
1976). A summary treatment of general symptoms
and i n j u r y t h r e s h o l d s f o r t h e gaseous
contaminants included i n t h i s section is
contained i n Smith (1980).
FOREST ECOSYSTEM RESPONSE
The primary response of a forest ecosystem
t o sustained intermediate dose and Class I1
i n t e r a c t i o n would be reduced growth and consequently reduced biomass. Reduced essential
element availability, decreased photosynthesis,
increased respiration, increased i n s e c t and
disease s t r e s s and decreased f o l i a r t i s s u e
would a l l contribute t o a reduction i n t r e e
growth rates and ultimately t o lessened forest
biomass.
Alterations i n t h e reproductive
s t r a t e g i e s of i n d i v i d u a l t r e e s p e c i e s o r
d i f f e r e n t i a l response of these species t o
reduced nutrition, altered metabolism and pest
s t r e s s and t o d i r e c t f o l i a r i n j u r y may cause
changes i n competitive a b i l i t y and u l t i m a t e l y
lead t o a l t e r a t i o n s i n t r e e succession and
species composition. Recent reviews of Class
I1 vegetative responses t o a i r p o l l u t a n t s
include Heck and o t h e r s (19772, Jensen and
others (1976) and Weinstein and McCune (1979).
Forest Growth
Forest growth is complex i n concept and
measurement. Addition of woody tissue is the
dominant f e a t u r e of f o r e s t growth. The
accumulation of woody biomass (1iving weight)
represents gross photosynthetic production
l e s s respiratory losses. The most fundamental
characteristic of an ecosystem is its product i v i t y . Forest productivity is high r e l a t i v e
t o other ecos stems nd n e t productivity of
1200 dry g m'year-'
f o r t r e e s and shrubs
together is quite typical for temperate forests
(Whittaker 1975). Productivity i s strongly
controlled, however, by a variety of variables
i n c l u d i n g system a g e and e n v i r o n m e n t a l
parameters. The most important of the l a t t e r
include n u t r i e n t a v a i l a b i l i t y , water availab i l i t y and temperature. Because of the variety
of Class I1 i n t e r a c t i o n s i d e n t i f i e d , a i r
quality also influences forest productivity i n
certain environments.
Productive f o r e s t s are critically
important, not only f o r t h e obvious relations h i p between wood volume and commercial
products i n managed f o r e s t s , but a l s o f o r t h e
regulation and maintenance of q u a l i t y f o r
associated ecosystems, amenity functions and
general climatic and t e r r e s t r i a l stability. It
is disconcerting t o r e a l i z e , theref ore, t h a t
there is substantial and impressive evidence t o
indicate that two widespread a i r contaminants,
s u l f u r dioxide and ozone, a r e capable of
reducing f o r e s t growth. The more l o c a l i z e d
release of fluoride can also reduce the amount
of f o r e s t biomass (Smith 1980).
Evidence from a v a r i e t y of s t u d i e s
examining f o r e s t growth i n t h e v i c i n i t y of
l a r g e p o i n t sources of s u l f u r dioxide has
i n d i c a t e d s i g n i f i c a n t l y reduced growth.
Generally the correlation of growth impact w i t h
degree of f o l i a r i n j u r y c a u s e d by s u l f u r
dioxide is not high. Growth retardation occurs
i n t h e absence of any v i s i b l e i n d i c a t i o n of
stress.
Most s u l f u r dioxide s t u d i e s have
accounted for precipitation influence on forest
growth over t h e study periods. Evidence f o r
ozone suppression of f o r e s t growth has been
provided by t h e comprehensive oxidant impact
study of the Western Montane forest ecosystem
i n California. Localized reduction of f o r e s t
growth may also occur i n environments subject
t o elevated l e v e l s of fluoride.
There a r e two s e r i o u s d e f i c i e n c i e s of
f o r e s t growth - a i r pollution s t r e s s research.
The f i r s t r e l a t e s t o the paucity of ambient a i r
quality determinations i n growth studies. This
makes establishment of dose thresholds or
c o r r e l a t i o n s of dose with growth influence
nearly impossible. The second serious l i m i t a tion relates t o the inability t o partition
reduced g r o w t h t o t h e v a r i o u s C l a s s I1
i n t e r a c t i o n s t h a t may actually be responsible
f o r it. For example, what percentage of
reduced growth may be due t o reduced nutrition,
reduced photosynthesis, increased i n s e c t or
disease a c t i v i t y or increased f o l i a r damage?
Future investigations of forest growth, a s
impacted by a i r q u a l i t y , must a l s o include
better accounts of growth inÂluencing f a c t o r s
other than p r e c i p i t a t i o n and a i r pollutants.
B e t t e r awareness of a d d i t i o n a l c l i m a t i c factors, impacts of insect and disease influence,
and management strategies must be indicated.
Forest Succession
A s a r e s u l t of t h e considerable v a r i e t a l
and s p e c i e s v a r i a t i o n i n r e l a t i v e
s u s c e p t i b i l i t y t o t h e v a r i o u s C l a s s I1
interactions, it is reasonable t o suppose t h a t
d i f f e r e n t i a l tolerance t o a i r pollution
influence a t the species level may be reflected
i n a l t e r e d p a t t e r n s of succession and s p e c i e s
composition a t the ecosystem level.
Ecologists recognize two major types of
processes t h a t influence ecosystem succession.
Autogenic processes a r e those r e s u l t i n g from
b i o l o g i c a l f a c t o r s w i t h i n t h e system.
In
f o r e s t ecosystems autogenic processes would
i n c l u d e s i t e a l t e r a t i o n s c a u s e d by t h e
vegetation, i n f l u e n c e of one p l a n t s p e c i e s on
another and impact of native insect or disease
microorganisms. Allogenic processes, on t h e
other hand, a r e abiotic factors t h a t influence
s u c c e s s i o n from w i t h o u t t h e system.
Geochemical and climatic forces a r e especially
important examples of a l l o g e n i c f a c t o r s t h a t
inÂluence f o r e s t ecosystems. I d e a l i z e d ecosystem development c h a r a c t e r i s t i c a l l y i s
portrayed a s an o r d e r l y change of b i o l o g i c a l
p r o g r e s s i o n o c c u r r i n g i n a more o r l e s s
constant environment (Odum 1969, Woodwell
1974). It has been g e n e r a l l y assumed t h a t
autogenic processes dominate a l l o g e n i c
processes in t e r r e s t r i a l ecosystem succession.
This g e n e r a l i z a t i o n , however, is q u i t e incons i s t e n t w i t h d a t a g e n e r a t e d by r e c e n t
imaginative s t u d i e s with f o r e s t ecosystems.
The importance of f i r e (an allogenic force) i n
influencing pre-settlement f o r e s t ecosystems i n
t h e North Central s t a t e s of t h e United S t a t e s
has been s u b s t a n t i a l (Loucks 1970, F r i s s e l l
1973, Heinselman 1973). The s i g n i f i c a n c e of
wind s t r e s s (an a l l o g e n i c f o r c e ) has been
suggested t o e x e r t s u b s t a n t i a l c o n t r o l over
successional development of f o r e s t ecosystems
i n New England (Stephens 1955, 1956, Raup 1957,
Henry and Swan 1974). F o r e s t management
p r a c t i c e s imposed by man, f o r example c l e a r cutting, may simulate the influence of natural
a l l o g e n i c f o r c e s on f o r e s t development and
i n t e r r u p t p r o g r e s s t o w a r d a steady s t a t e
c o n d i t i o n (Bormann a n d L i k e n s 1 9 7 9 ) .
Conversely other forest management procedures,
f o r example f i r e control, may e l i m i n a t e a
c o n t r o l l i n g a l l o g e n i c f o r c e and p e r m i t
succession t o proceed toward an unnatural
steady s t a t e condition. Class I1 s t r e s s e s
imposed on forest ecosystems by a i r pollutants
may be considered a 20th Century a l l o g e n i c
process of p o t e n t i a l importance t o f o r e s t
ecosystem development. A s i n t h e case of
clearcutting, t h i s human related force might be
expected t o a l t e r t h e a t t a i n m e n t of steady
s t a t e conditions. Air p o l l u t i o n s t r e s s would
appear t o have c e r t a i n unique q u a l i t i e s t h a t
may make it a n a l l o g e n i c i n f l u e n c e of
p a r t i c u l a r importance. Length of exposure t o
t h i s f o r c e precludes evolutionary adjustment
and i t s influence, i n c e r t a i n a r e a s , may be
q u i t e continuous r a t h e r than c y c l i c a s a r e
windstorms and f i r e s . What i s t h e evidence
a v a i l a b l e t o support t h e importance of a i r
pollution a s an allogenic force of significance
in forest ecosystem development?
I n 1968, p r i o r t o s o p h i s t i c a t e d
understanding of most Class I1 i n t e r a c t i o n s ,
Treshow (1968) provided an excellent review of
t h e i m p a c t of a i r c o n t a m i n a n t s on p l a n t
populations. Treshow's review, along w i t h a
v a r i e t y of a d d i t i o n a l l a t e 1960's papers, f o r
example Niklfeld (19671, ~ a j d f i kand ~ u s i 6 k a
(1968) and Trautmann and o t h e r s (19701, have
indicated a l t e r a t i o n s i n successional pattern
or s p e c i e s composition i n f o r e s t ecosystems
subject t o a i r pollution exposure.
The f o r e s t s of t h e San B e r n a r d i n o
Mountains i n southern C a l i f o r n i a have been
subject t o oxidant stress from the Los Angeles
m e t r o p o l i t a n complex f o r t h i r t y y e a r s .
Intensive investigations conducted i n t h e San
Bernardino National Forest over the years have
provided valuable insight and perspective on a
variety of forest a i r pollution relationships.
I n 1970, Cobb and Stark concluded t h a t i f a i r
pollution from the Los Angeles basin continued
t o increase, t h e r e w i l l be a conversion from
w e l l stocked f o r e s t s dominated by ponderosa
Doug ex. Laws) t o poorly
pine Qirui
stocked stands of l e s s susceptible tree species
i n the San Bernardino Mountains. Miller (1973)
has provided a thorough discussion of this
oxidant induced f o r e s t community change.
Ponderosa pine is one of f i v e major species of
the "mixed conifer type" that covers wide areas
of the western S i e r r a Nevada and t h e mountain
ranges, including the San Bernardino Mountains,
i n southern C a l i f o r n i a from 1000 t o 2000 m
(3000-6000 f e e t ) elevation.
Other s p e c i e s
r e p r e s e n t e d i n c l u d e s u g a r p i n e (W
l a m k r t h u Douql.) , white f i r Wigs
[Gord. & Glend.] L i n d l . ) , i n c e n s e - c e d a r
(WoceTorr.) and C a l i f o r n i a
b l a c k oak ( Q u e r c u
Newb.).
The
response of t h e s e f i v e major t r e e s p e c i e s t o
oxidant a i r contaminants i n the San Bernardino
National F o r e s t has been variable. Ponderosa
pine exhibits the most severe f o l i a r response
t o elevated ambient ozone. A 1969 a e r i a l survey
c o n d u c t e d by t h e U.S.D.A.
Forest Service
i n d i c a t e d 1.3 m i l l i o n ponderosa (or J e f f r e y ,
Pinus j e f f r e i Grev. & Balf.) p i n e s on more
than 405 km (100,000 acres) were s t r e s s e d t o
some degree. M o r t a l i t y of ponderosa pine has
been extensive. Actual death i s t y p i c a l l y
a t t r i b u t e d t o bark b e e t l e i n f e s t a t i o n of a i r
pollution stressed trees.
White f i r h a s
s u f f e r e d s l i g h t damage, but s c a t t e r e d t r e e s
have e x h i b i t e d severe symptoms. Sugar pine,
incense cedar and black oak have exhibited only
s l i g h t f o l i a r damage from oxidant exposure. A
233 ha (575 acre) study block w a s delineated i n
t h e northwest s e c t i o n of t h e San Bernardino
N a t i o n a l F o r e s t i n o r d e r t o conduct a n
i n t e n s i v e inventory of vegetation present i n
v a r i o u s s i z e c l a s s e s and t o e v a l u a t e the
h e a l t h f u l n e s s of t h e f o r e s t . Ponderosa p i n e s
i n the 30 can (12 inch) diameter class or larger
were more numerous than any other s p e c i e s of
comparable s i z e i n the study area. These pines
were most abundant on t h e more exposed r i d g e
c r e s t sites of the sample area. Mortality of
ponderosa pine ranged from 8-10 percent during
1968-1972. The l o s s of a dominant species i n a
f o r e s t ecosystem clearly exerts profound change
i n t h a t system. Miller concluded from h i s
investigation that the lower two-thirds of the
study a r e a w i l l probably s h i f t t o a g r e a t e r
proportion of white f i r . I t was judged t h a t
incense cedar w i l l probably remain secondary t o
w h i t e f i r . Sugar p i n e was presumed t o be
r e s t r i c t e d by l e s s e r competitive a b i l i t y and
dwarf m i s t l e t o e i n f e c t i o n . The r a t e of
composition change w a s deemed dependent on t h e
2
r a t e of ponderosa pine mortality. The upper
one-third of t h e study area, c h a r a c t e r i z e d a s
more environmentally severe due t o climatic and
edaphic s t r e s s , supports less vigorous white
f i r growth. Following l o s s of ponderosa pine
i n this area, sugar pine and incense cedar may
assume g r e a t e r importance.
M i l l e r judged,
however, t h a t n a t u r a l regeneration of t h e
l a t t e r s p e c i e s may be r e s t r i c t e d i n t h e more
barren, dry sites c h a r a c t e r i s t i c of t h e upper
ridge area. C a l i f o r n i a black oak and shrub
s p e c i e s may become more abundant i n t h e s e
disturbed areas. Additional and i n t e n s i v e
research on f o r e s t composition i n t h e San
Bernardino National Forest has been reported
(Miller 1977). Tree population dynamics were
examined on 18 permanent p l o t s established i n
1972 and 1973 and on 83 t e m p o r a r y p l o t s
e s t a b l i s h e d i n 1974 t o i n v e s t i g a t e f o r e s t
development a s a f u n c t i o n of t i m e s i n c e t h e
most recent f i r e . Generally the d a t a s t i l l
support the hypothesis t h a t f o r e s t succession
toward more tolerant species such as white f i r
and incense cedar occurs i n t h e absence of
f i r e . I n t h e presence of f i r e , pine may be
favored by seedbed preparation and elimination
of competing s p e c i e s . These more r e c e n t
studies suggest a larger number of f o r e s t subtypes may e x i s t w i t h i n the f o r e s t ecosystem
than i n i t i a l l y realized.
The changes i n f o r e s t composition caused
by oxidants in this southern California f o r e s t
have c r e a t e d a management concern, a s w e l l a s
e c o l o g i c a l change, b e c a u s e t h e f o r e s t i s
intensively used as a recreational resource and
the l o s s of ponderosa pine is judged t o reduce
aesthetic q u a l i t i e s of the forest.
Other examples, not as dramatic a s the San
Bernardino example, can be found. Hayes and
Skelly (1977) have monitored t o t a l oxidants and
associated oxidant injury t o eastern white pine
i n t h r e e r u r a l V i r g i n i a sites between A p r i l
1975 and March 1976. V a r i e t i e s of p i n e
categorized a s s e n s i t i v e and i n t e r m e d i a t e t o
oxidant s t r e s s were judged t o be under stress.
The authors speculated that susceptible eastern
LJ i n the Blue Ridge
white pine
and Southern Appalachian Mountains may be
rendered less competitive by a i r p o l l u t i o n
s t r e s s . S h i f t s i n s p e c i e s composition away
from white pine importance along with o t h e r
changes i n tree distributions may be occurring
i n certain eastern regions. Brandt and Rhoades
(1973) in t h e i r investigation of limestone dust
impact i n deciduous f o r e s t s i n southwestern
V i r g i n i a p r e d i c t e d changes i n s p e c i e s
composition r e s u l t i n g from d u s t influence.
Dusty s i t e s had reduced seedling and s a p l i n g
LJ, chestnut
density of red maple Q & ~ L
L.1 and red oak -(
oak (Quercw
Michx. £.I This observation along
w i t h documentation of reduced mean basal area
and l a t e r a l growth of t h e s e t r e e s , l e d t h e
a u t h o r s t o s u g. g.e s t t h a t y e l l o w - p o p l a r
L), more resistant t o
s t r e s s caused by d u s t accumulation, would
increase i n importance i n t h e s e hardwood
stands.
Treshow and Stewart (1973) have conducted
one of the few studies truly concerned with a i r
p o l l u t i o n i m p a c t on a n e n t i r e vegetative
community. Portable fumigation chambers were
placed over r e p r e s e n t a t i v e p l a n t s i n
intermountain grassland, oak, aspen and conifer
communities. Ozone fumigations were conducted
t o e s t a b l i s h i n j u r y thresholds f o r 70 common
plant species indigenous t o these communities.
G e n e r a l l y i n j u r y was e v i d e n t a t v a r yjJig
concentrations above 15 pphm (294 p g m 1.
Species that were found t o be most sensitive t o
ozone i n t h e grassland and aspen communities
investigated included some dominants which were
considered key t o community i n t e g r i t y . The
most dramatic example was aspen
h a n u l o i d e s Michx.) i t s e l f . Single two-hour
e x p o s u r e t o 1 5 pphm ozone caused s e v e r e
symptoms on 30 percent of the foliage exposed.
White f i r seedlings r e q u i r e aspen shade f o r
optimal juvenile growth. The authors judged
t h a t s i g n i f i c a n t aspen l o s s might r e s t r i c t
w h i t e f i r development and a l t e r f o r e s t
succession. In a companion study, Harward and
Treshow (1975) pursued t h e i r i n t e r e s t i n
evaluating ozone impact on aspen communities by
evaluating the growth and reproductive response
of 14 understory species t o ozone. Plants were
fumigated i n greenhouse chambers throughout
their growing seasons. It w a s concluded from
these fumigations t h a t p l a n t s e n s i t i v i t i e s
varied s u f f i c i e n t l y t o make probable major
s h i f t s i n composition i n aspen communities
following only a year or two of exposure t o
(137
ozone above concentrations of 7-15
294 (tg m 3 ) .
The a u t h o r s observed t h a t
comparable doses a r e widespread i n the vicinity
of urban a r e a s and t h a t widespread impacts on
p l a n t community s t a b i l i t i e s may be common i n
nature. The e f f o r t s of Michael Treshow and
c o l l e a g u e s h i g h l i g h t s t h e i m p o r t a n c e of
examining shrub and herb s t r a t a when assessing
a i r pollution impact on forest ecosystems.
(m
-
McClenahen (1978) has provided a most
interesting study with quantitative data on the
impact of polluted a i r on the various s t r a t a of
a f o r e s t ecosystem. F o r e s t vegetation was
measured i n seven stands on similar s i t e s in a
50 km area of the upper Ohio River Valley. The
stands were s i t u a t e d along a g r a d i e n t of
polluted a i r containing elevated concentrations
of chloride, s u l f u r dioxide, f l u o r i d e and
perhaps other contaminants. Species richness
(number of d i f f e r e n t s p e c i e s ) evenness
(dominance index - low values i n d i c a t e dominance by one or a few species) and Shannon
d i v e r s i t y index were typically reduced within
t h e overstory, subcanopy and herb s t r a t a near
i n d u s t r i a l sources of a i r contaminants. Increasing a i r pollutant exposure reduced canopy
stem density, but abundance of vegetation i n
other s t r a t a tended t o increase along the same
gradient. The r e l a t i v e importance of sugar
maple (AQX s a c c Marsh.)
~
was g r e a t t y
reduced i n all s t r a t a with increasing pollutant.
dose, while yellow buckeye ( A e s c w octandra
Marsh.) appeared tolerant of poor air quality.
In the shrub layer the importance of spicebush
b e n z a 1L.I B1.1 increased w i t h
increasing pollutant exposure.
(m
I n southern C a l i f o r n i a t h e predominant
n a t i v e s h r u b l a n d v e g e t a t i o n c o n s i s t s of
chaparral and c o a s t a l sage scrub. The former
occupies upper e l e v a t i o n s of t h e c o a s t a l
mountains, extending i n t o t h e North Coast
ranges, e a s t t o c e n t r a l Arizona, and south t o
Ba j a California; while t h e former occupies
lower e l e v a t i o n s on t h e c o a s t a l and i n t e r i o r
sides of the coast ranges from San Francisco t o
Baja C a l i f o r n i a . Westman (1979) a p p l i e d
standard p l a n t ordination techniques t o these
shrub communities t o examine the influence of
a i r pollution. The reduced cover of n a t i v e
species of c o a s t a l sage scrub documented on
some s i t e s was s t a t i s t i c a l l y indicated t o be
caused by elevated atmospheric oxidants. S i t e s
of h i g h a m b i e n t o x i d a n t s w e r e a l s o
characterized by declining species richness.
Influence of a i r p o l l u t i o n s t r e s s on
succession and ecosystem species composition
probably varies with the age and successional
s t a t u s of t h e f o r e s t .
Harkov and Brennan
(1979) have observed t h a t most woody p l a n t s
susceptible t o ozone injury are generally early
s u c c e s s i o n a l p l a n t s p e c i e s . Most t r e e s
intermediate or t o l e r a n t of ozone s t r e s s a r e
typically mid- or l a t e successional types. It
i s not unreasonable t o propose, a s Harkov and
Brennan did, t h a t l a t e successional f o r e s t
communities may be t h e most r e s i s t a n t t o
compositional change as a result of chronic a i r
pollution exposure. Mature ecosystems are a l s o
t y p i f i e d by other c h a r a c t e r i s t i c s t h a t may
increase t h e i r r e s i s t a n c e t o a i r p o l l u t i o n
stress.
Low n e t p r o d u c t i o n may reduce
potential importance of restrictions imposed by
a i r contaminants on photosynthesis. Closed and
slow nutrient cycling may make nutrient capital
l e s s l i a b l e t o l o s s by a i r pollutant influence.
There is increasing appreciation of t h e
i m p o r t a n c e of a l l o g e n i c f o r c e s on f o r e s t
ecosystem succession. The significance of f i r e
and wind s t r e s s on f o r e s t development is
s u b s t a n t i a l i n c e r t a i n environments. I t is
concluded t h a t a i r p o l l u t a n t impact may a l s o
exert c r i t i c a l l y important control over forest
succession and species composition. Long-term,
continual s t r e s s tends t o decrease t h e t o t a l
f o l i a r cover of v e g e t a t i o n , decrease t h e
s p e c i e s r i c h n e s s , and t o i n c r e a s e t h e
concentration of dominance by favoring a few,
tolerant species.
CONCLUSIONS
Large a r e a s of t h e t e m p e r a t e f o r e s t
ecosystem a r e c u r r e n t l y experiencing major
perturbation from a i r pollution. The influence
of a v a r i e t y of a i r c o n t a m i n a n t s on
biogeochemical cycling, patterns of succession
and competition and i n d i v i d u a l t r e e health,
designated Class I1 interactions (Smith 19801,
a r e causing s i g n i f i c a n t f o r e s t change i n t h e
temperate zone. A t t h e ecosystem l e v e l t h e
major p e r t u r b a t i o n s include decreased
productivity, biomass and d i v e r s i t y ; a t t h e
community l e v e l reduced growth; and a t t h e
population level a l t e r e d s p e c i e s composition.
E a r l y and m i d - s u c c e s s i o n a l f o r e s t s a r e
concluded t o be a t particular risk. Temperate
f o r e s t s have h i s t o r i c a l l y been subjected t o
major change resulting from the a c t i v i t i e s of
human beings.
For c e n t u r i e s t h e major
i n f l u e n c e was g r o s s d e s t r u c t i o n f o r
a g r i c u l t u r a l , f u e l o r o t h e r wood-product
purposes. In the present Century reduced need
f o r a g r i c u l t u r a l land and increased f o r e s t
management has reduced t h e adverse impact on
f o r e s t s i n temperate latitudes.
Human
a c t i v i t i e s of primary contemporary importance
t o f o r e s t structure and function have included
t h e i n t r o d u c t i o n of e x o t i c a r t h r o p o d and
m i c r o b i a l t r e e p e s t s i n t o f o r e s t systems
l a c k i n g e v o l u t i o n a r y exposure t o t h e s e
d e s t r u c t i v e agents, enhancement of native and
natural stresses by cultural practices, and the
creation of a r t i f i c i a l forests of one or a few
commercially important species. I n t h e p a s t
several decades, however, w e have accumulated
s u f f i c i e n t evidence t o i n d i c a t e t h a t an
a d d i t i o n a l major anthropogenic modifier of
temperate f o r e s t ecosystem development is a i r
pollution.
Research
During the l a s t decade f o r e s t researchers
have outlined numerous Class I1 interactions by
l a r g e l y u t i l i z i n g r e l a t i v e l y young f o r e s t
p l a n t s grown i n c o n t r o l l e d e n v i r o n m e n t
f a c i l i t i e s . During t h e next decade we must
make a n e f f o r t t o perform experiments i n
n a t u r a l f o r e s t e c o s y s t e m s t o confirm our
hypotheses t h a t a m b i e n t a i r p o l l u t i o n i s
reducing f o r e s t p r o d u c t i v i t y and a l t e r i n g
species composition.
The very highest research p r i o r i t y is
reserved f o r the establishment of comprehensive
investigations t o systematically examine Class
I1 interactions i n f o r e s t ecosystems located i n
t h o s e p o r t i o n s o f t h e t e m p e r a t e zone
particularly subject t o a i r pollution stress.
These investigations should include analysis of
a i r contaminant i n f l u e n c e on s o i l metabolism
and s t r u c t u r e f n u t r i e n t c y c l i n g , t r e e
reproduction, photosynthesis and r e s p i r a t i o n ,
important arthropod and microbial pathogens,
f o l i a r symptoms of important vegetation i n a l l
f o r e s t s t r a t a and a c a r e f u l examination of
f o r e s t p r o d u c t i v i t y and a l t e r a t i o n s i n
successional t r e n d s and s p e c i e s dominance.
These s t u d i e s w i l l be of extended term. They
w i l l r e q u i r e the p a r t i c i p a t i o n of numerous
s c i e n t i f i c d i s c i p l i n e s , minimally including
pathology, entomology meteorology, s o i l
science, s o i l microbiology, ecology and systems
analysis. Continuous meteorological and a i r
Air
q u a l i t y monitoring w i l l be required.
p o l l u t a n t s measured should include s u l f u r
dioxide, nitrogen oxides, hydrocarbons, ozone
and p a r t i c u l a t e s , t h e l a t t e r t o i n c l u d e
determination of s u l f a t e s , n i t r a t e s and t r a c e
metals.
P r e c i p i t a t i o n a c i d i t y w i l l be
routinely determined. The o b j e c t i v e of t h e s e
comprehensive s t u d i e s w i l l be t o c l a r i f y and
q u a n t i f y various Class I and I1 i n t e r a c t i o n s .
The ecosystems w i l l be evaluated f o r their
a b i l i t y t o r e s i s t ( i n e r t i a ) and respond
(resilience) t o disturbance from a i r pollution
s t r e s s . Model development f o r t h e various
i n t e r a c t i o n s w i l l h o p e f u l l y allow f u t u r e
projectionsr given various a i r q u a l i t y
sceneries, and allow extrapolation of findings
t o other ecosystems.
I n t h e United S t a t e s t h e only research
program presently addressing this need is the
oxidant study i n progress on the San Bernardino
I t is
National Forest i n California.
imperative t h a t a d d i t i o n a l i n v e s t i g a t i o n s be
i n i t i a t e d a s soon a s possible. The s t u d i e s
should be established i n those areas judged t o
be under the greatest stress and they should be
initiated, where possible, i n association with
integrated and comprehensive f o r e s t ecosystem
studies currently in progress. Priority f o r e s t
ecosystems i n t h e United S t a t e s include: 1)
Northern Hardwood f o r e s t , 2) Central Hardwood
f o r e s t and 3) Western Montane f o r e s t (San
Bernardino p r o j e c t i n progress). Appropriate
l o c a t i o n s , i n t e r m s of e x i s t i n g r e s e a r c h
f a c i l i t i e s or abundant ancillary information,
f o r t h e Northern f o r e s t a r e t h e Hubbard Brook
Experimental Forest i n New Hampshire, the Isle
Royale National Park, Michigan and t h e I t a s c a
Forest, Minnesota. I n t h e Central f o r e s t the
CampBranchForestwatershed i n e a s t - c e n t r a l
Tennessee and the Coweeta Hydrologic Laboratory
i n western North Carolina would be appropriate.
With regard t o l o c a t i o n , t h e Wayne National
Forest i n Ohio would appear t o represent an interesting research opportunity. In addition t o
t h e San Bernardino Forest study, t h e Andrews
Experimental Forest, Oregon and the Bitterroot
N a t i o n a l F o r e s t , I d a h o would be o t h e r
s t r a t e g i c a l l y located sites f o r the Western
Montane forest.
Policy
It is recognized t h a t a i r pollution is one
of t h e most s i g n i f i c a n t c o n t e m p o r a r y
anthropogenic s t r e s s e s imposed on temperate
forest ecosystems. Gradual and s u b t l e change
in forest m e t a b o l i s m and composition over wide
areas of the temperate zone over extended time,
rather than dramatic destruction of forests i n
t h e immediate v i c i n i t y of p o i n t sources over
s h o r t periods, m u s t be recognized a s t h e
primary consequence of a i r p o l l u t i o n stress.
This realization means t h a t forest interactions
with a i r contaminants must be given cons i d e r a t i o n i n d e l i b e r a t i o n s concerning clean
a i r laws and regulations, a l t e r n a t i v e energy
s t r a t e g i e s , i n d u s t r i a l and t r a n s p o r t a t i o n
location and forest research funding.
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