Secondary and Interactive Effects of
Chronic Gaseous Pollutant Exposure
of Producers, Consumers, and
Decomposers
Influence of Chronic Air Pollution
on Mineral Cycling in Forests1
Paul J. Zinke 2 Abstract: This paper reviews the literature concerning the impact of'chronic air pollution on mineral element cycling in forests. The concept involves the forest trees taking up essential and other elements from the soil and surrounding en-
vironment eventually to return them to the soil upon mortality and decay. Chronic pollutants are considered in the context of this cycling as another form of elemental addition to the site subject to cycling in the same manner. The review is organized to assess the addition of the major elements, carbon, nitrogen, and sulfur, and the trace metallic elements. In addition, pollutant effects upon the ecosystem living components in terms of producers and decompos- ers are considered along with potential changes in the redox and pH state of the different portions of the forest. Some oriuinal data on foliar comnosition of Big Cone Spruce (Pseudotsuga macrocarpa (vasey) Mayr) in relation to pollution exposure, and the evaluation of a soil subject to increments o$ hydrogen in simu- lated acid rain leaching are presented. INTRODUCTION
T h i s paper w i l l p r e s e n t a review of
various
aspects
of
mineral
element
c y c l i n g i n f o r e s t s a s a f f e c t e d by c h r o n i c
atmospheric p o l l u t i o n .
L
Presented at the Symposium on Effects
of Air Pollutants on Mediterranean and
Temperate Forest Ecosystems, June 22-27,
1980, Riverside, California, U.S.A.
Associate Professor of Forestry, Dep.
of Forestry and Resource Manage., University of California, Berkeley, Calif.
The f o r e s t w i l l be c o n s i d e r e d t o b e
t h e s t a n d of t r e e s and t h a t p o r t i o n o f
t h e atmosphere encompassed by canopy and
t r u n k s p a c e , and t h e p o r t i o n o f t h e s o i l
encompassed by t h e r o o t s p a c e .
Mineral
c y c l i n g i s t h e p r o c e s s of c y c l i n g of e l e ments from t h e s o i l t h r o u g h u p t a k e by
r o o t s o r by f o l i a g e , t r a n s p o r t w i t h i n t h e
t r e e s and t h e e v e n t u a l r e t u r n t o t h e
f o r e s t s o i l i n t h e processes of f o l i a r
leaching, root exudation, f o l i a g e drop,
e t c . Return t o t h e s o i l s t o r a g e occurs,
and t h e c y c l e i s c o n t i n u e d by u p t a k e
a g a i n , o r i t may be broken by l o s s from
t h e s o i l , o r t i e u p as i n s o l u b l e p r e c i p i A i r p o l l u t i o n expot a t e s o r compounds.
s u r e w i l l be c o n s i d e r e d t o b e t h e a d d i t i o n a l a t m o s p h e r i c i n p u t s which e n t e r t h e
nutritional
and
elemental
cycle
of
f o r e s t s due t o man made e f f e c t s on atmosp h e r i c composition.
ELEMENTAL CYCLIdG
The i d e a o f t h e c y c l i n g of e l e m e n t s
from v e g e t a t i o n t o s o i l , f o l l o w i n g u p t a k e
from
s o i l probably
outdates written
r e c o r d s as i s a p p a r e n t from t h e p r i m i t i v e
a g r i c l t u r a l p r a c t i c e of s h i f t i n g cultivat i o n wherein a f o r e s t i s c u t and burned
f o r s o i l enrichment by t h e a s h .
This i s
f o l l o w e d by t h e regrowth o f a f a l l o w
f o r e s t c r o p , which i n t u r n i s burned
again.
The f o r e s t v e g e t a t i o n c y c l e s e l e ments e s s e n t i a l f o r v e g e t a t i v e growth as
w e l l as u n n c e s s a r y e l e m e n t s a c c i d e n t a l t o
t h e p a r t i c u l a r environment. The 16 o r 1 7
e s s e n t i a l e l e m e n t s ( c , d, 0, P, K, N, S,
C a , Fe, Mg, Mn, Cu, Zn, Mo, B, C l , and
p e r h a p s S e ) , a r e c y c l e d by n e c e s s i t y f o r
w i t h o u t them t h e r e would be no f o r e s t .
I n a d d i t i o n a l m o s t e v e r y o t h e r element i s
t r a n s l o c a t e d by p l a n t s .
T h i s concept i s
used i n geochemical p r o s p e c t i n g f o r many
o f t h e more v a l u a b l e e l e m e n t s , u s i n g t h e
p l a n t as a chemical p r o s p e c t o r (NASA
1 9 6 8 ) . These e l e m e n t s which a r e c y c l e d
may be e n r i c h e d i n c o n c e n t r a t i o n i n v a r i ous p o r t i o n s of t h e c y c l e , as i n t h e
foliage,
the
plant
d e t r i t u s on t h e
ground, o r i n t h e s u r f a c e o f t h e s o i l
beneath t h e p l a n t s .
Such enrichment i s
o f t e n t h e i n d i c a t i o n of an extraneous
element. S i m i l a r l y t h e input of extraneous e l e m e n t s i n t h e p r o c e s s o f p o l l u t i o n
may b e evidenced by enrichment o v e r t h e
normal background amounts.
The s t a t e o f t h e v e g e t a t i o n and i t s
capacity f o r storage of elements w i l l
d e t e r m i n e t h e r e l a t i v e change induced by
t h e a d d i t i o n o f a p o l l u t a n t element. The
s t a t e o f t h e v e g e t a t i o n is p a r t l y d e t e r mined by t h e f a c t t h a t v e g e t a t i o n i s a
g i a n t r e d u c t i o n r e a c t i o n i n which phot o s y n t h e s i s r e d u c e s c a r b o n from carbon
d i o x i d e t o c a r b o n i n reduced carbon comounds as d e s c r i b e d by Stumm and -Morgan
71 970)
The f o r e s t t r e e s c a r r y o u t t h i s
r e d u c t i o n r e a c t i o n , f o l l o w e d by t h e i r
d e a t h and t h e s u b s e q u e n t o x i d a t i o n of t h e
carbon
compounds
in
the
soil.
The
c y c l i n g of t h e e l e m e n t s on t h e s i t e
o c c u r s i n t h e c o n t e x t o f t h i s g i a n t redox
r e a c t i o n ( ~ a r r e l s ,e t a l . , 1 9 7 5 ) , and i t s
s t a t e and magnitude d e t e r m i n e t h e r a t e
and amount a t which t h e o t h e r e l e m e n t s
w i l l be c y c l e d .
.
The c y c l i n g of most o f t h e e l e m e n t s
which undergo redox changes i n t h e f o r e s t
) ill
n u t r i e n t c y c l e (C H 0 N S Mn ~ e w
tend
to
be
reduced
i n the
living
v e g e t a t e d p o r t i o n o-f t h e c y c l e and comp l e t e t h e c y c l e t o an o x i d i z e d form i n
the soil.
However, l o c a l s o i l f a c t o r s
f a v o r i n g a n a e r o b i c c o n d i t i o n s such as
w a t e r i n e x c e s s , may c a u s e t h e s o i l t o
become a s i n k f o r some e l e m e n t s i n t h e
reduced form, o r f o r o t h e r e l e m e n t s i n
t h e o x i d i z e d form.
Thus p o l l u t a n t s may e n t e r t h e e l e mental c y c l e s i n f o r e s t s and v a r y i n
m o b i l i t y depending upon t h e redox potent i a l a t v a r i o u s p o r t i o n s of t h e e l e m e n t a l
cycle.
Some p o l l u t a n t s may a l s o b e oxidants i n r e l a t i o n t o the portion of t h e
ecosystem t h a t i s a b s o r b i n g them and t h u s
a f f e c t t h e redox p o t e n t i a l a t t h a t p o i n t
a c c o r d i n g t o Haagen-Smit ( 1 9 5 8 ) .
STORAGE POINTS AND SINKS
The soil and vegetation of the forest have several points of long term s t o r a g e o f m a t e r i a l s added t o t h e element a l c y c l i n g system.
It h a s been l e a r n e d
from p a s t f e r t i l i z a t i o n e x p e r i e n c e t h a t
e l e m e n t s added t o t h e f o r e s t , e i t h e r t o
s o i l o r d i r e c t t o t r e e s , may b e s t o r e d
f o r v a r y i n g p e r i o d s of t i m e i n d i f f e r e n t
p o r t i o n s of t h e f o r e s t .
Obviously, t h e
t r e e trunks
provide
storage of t h e
m a t e r i a l s c o n t a i n e d i n t h e wood f o r t h e
l e n g t h of l i f e o f t h e t r e e and i t s subseq.uent decomposition t i m e . Deciduous port i o n s of t h e t r e e r e t a i n m a t e r i a l s f o r
l e n g t h s of t i m e p r o p o r t i o n a t e t o t h e i r
r e s i d e n c e t i m e on t h e t r e e ; b a r k f o r
l o n g e r p e r i o d s , l e a v e s and t w i g s f o r
l e s s e r p e r i o d s . The s t o r a g e t i m e i n t h e
decomposing o r o x i d i z i n g p o r t i o n s o f t h e
d e t r i t u s dropped t o t h e s o i l depends upon
l o c a l environmental c o n d i t i o n s of temp e r a t u r e , redox s t a t e , and a v a i l a b i l i t y
o r t o x i c i t y of e l e m e n t s t o decomposing
( oxidizing)
organisms.
For
example,
decomposition t i m e s f o r s u r f a c e d e t r i t u s
on t h e s o i l s u r f a c e i n a f o r e s t may v a r y
from a f r a c t i o n o f a y e a r t o many y e a r s .
The s o i l b e n e a t h t h e f o r e s t i s a
g i a n t fixed-bed i o n exchanger, and once
elements e n t e r t h e s o i l f o l l o w i n g r e l e a s e
from s t o r a g e i n t h e v e g e t a t i v e p o r t i o n o f
t h e f o r e s t and i t s d e t r i t u s t h e y may b e
s t o r e d on t h i s exchange complex.
The
c a p a c i t y of t h i s i o n exchange bed as w e l l
as t h e n a t u r e o f a s s o c i a t e d c a t i o n s w i l l
determine t h e s t o r a g e p r o b a b i l i t y of elements added t o t h e f o r e s t
whether as
additives (pollutants, f e r t i l i z e r s ) , or
i n t h e normal c o u r s e of m i n e r a l weathering or r a i n f a l l additions.
The t o t a l
c a p a c i t y o f t h i s bed f o r c a t i o n exchange
i n c o n i f e r o u s f o r e s t s o i l s r a n g e s from 40
t o 300 gm e q u i v a l e n t s per meter s q u a r e d
t o a meter d e p t h ( Z i n k e , & g . , 1 9 7 9 ) .
Whether t h e p o l l u t a n t added h a s a s i g n i f i c a n t e f f e c t depends upon t h e n a t u r a l
base l i n e composition o f o t h e r c t i o n s o n
t h e s o i l column ( u s u a l l y H , Ca¥f, Mg ,
K',
N a ) maintained.
by t h e f o r e s t and
the lyotropic
series
( l e a c h i n g precedence) of t h e s e e l e m e n t s .
The f o r e s t
s o i l a l s o h a s a n i o n exchange c a p a c i t y
a l t h o u g h u s u a l l y of l e s s e r amount. Thus,
depending upon t h e n a t u r e of t h e p o l l u -
t a n t a d d i t i v e , and whether i t a t t a i n s
i o n i c form, i t may be s u b j e c t t o scrubb i n g out a t t h e s o i l exchange complex
stage of t h e elemental cycle.
T h i s would
a p p l y t o t h e hydrogen and s u l f a t e o f a c i d
r a i n , o r t h e c a t i o n i c forms o f some
m e t a l l i c p o l l u t a n t s such as l e a d o r z i n c .
L a b o r a t o r y s i m u l a t i o n through l e a c h i n g
w i t h s u c c e s s i v e i n c r e m e n t s of t h e p o l l u t a n t such as a c i d r a i n can be made
r e a d i l y t o d e t e r m i n e t h i s c a p a c i t y , and
an example o f t h i s f o l l o w s l a t e r .
The s o i l h a s o t h e r c a p a c i t i e s f o r
storage of a d d i t i v e s i n addition t o t h a t
of t h e i o n exchange c a p a c i t i e s .
Either
f o l l o w i n g b r e a k t h r o u g h o r s a t u r a t i o n of
t h e exchange c a p a c i t y , an a d d i t i v e e l e ment may be s t o r e d on t h e m e t a l l i c o x i d e
complex of t h e s o i l , o r as i n s o l u b l e prec i p i t a t e s or oxides.
The r e l e a s e and
u p t a k e o f e l e m e n t s i n t o s t o r a g e i n assoc i a t i o n with t h e m e t a l l i c oxides ( u s u a l l y
i r o n and manganese) w i l l depend upon t h e
pH and redox p o t e n t i a l of t h e s o i l as
reviewed by Jenne ( 1 9 6 8 ) . R e t e n t i o n w i l l
be l e a s t under t h e r e d u c i n g c o n d i t i o n s
brought about by l a r g e amounts of o r g a n i c
m a t t e r and p o o r l y d r a i n e d
wet conditions.
-
Thus, t h e f o r e s t s o i l i s a major
determinant i n the f a t e of t h e chronic
p o l l u t a n t element added t o t h e f o r e s t .
The b r e a k t h r o u g h c a p a c i t y of t h e s o i l
f o r t h e added m a t e r i a l w i l l depend upon
t h e c u r r e n t i n p u t o f s i m i l a r e l e m e n t s by
t h e n a t u r a l c y c l i n g of c a t i o n s from t h e
t r e e c o v e r , t h e i n p u t s by c u r r e n t m i n e r a l
weathering,
t h e current additions of
hydrogen from r a i n f a l l and o r g a n i c compounds produced by t h e f o r e s t , t h e deplet i o n o f b a s i c m e t a l l i c c a t i o n s t a k e n up
by t h e t r e e growth as t h e t r e e s a g e on
the s i t e .
The g r e a t e r t h e s t o r a g e capac i t y of t h e s o i l e i t h e r as i o n exchange
o r m e t a l l i c oxide (hydrous) c a p a c i t y t h e
g r e a t e r the buffering capacity of the
f o r e s t on t h e i n p u t o f p o l l u t a n t s .
It w i l l be o f i n t e r e s t now t o review
some o f t h e e x p e r i e n c e o f how t h e v a r i o u s
p o l l u t a n t s behave i n r e l a t i o n t o t h e s e
processes
of
elemental
cycles
in a
forest.
POLLUTANT ADDITIVES TO FOREST CYCLES
Any of t h e e l e m e n t s added t o t h e
f o r e s t as p o l l u t a n t s can i n f l u e n c e e l e mental c y c l i n g , e i t h e r by a c t i n g as
n u t r i e n t e l e m e n t s r e q u i r e d f o r t h e growth
o f t r e e s , by changing t h e redox s t a t e o f
any p a r t of t h e f o r e s t , o r by changing
t h e pH a t some p o i n t i n t h e system. Some
o f t h i s i n t e r a c t i o n may b e p h y s i o l o g i c a l
i n t h e v e g e t a t i o n , o r i n t h e s o i l micro-
f l o r a , o r may be a m a t t e r o f s o i l chemistry.
Growth r a t e s of t h e v e g e t a t i o n may
b e changed, t h u s a f f e c t i n g t h e r a t e s of
e l e m e n t a l c y c l i n g . Each p o l l u t a n t may
have s e p a r a t e e f f e c t s depending upon i t s
chemical and p h y s i o l o g i c a l n a t u r e , and
t h e r e may b e s y n e r g i s t i c e f f e c t s w i t h
combinations of a d d i t i v e s .
Some o f t h e
major c h r o n i c p o l l u t a n t s w i l l be cons i d e r ed s e p a r a t e l y .
Carbon
Compounds &
i Accompanying
dan-fcs Oxi-
Carbon a d d i t i o n s t o t h e f o r e s t may
b e i m p o r t a n t because o f t h e r o l e t h e y
p l a y i n p l a n t growth and s u b s e q u e n t
mineral cycling.
F i n l a y s o n and P i t t s
(1976) have r e p o r t e d t h a t c a r b o n may
account f o r 45$ of t h e mass o f smog aeros o l . Much o f t h i s may b e t h e r e s u l t o f
secondary r e a c t i o n s c r e a t i n g c a r b o x y l i c
acids,
esters,
carbonyl
compounds,
a l c o h o l s , p e r o x i d i c polymers, l o n g c h a i n
a l k a n e s and a l k e n e s , and f a t t y a c i d s .
In
a d d i t i o n , c a r b o n i n t h e forms of v a r i o u s
compounds i s a world-wide
atmospheric
p o l l u t a n t due t o human a c t i v i t i e s o x i d i z i n g reduced carbon f o r e n e r g y , and t o
i n d i r e c t e f f e c t s such as enhanced oxidat i o n of s o i l o r g a n i c m a t t e r due t o c l e a r ing forestland for agriculture.
Thus
carbon d i o x i d e as a c h r o n i c p o l l u t a n t h a s
been measured by o b s e r v a t i o n s a t Mauna
Loa (Hawaii) t o b e r i s i n g a t t h e r a t e o f
from .35 t o 1 .79 ppm per y e a r t o a l e v e l
, 1974).
of 325 ppm i n 1 974 (Hobbs, g
P e t e r s o n (1969) i n a review s t a t e d t h a t
carbon d i o x i d e a t i t s p r e s e n t l e v e l i n
t h e atmosphere i s s t i l l l i m i t i n g t o p l a n t
growth and t h a t t h e p r o d u c t i v i t y
of
p l a n t s should i n c r e a s e as t h e C o n c o n t e n t
increases. A r e s u l t i n g increase of plant
and f o r e s t growth of 5$ by t h e y e a r 2000
is a ' p r e d i c t e d , and t h i s would i n c r e a s e
t h e r a t e s of u p t a k e o f n e c e s s a r y growth
e l e m e n t s from t h e s o i l , t h u s i n c r e a s i n g
r a t e s of elemental cycling.
This a l l
assumes o t h e r e l e m e n t s o r r e q u i r e m e n t s
such as water a r e n o t l i m i t i n g t o p l a n t
growth. On t h e o t h e r hand, r e d u c t i o n i n
p l a n t growth may occur where t o x i c c a r b o n
compounds from p o l l u t i o n c a u s e damage t o
t r e e f o l i a g e , thus reducing r a t e s of
mineral cycling.
Ozone produced as a
secondary p r o d u c t from u l t r a v i o l e t radiat i o n on hydrocarbons i n t h e atmosphere
may r e d u c e p l a n t growth.
Evans, g &.
( 1 974) found ozone c o n t e n t s of 0.1 ppm a t
t h e t o p of a smoke plume from a f o r e s t
fire.
However p l a n t s s y n t h e s i z e methyl
c h l o r i d e a c c o r d i n g t o Lovelock (1 9 7 5 ) ,
and t h i s may d e s t r o y s u c h added ozone.
The o x i d a n t s formed from t h e o r g a n i c poll u t a n t s i n t r o d u c e d t o t h e atmosphere w i l l
have a d v e r s e e f f e c t s upon v a r i o u s amino
a c i d s i n p l a n t s r e s u l t i n g i n damage
&.
(Haagen-Smit , 1 9 5 8 ) .
F a t t y a c i d s on
p l a n t s u r f a c e s may be a l t e r e d by t h e
s i n g l e t oxygen r e s u l t i n g from NO2, benz a l d e h y d e , and p o l y n u c l e a r hydrocarbons,
increasing saturated acid content of t h e
f o l i a g e a c c o r d i n g t o Dowty
&. (1 9 7 3 ) .
Other
oxidants
such as p e r o x y a c e t y l
n i t r a t e ( P A N ) , hydroxyl OH, hydroperoxyl
HO , a l s o have similar e f f e c t s on vegetati$n.
T h e i r e f f e c t s as o x i d a n t s a r e
d e f i n e d by t h e i r c a p a b i l i t y t o o x i d i z e
i o d i d e i o n i n aqueous s o l u t i o n of potassium i o d i d e a c c o r d i n g t o Kuntz, e t 9.
(1 973).
Also, t h e i r a c t i o n may b e s y n e r g i s t i c , s o t h a t a l t h o u g h one o r a n o t h e r
i s i n low a t m o s p h e r i c c o n c e n t r a t i o n t h e
sum of t h e o x i d a n t s must be c o n s i d e r e d i n
e f f e c t on t h e v e g e t a t i o n .
Also, t h e
v o l a t i l e t e r p e n e s produced by t h e f o r e s t
i t s e l f must b e t a k e n i n t o a c c o u n t , and
a c c o r d i n g t o Rasmussen (1 9 7 0 ) , as many as
1008 of t h e s p e c i e s i n some w e s t e r n conif e r o u s f o r e s t s may produce such v o l a t i l e
hydrocarbons.
Nitrogen
N i t r o g e n as i t c y c l e s i n t h e f o r e s t
i s i n reduced form i n t h e p l a n t and f o l lowing m i n e r a l i z a t i o n
to
ammonia
in
decomposing d e t r i t u s i n t h e s o i l it is
g r a d u a l l y o x i d i z e d t o n i t r a t e where i t i s
a g a i n t a k e n up by p l a n t s t o b e reduced i n
v a r i o u s n i t r o g e n compounds.
Nitrogen is
added as a c h r o n i c a i r p o l l u t a n t as
ammonium, and n i t r a t e n i t r o g e n which a l s o
i s t h e end p r o d u c t o f o x i d a t i o n of 80 by
ozone. Where n i t r o g e n i s l i m i t i n g i n t h e
f o r e s t as an e s s e n t i a l element t h i s
s h o u l d s t i m u l a t e f o r e s t growth and decomp o s i t i o n p r o c e s s e s provided o t h e r e l e ments a r e n o t l i m i t i n g .
However, i f
o t h e r e l e m e n t s a r e l i m i t i n g t h i s would
t e n d t o emphasize t h e o t h e r d e f i c i e n c i e s .
A d d i t i o n s as a c h r o n i c p o l l u t a n t should
show similar symptoms t o t h o s e o f t h e
a d d i t i o n o f n i t r o g e n as a f e r t i l i z e r .
Thus f o l i a r n i t r o g e n c o n t e n t s should be
h i g h e r . A r e s u l t similar t o t h i s encount e r e d i n Big cone s p r u c e f o l i a g e i n t h e
San B e r n a r d i n o mountains i s r e p o r t e d
l a t e r i n t h i s paper.
S-u l f u r
The s u l f u r c y c l e i n f o r e s t s i s such
t h a t t h e s u l f u r i s i n reduced form i n
a s s o c i a t i o n w i t h o r g a n i c compounds i n t h e
p l a n t s , b u t i s o x i d i z e d upon decomposit i o n i n the organic d e t r i t u s returned t o
the soil.
The decomposing s o i l microf l o r a c o n v e r t t h e s u l f u r t o s u l f a t e . The
d e g r e e t o which t h i s t a k e s p l a c e depends
upon t h e redox p o t e n t i a l of t h e s o i l . For
example, i f i t i s v e r y low, t h e s u l f u r
w i l l be r e t a i n e d i n s u l f i d e form, f r e q u e n t l y t y i n g up heavy m e t a l s .
The forms o f s u l f u r added i n c h r o n i c
atmospheric p o l l u t i o n have been SO?,
SO ", w i t h a s s o c i a t e d c a t i o n s H , NH
a n t HSO
as determined i n t h e p o l l u t h ~
plume trim S t . L o u i s M i s s o u r i by CharlThey found t h a t
s o n , g 9. ( 1 9 7 3 ) .
t r o p i c a l a i r masses were dominated by t h e
more a c i d i c NH HSO w h i l e n o r t h e r n a i r
masses were l e s s a c i d i c and dominated by
(NH ) SO (1 9 7 5 ) . U s u a l l y t h e s u l f u r i n
the4a?mo%-phere w i l l be o x i d i z e d t o s u l f a t e and t h i s w i l l o c c u r e i t h e r
as
ammonium o r c a l c i u m s u l h a t e d u s t a c c o r d and s i n c e
i n g t o daagen-Snit
t r a p p i n g s u r f a c e s o f v e g e t a t i o n a r e aerob i c , any reduced s u l f u r w i l l be o x i d i z e d
t o sulfate in the foliage.
(1959),
S i n c e s u l f u r is a n e s s e n t i a l element
f o r p l a n t growth, t h e a d d i t i o n s may o r
may n o t b e d e l e t e r i o u s
A c t u a l d e l e t e r ious e f f e c t s would occur t o t r e e s i f s u l f u r d i o x i d e were t h e main a d d i t i v e .
This
would occur o n l y c l o s e t o t h e e m i s s i o n
s o u r c e as h a s happened a t K e n n e t t , C a l i f o r n i a ; Copper B a s i n , Tennessee; and Sudbury, Ontario. A t g r e a t e r d i s t a n c e t h i s
would be o x i d i z e d .
Presumably i f t h e
p o l l u t a n t were added i n extreme amounts,
t h e t i t r a b l e a c i d i t y produced would b r e a k
t h r o u g h t h e s o i l exchange c a p a c i t y a f t e r
depleting other cations present.
An
example o f a s i m u l a t i o n o f t h i s i s
offered i n t a b l e 2 explained l a t e r .
.
T r a c e Elements
lusts
'
.
Washout, P a r t i c u l a t e s ,
Most o f t h e e l e m e n t s o t h e r t h a n C ,
N, and S w i l l be added i n d u s t and r a i n
as c h r o n i c p o l l u t a n t s .
The p a r t i c u l a t e s
i n atmospheric p o l l u t i o n c o n t a i n elements
such
as
lead,
sodium,
magnesium,
aluminium, vanadium, and z i n c i n Los
Angeles t y p e smog a c c o r d i n g t o F i n l a y s o n
Sedimentary c o r e s
and P i t t s ( 1 976).
t a k e n o f f s h o r e i n t h e P a c i f i c Ocean by
Bruland, e t S., ( 1 9 7 4 ) , i n d i c a t e d t h a t
l e a d , s i l v e r , c o p p e r , z i n c , chromium,
nickel,
molybdenum,
and
cobalt
are
c h r o n i c p o l l u t a n t s i n t h e Los Angeles
area.
Lead, i r o n , manganese, n i c k e l ,
copper and z i n c were analyzed i n p r e c i p i t a t i o n as common t r a c e element p o l l u t a n t s
throughout t h e U.S. a c c o r d i n g t o Lazarus
Beryllium is common i n
e t a l . (1 9 7 0 ) .
i n d u s t r i a l d u s t s n e a r s o u r c e s . The amount
of t r a c e element f a l l o u t l e s s e n s as t h e
s q u a r e o f t h e d i s t a n c e from s o u r c e s
a c c o r d i n g t o B e r t i n e & Goldberg ( 1 9 7 4 ) .
Cannon and B o l e s (1962) found t h a t highways r e p r e s e n t e d l i n e a r s o u r c e s f o r l e a d ,
the
amount
in
vegetation
decreasing
r a p i d l y w i t h d i s t a n c e from t h e s o u r c e .
( 1 970) found t h a t t h i s
Dedolph e t
d i m u n i t i o n was l o g a r i t h m i c w i t h d i s t a n c e
f o r p a r t i c u l a t e l e a d . However, some e l e ments such as cadmium, n i c k e l , l e a d , and
-
z i n c may b e v a p o r i z e d a t t h e s o u r c e and
carried longer distances according t o
L a g e r w e r f f & S p e c h t (1 9 7 0 ) .
The t r a c i n g o f i n p u t o f t r a c e e l e ments i n t h e e l e m e n t a l c y c l e s i n vegetat i o n h a s b e e n a t t e m p t e d by many i n v e s t i gators.
C h e s t e r and S t o n e r (1 973) used
a n e n r i c h m e n t f a c t o r i n which a r a t i o o f
t h e element t o iron. i n t h e p a r t i c u l a t e
b e i n g added i s d i v i d e d by t h e a v e r a g e
r a t i o of t h e element t o i r o n i n t h e
earth's crust.
They f o u n d
that tin,
l e a d , and z i n c most o f t e n were t h e e l e ments enriched by p o l l u t i o n .
Peirson, e t
a l . (1 9 7 4 ) employed a n e n r i c h m e n t f a c t o r
i n t h e form o f t h e r a t i o o f t h e e l e m e n t
t o Scandium c o n t e n t , compared t o t h e same
for the local soils.
They f o u n d t h e
s o i l s e n r i c h e d f o r V, Co, N i , Zn, A s , S e ,
Sb, and Pb t h i s way.
S i m i l a r enrichment
r a t i o s f o r o t h e r p o l l u t a n t s should ident i f y augmentations of t h e elements i n
elemental cycles i n f o r e s t s .
-
The c o n t e n t s o f p o l l u t a n t s i n t h e
plants
should
be
identifiable
by
anomalies i n composition.
Thus, Schackl e t t e and Connor (1 9 7 3 ) u s e d t h e r e g i o n a l
v a r i a t i o n of vanadium i n S p a n i s h moss
( ~ i l l a n d s i a )along t h e gulf coast of t h e
U.S. t o i d e n t i f y a r e a s where c h r o n i c p o l l u t i o n b y a i r b o r n e vanadium o c c u r s .
Cont e n t s as h i g h as 560ppm V were found i n
c e r t a i n a r e a s , and t h e s e were assumed t o
r e p r e s e n t t h e o u t p u t from o i l r e f i n e r i e s
u s i n g V e n e z u e l a n c r u d e o i l which i s h i g h
i n vanadium.
In soil-vegetation cycling,
vanadium i s f r e q u e n t l y h e l d a t t h e s o i l r o o t i n t e r f a c e due t o i m m o b i l i z a t i o n i n
t h e oxidized s t a t e (pentavalent form).
Thus, t h e r e d o x s t a t e o f
the soilv e g e t a t i o n s y s t e m and i t s components i n
t h e f o r e s t may d e t e r m i n e where a c h r o n i c
p o l l u t i n g e l e m e n t may b e i m m o b i l i z e d .
Elements undergoing changes i n s o l u b i l i t y
w i t h v a r i o u s o x i d a t i o n s t a t e s may b e
i m m o b i l i z e d a t v a r i o u s i n t e r f a c e s where
pH o r Redox c h a n g e .
Chromium, vanadium,
manganese, and i r o n a r e s u s c e p t i b l e t o
this.
Some o f t h e c h r o n i c p o l l u t a n t s added
t o t h e e l e m e n t a l c y c l e o f f o r e s t s may
l a t e r b e r e l e a s e d from t h e f o r e s t by
vaporization.
F o r example, C u r t i n e t a l .
( 1 974) found t h a t t i n i s t r a n s p i r e d i n
v a p o r s from c o n i f e r s t o t h e amount o f
23-80 ppm i n t h e r e s i d u e o f t h e v a p o r .
They f o u n d t h a t some c o n i f e r o u s t w i g s
c o n t a i n e d up t o 6-40 ppm t i n i n t h e a s h .
The t i n w a s added as a t m o s p h e r i c p o l l u t a n t i n d u s t from i n d u s t r i a l a r e a s .
Howe v e r , n o m e n t i o n w a s made o f t h i s as
being deleterious.
The
inputs
of
dry
particulate
m a t e r i a l s as d u s t s may b e washed o f f b y
rain.
T h i s w a s h o f f may b e a m a j o r proc e s s of c y c l i n g o f t h e added e l e m e n t t o
soils.
Carlson et a l . ( 1 976) found t h a t
a s i m u l a t e d r a i n removed 45% o f a n
a p p l i e d a e r o s o l o f PbC12, and t h a t l i g h t
m i s t y r a i n i s most e f f e c t i v e . H e i c h e l &
Hankin ( 1 9 7 2 ) found t h a t t h e p a r t i c u l a t e s
i n which l e a d a d h e r e d t o t r e e s a v e r a g e d 7
micrometers i n diameter.
C h l o r i n e and
Bromine were t h e main a s s o c i a t e d n e g a t i v e
elements associated
with
them.
The
assessment o f t h e i n t e n s i t y o f i n p u t o f
c h r o n i c p o l l u t a n t s s u c h as t h e s e h a v e
b e e n made b y a n a l y z i n g c o n c e n t r a t i o n s o n
t r e e b a r k b y L o t s c h e r t ( l 9 7 7 ) , and Grodz i n s k a (1 9 7 7 ) .
Some o f t h e s e accumulat i o n s a r e washed down t h e t r e e t r u n k b y
s t e m f l o w and may b e a c c u m u l a t e d i n t h e
s o i l at t h e t r e e base.
POLLUTANT INPUT I N PRECIPITATION
Washout as w e l l as i n p u t o f e l e m e n t s
i n s o l u t i o n i n p r e c i p i t a t i o n is a major
path of input t o t h e elemental cycling
t h a t o c c u r s i n f o r e s t s . F o r example, t h e
n i t r o g e n c o n t e n t s t o r e d i n a 1000 y e a r
o l d redwood f o r e s t i s a b o u t t h e amount
c o n t r i b u t e d by r a i n f a l l d u r i n g t h a t t i m e
The geop e r i o d ( ~ i n k e ,5 g . , 1 9 7 9 ) .
c h e m i s t r y o f p r e c i p i t a t i o n w a s reviewed
t h o r o u g h l y b y C a r r o l l (1 9 6 2 ) .
She found
t h a t t h e c a t i o n s which b a l a n c e t h e i o n s
i n r a i n w a t e r were mostly b a s i c m e t a l l i c
elements
near
coast
lines
or
arid
regions, but t h a t along the storm v e c t o r
from t h e s e s o u r c e s a n d o v e r r e g i o n s w i t h
more v e g e t a t i o n , t h e r e would t e n d t o b e
a c i d i f i c a t i o n due t o l e s s d u s t o r o c e a n
aerosols t o provide t h e b a s i c m e t a l l i c
cations.
The c o n t r o l o f wind e r o s i o n
o v e r t h e G r e a t P l a i n s t h u s would t e n d t o
add t o t h e a c i d f i c a t i o n
of
rainfall
downwind from t h e a r e a .
However t h e
c u r r e n t e m p h a s i s o n p o l l u t i o n h a s added
the consideration of sources of anions i n
p r e c i p i t a t i o n t h a t come from b u r n i n g f o s sil fuels.
A s C a r r o l l (1962) mentioned,
a pH below 5.7 i n d i c a t e s t h a t h y d r o g e n i s
i o n i z i n g t o meet t h e n e c e s s a r y b a l a n c e
with anions.
The e f f e c t o f p r e c i p i t a t i o n i n p u t
upon n u t r i e n t e l e m e n t c y c l i n g i n a f o r e s t
w i l l t e n d t o b e s p e c i f i c t o t h e s i t e cond i t i o n s . T h i s would b e d e t e r m i n e d by t h e
following l o c a l factors:
1. background
n a t u r a l composition of t h e s o i l s o l u t i o n .
2. t h e c a t i o n exchange c a p a c i t y o f t h e
s o i l and t h e c o m p o s i t i o n o f c a t i o n s occup y i n g t h i s c a p a c i t y . 3. t h e volume o f
w a t e r e n t e r i n g as r a i n f a l l , 4. t h e a c i d
b a s e b a l a n c e o f t h e r a i n f a l l , 5. t h e
n a t u r e of t h e v e g e t a t i o n s p e c i e s w i t h
r e g a r d t o i n t e n s i t y of c y c l i n g b a s i c
m e t a l l i c e l e m e n t s , and perhaps o t h e r s
unique t o t h e s i t e . The e f f e c t s of i n p u t
i n p r e c i p i t a t i o n w i l l most obvious on
i n p r e c i p i t a t i o n w i l l b e most o b v i o u s on
s i t e s w i t h s o i l s h a v i n g low exchange
m a t t e r c o n t e n t s o i l s ) and w i t h s p a r s e
slow growing v e g e t a t i o n ( p i n e s , s p r u c e s ,
h e a t h l a n d ) , and i n c l i m a t e s w i t h l a r g e
amounts o f p r e c i p i t a t i o n .
FOREST ECOSYSTEM EFFECTS
The m i n e r a l c y c l i n g
in a forest
t a k e s p l a c e i n t h e c o n t e x t o f an ecosystem of p r o c e s s e s l i n k i n g t h e v a r i o u s l i v i n g organisms and t h e components o f t h e
environment.
Chronic a t m o s p h e r i c p o l l u t i o n i s one o f t h e s e components.
The
e l e m e n t s added w i l l be u t i l i z e d by t h e
Producers i n t h e f o r e s t .
These a r e t h e
organisms which c a r r y o u t t h e r e d u c t i o n
of
carbon t o c a r b o n compounds which
comprise t h e f o r e s t .
T h i s f i x e d carbon
t h e n s e r v e s as an energy s o u r c e f o r t h e
Decomposers i n t h e f o r e s t which a l s o have
requirements f o r t h e n u t r i e n t elements
e i t h e r i n t h e biomass o f t h e p r o d u c e r s o r
f u r n i s h e d d i r e c t l y by t h e s o i l .
Thus
p o l l u t a n t elements w i l l i n t e r a c t i n the
c y c l e between P r o d u c e r s and Decomposers,
w i t h s t o r a g e o f e l e m e n t s and p o s s i b l e
s i n k s o f u n a v a i l a b l e m a t e r i a l accumulating i n t h e s o i l portion of t h e cycle.
of Chronic P o l l u t i o n
Effects -
on
Producers
These
effects
can
range
from
enhancement o f p r o d u c t i v i t y t o a marked
d e c r e a s e depending upon whether t h e addi. t i v e
is a n e l e m e n t c u r r e n t l y l i m i t i n g
If toxic,
growth o r i s a t o x i c element.
t h e e f f e c t s w i l l show up i n f o l i a r dama g e , o r i n t e r f e r e n c e w i t h v a r i o u s physiol o g i c a l processes.
The syposium proceedi n g s e d i t e d by Naegele (1973) c o n t a i n s
many d e s c r i p t i o n s o f t h e s e t o x i c e f f e c t s .
Mc Cune i n t h i s p u b l i c a t i o n f e l t t h a t
such t o x i c e f f e c t s should be s p e c i f i c
with regard t o t h e Receptor ( l e a f , t r e e ,
f o r e s t ) , t h e P o l l u t a n t , t h e E v e n t , and
t h e Environment.
Acute e f f e c t s a r e r e l a t i v e l y e a s y t o d e t e r m i n e , as i n t h e d e a t h
o f l e a v e s n e a r a s m e l t e r r e l e a s i n g SO2.
Obviously t h i s would d e c r e a s e t h e r a t e o f
elemental cycling at the s i t e along with
a b r i e f s u r g e o f added m a t e r i a l s t o t h e
s o i l as t h e d e f o l i a t i o n t o o k p l a c e and
l e a v e s dropped t o t h e s o i l t o b e decomposed.
Whether t h i s is a l o s s t o t h e
s i t e depends upon t h e c a p a c i t y o f t h e
u n d e r l y i n g s o i l as d i s c u s s e d i n r e l a t i o n
t o d e f o l i a t i o n by h e r b i c i d e s by Zinke
(1974).
The e f f e c t s a r e more d i f f i c u l t
t o a s s e s s i n t h e c a s e o f c h r o n i c low
l e v e l p o l l u t i o n as d i s c u s s e d by 'Feder
(1 9 7 3 ) .
The changes i n p r o d u c t i v i t y
would need t o be s t a t i s t i c a l l y s i g n i f i c a n t b e f o r e and a f t e r t h e i n i t i a t i o n o f
t h e p o l l u t i o n . M i l l e r (1 973) h a s made an
approach t o i n d i c e s of l e v e l of c h r o n i c
p o l l u t i o n i n terms o f v i s u a l c h a r a c t e r i s t i c s on t h e t r e e s ; n e e d l e r e t e n t i o n , needle length,
needle chlorosis,
branch
d e a t h i n t h e c a s e of ponderosa p i n e .
F o l i a g e composition should i n d i c a t e such
i n p u t s , and a paper by Arkley and Glauser
i n t h i s symposium c o v e r s t h i s .
Also an
example i n t h e c a s e o f Big Cone Spruce
foliage
is
presented
in
table
1.
McBride, e t a l . (1975) made measurements
of a c t u a l g r o w t h r a t e r e t a r d a t i o n o f 26%
f o r h e i g h t and volume growth o f ponderosa
White
In a g r i c u l t u r a l plants,
found a d e c r e a s e i n C02 u p t a k e due
t o s y n e r g i s t i c e f f e c t s of NO + SO2 when
each were p r e s e n t a t l e v e f s n o t cons i d e r e d i n h i b i t i n g t o growth. S t i m u l a t i o n
of primary p r o d u c e r s by p o l l u t i o n i s n o t
o f t e n r e p o r t e d due t o t h e n e g a t i v e connot a t i o n of t h e t e r m . However, Schnappinger
(1975) found a n i n c r e a s e i n growth d u e t o
response t o z i n c contained i n f l y ash.
1974)
There a r e numerous v a r i a b l e s which
may a f f e c t t h e i n t e n s i t y w i t h which a
g i v e n l e v e l of p o l l u t a n t w i l l a f f e c t t h e
p r o d u c e r s i n an ecosystem.
Thus t h e
t r a p p i n g e f f i c i e n c y of t h e f o l i a g e s u r f a c e i s d i f f e r e n t f o r v a r i o u s s p e c i e s as
d i s c u s s e d by Zinke ( 1 9 6 6 ) , t h e v e l o c i t y
of t h e a i r p a s t t h e t r a p p i n g s u r f a c e as
h a s been e v a l u a t e d by Hori (1 953) and
Following t r a p p i n g t h e
S l i n n ( 1 976).
m a t e r i a l may n o t be absorbed by t h e s u r f a c e as found by Motto ( 1 9 7 0 ) . T h i s i s
partially attributable t o the particle
s i z e a c c o r d i n g t o Natusch & Wallace
( 1 9 7 4 ) . There may be s y n e r g i s t i c e f f e c t s
a t t h e f o l i a g e s u r f a c e . iiovelock (1974)
has alluded t o t h e possible c r e a t i o n of
PAN on f o l i a g e s u r f a c e by t h e combination
of 0 and hydrocarbons as o c c u r s on drying linen.
Once absorbed by t h e producer t h e
p o l l u t i n g element w i l l e n t e r t h e element a l c y c l e on t h e s i t e .
The d i s p o s i t i o n
from t h e p l a n t may be n o t o n l y t h r o u g h
l e a f d r o p , b u t may b e by d i r e c t r o o t exud a t i o n as Olson e t a1 (1 962) found w i t h
a d d i t i o n s of r a d i o a c t i v e Cesium added t o
a t r e e t r u n k . However upon b e i n g dropped
t o t h e s o i l as d e t r i t u s o r e n t e r i n g i n
o t h e r ways, t h e p o l l u t i n g e l e m e n t w i l l
t h e n b e a f f e c t i n g t h e decomposers i n t h e
forest.
Effects
nosers
of
-
Chronic P o l l u t i o n
on
Decom-
The e f f e c t s upon decomposers, t h e
s o i l m i c r o f l o r a and f a u n a t h a t complete
t h e e l e m e n t a l c y c l e s i n t h e s o i l , w i l l be
variable.
A s w i t h t h e p r o d u c e r s which
f i x carbon d i o x i d e , t h e a d d i t i v e s t o t h e
s i t e t h r o u g h a i r p o l l u t i o n may i n c r e a s e
or decrease
their
activities.
These
organisms r e q u i r e t h e same n u t r i e n t e l e ments as t h e p r o d u c e r s as w e l l as t h e
a d d i t i o n a l ones o f sodium, i o d i n e , and
vanadium f o r t h e s o i l f a u n a . If t h e poll u t a n t s a r e added i n t o x i c q u a n t i t i e s
t h e y would presumably r e t a r d t h e decompos i t i o n of o r g a n i c m a t t e r i n t h e s o i l and
t h u s slow o r b l o c k e l e m e n t a l c c l i n g .
They may b e s u b l e t h a l o r even mutagenic
t o t h e s e organisms a c c o r d i n g t o S t o t z k y
1974).
The d e t r i t u s o r l i t t e r l a y e r on t h e
f o r e s t f l o o r is t h e f i r s t major a r e a o f
a c t i v i t o f t h e decomposers.
Wittkamp &
Frank
969) found t h a t l i t t e r samples
impregnated w i t h i n t r o d u c e d e l e m e n t s such
as C o b a l t 60 and Cesium 137 had logarithmic r e l a t i o n s h i p with time i n the
f r a c t i o n r e m a i n i n g , and t h a t l o s s c o e f f i c i e n t s were d i f f e r e n t f o r d i f f e r e n t e l e ments.
These v a r i e d w i t h t h e s p e c i e s of
t r e e yielding the detritus.
The s t o r a g e
p e r i o d of t h e a d d i t i v e element depended
upon r e l a t i v e chemical m o b i l i t y of t h e
e l e m e n t , c o m p o s i t i o n of o t h e r e l e m e n t s
p r e s e n t , and t h e m o i s t u r e and t e m p e r a t u r e
conditions of the s i t e .
(1
If a p o l l u t a n t i s an element which
i s l i m i t i n g r a t e o f decompostion, t h e
e f f e c t on t h e decomposers may b e p o s i tive.
For example l e a f l i t t e r w i t h t o o
h i g h a ~ a r b o n / ~ i t r o g e nr a t i o ( n i t r o g e n
l i m i t i n g ) decomposes v e r y s l o w l y . Adding
n i t r o g e n as a c h r o n i c p o l l u t a n t would
a c c e l e r a t e t h i s decomposition and r e l e a s e
s t o r e d e l e m e n t s more r a p i d l y .
The s o i l f a u n a s e r v e a major t a s k i n
e l e m e n t a l c y c l i n g i n a f o r e s t ecosystem
by
physically
decomposing
organic
detritus,
reducing
it
in
size
and
i n c r e a s i n g s u r f a c e a r e a t o b r i n g about
f a s t e r r a t e s o f f u n g a l and b a c t e r i a l
decomposition.
Earthworms
of
various
s p e c i e s were found by Gish & C h r i s t e n s e n
( 1 9 7 3 ) t o accumulate t r a c e e l e m e n t s from
particulate
pollution
in
order
of
i n c r e a s i n g a t o m i c w e i g h t : N i < Zn < Cd <
Pb.
The s o i l f a u n a may s e r v e as a l i n k
f o r t r a n s f e r of n u t r i e n t e l e m e n t s t o
v a r i o u s p r e d a t o r s i n t h e f o r e s t ecosystem.
S t o t z k y ( 1 974)
characterizes the
s o i l as b o t h an a b i o t i c as w e l l as b i o t i c
s i n k f o r p o l l u t a n t s . E t h y l e n e and C O a r e
degraded by s o i l micro organisms.
Fungi
i n s o i l m e t a b o l i z e v o l a t i l e s from p l a n t
f o l i a g e s u c h as e t h a n e , b u t a n e , , e t c .
Thus s o i l by v i r t u e o f t h e v a r i o u s organi s m s present has a strong capability t o
detoxify pollutants.
A t low c o n c e n t r a t i o n s p o l l u t a n t s may b r i n g about an
enrichment o f t h e micro organisms which
can u t i l i z e them.
The u l t i m a t e r o l e o f t h e decomposers
i s t h u s t o c y c l e e l e m e n t s from t h e veget a t i o n t o the s o i l , usually oxidizing
them as e n e r g y s o u r c e s , and u l t i m a t e l y
r e l e a s i n g them t o t h e chemical and physic a l p r o c e s s e s of t h e s o i l o r renewed
uptake by t h e r o o t s of t h e p r o d u c e r s .
Chronic
Pollutants
into
Soil
The f i n a l f a t e of a d d i t i v e s t o t h e
ecosystem may b e t o remain i n t h e s o i l i n
i n s o l u b l e form.
Thus once p r o c e s s e d by
t h e decomposers t h e e l e m e n t s may become
m i n e r a l p r e c i p i t a t e s which may a c t as
s i n k s ( N a t . Res. Council 1 9 7 7 ) .
Thus
f l u o r i n e added t h r o u g h p o l l u t i o n may b e
precipitated i n the s o i l a s insoluble
CaF2. Page and Ganje (1970) showed t h a t
t h e t o p 2.5 cm. of s o i l w a s most a c t i v e
in trapping lead entering the soilv e g e t a t i o n system i n s o u t h e r n C a l i f o r n i a .
S o i l s sampled i n 1967 were compared w i t h
p r e v i o u s samples o b t a i n e d i n 191 9.
An
average increase
of
15-36
ppm
lead
accounted f o r 1 / 5 of t h e l e a d c o n t a i n e d
i n t h e 47 b i l l i o n g a l l o n s of g a s o l i n e
which had been burned d u r i n g t h e p e r i o d
encompassed.
Keaton ( 1937) added l a r g e
amounts of l e a d n i t r a t e t o s o i l (2784
ppm) and found t h a t v e r y l i t t l e ( 1 7 ppm)
remained i n s o l u b l e form.
Lee & T a l l i s
( 1 9 7 3 ) found i t p o s s i b l e t o d a t e p e r i o d s
of l e a d p o l l u t i o n i n a p e a t bog i n G r e a t
B r i t a i n , f i n d i n g a peak i n 5 0 0 A.D. w i t h
t h e o p e r a t i o n of Roman l e a d m i n e s , and a
subsequent
industrial
peak
beginning
Similar b u t recent hisabout 1 460 AD.
t o r i c a l evidence of l e a d c o l l e c t i o n i n
ecosystem s i n k s w a s found i n wood c o n t e n t
o f l e a d d a t e d by a n n u a l r i n g s by Sheppard
& Funk ( 1 9 7 5 ) .
Soil
organic
matter
generally
enhances t h e r o l e of s o i l as a s i n k f o r
added t r a c e e l e m e n t s .
P u r r e t a1 ( 1 9 7 1 )
have noted t h a t pH w i l l d e t e r m i n e whether
s o i l is a source o r sink.
Thus, a t neut r a l t o s l i g h t l y a l k a l i n e pH; A s , B, C d ,
Go, Cu, F, Fe, Pb, Mn, N i , Sn, and Zn
w i l l t e n d t o b e immobilized, b u t Ca, Cr,
K Mg, Mo, Rb, Se, and S r may become more
available t o plants.
Thus a n y t h i n g causi n g a change i n s o i l pH may r e l e a s e prev i o u s p o l l u t a n t s t h a t had t e m p o r a r i l y
become t r a p p e d i n t h e s o i l as a s i n k .
Various p r e c i p i t a t e s such as s o i l c a r b o n a t e s may form, a l s o depending upon pH.
The s o i l i o n exchange c a p a c i t y w i l l
r e t a i n e l e m e n t s i n a form r e a d y t o b e
Table 1: Big cone s p r u c e f o l i a g e a n a l y s e s
chronic pollution i n t e n s i t y .
across
gradients
WESTERN SAN GABRIEL MTNS. Angeles N a t i o n a l F o r e s t
Location
Weldon Canyon
Woodwardia Canyon
NITROGEN
1.80
percent
rank
93
PHOSPHORUS
PPm
rank
of
decreasing
Cloudburst Can yon
T i e Canyon Summit
Snowcrest Camp
Big P i n e s
601
7
N /P
ratio
rank
20.2
92
EASTERN SAN GABRIEL MTNS. Angeles N a t i o n a l F o r e s t
Location
Lower San Antonio
Camp Baldy
NITROGEN
pet.
rank
PHOSPHORUS
Ppm
rank
1093
25
N /P ratio
rank
-
Cleveland N.F.
SAN BERNARDINO-SAN JACINTO MTNS. San Bernardino N.F.
Location
Lower Waterman
Upper Waterman
Crestline
Camp Angeles
(young)
(old)
(young)
(old)
NITROGEN
2.12
1.80
2.02
2.04
1.22
.99
pot.
rank
97
92
96
96
52
13
PHOSPHORUS
PPm
rank
N /P
ratio
rank
CHRONIC
POLLUTION
INTENSITY
6 48
838
7
1
32.7
99
21.4
94
HEAVIEST
1016
18
.
1685
81
19.8
92
12.2
70
HEAVY
1658
79
7.3
36
1552
70
6.4
26
MODERATE-LIGHT
Keene
1.06
26
1544
69
Palomar
1.13
38
1580
72
6.8
31
7.1
34
LOW
NIL
T a b l e 2: S i m u l a t i o n of a c i d r a i n f a l l a d d i t i o n by l e a c h i n g a s u r f a c e s o i l developed under t h e i n f l u e n c e of a mature pond e r o s a p i n e a t t h e a r i d l i m i t o f t h e o c c u r r e n c e of t h e
species.
( i n m i l l i e q u i v a l e n t s p e r 100 m s . f i n e e a r t h p o r t i o n exc e p t l a s t column as i n d i c a t e d )
S o i l Treatment
Exchangeable C a t i o n s
Remaining on S o i l
Exchange
Capacity
%
Leached s o i l s :
L e a c h a t e Composition-3 I
500 m l H20
+5.71 meq. H+
+11 . 4 0 meq. H+
+17.09 meq. H+
+22.9 meq. H+
1
'
F i n e e a r t h p o r t i o n , 0-2.5
i n c h sampling h o r i z o n .
D i f f e r e n c e between t h e sum ( ~ a "
Exchange C a p a c i t y .
^-IThe 'H
+
M~++
w a s added as 0.1N H C 1 t o the.500
s i n c e 1 m l of 0.1N H C 1 = 0.1 meq. H
.
r e c y c l e d back t o t h e l i v i n g organisms on
t h e s i t e , and a l s o k e e p them from l e a c h i n g away from t h e s i t e .
Depending upon
t h i s c a p a c i t y , e l e m e n t s added t h r o u g h
c h r o n i c p o l l u t i o n may b e r e t a i n e d i n t h e
e l e m e n t a l c y c l e o f a f o r e s t provided t h e y
a r e not trapped i n a s i n k o r leached
away.
FOLIAGE ANALYSES I N D I C A T I N G
FOLLrnION
The e f f e c t o f c h r o n i c a i r p o l l u t i o n
o f t h e t y p e t y p i c a l of t h e Los Angeles
San B e r n a r d i n o b a s i n on f o l i a r a n a l y s e s
Cone Spruce ( P s e u d o t s u g a
of
the
macrocarpaBi. Vasey) Mayr) w a s d e t e r m i n e d .
Samples o f t h e f o l i a g e were g a t h e r e d
t h r o u g h o u t t h e r a n g e o f t h e s p e c i e s , and
a l s o on g r a d i e n t s o f e l e v a t i o n o r d i s t a n c e from t h e a r e a s t y p i f i e d by "smog"
t o a r e a s r e l a t i v e l y f r e e o f "smog". Anal y s e s were made o f 9 major e l e m e n t s i n
t h e v a r i o u s a g e c l a s s e s of t h e f o l i a g e .
The e l e m e n t s most o b v i o u s l y r e l a t e d t o
t h e i n t e n s i t y o f t h e smog and t h e i r rating i n a cumulative probability d i s t r i b u -
-
+
K'
+
~a')
and
the
m l of d i s t i l l e d w a t e r ,
t i o n from l o w e s t
shown i n t a b l e 1.
to
highest
value
are
N i t r o g e n c o n t e n t of t h e f o l i a g e and
t h e r a t i o of n i t r o g e n t o phosphorus cont e n t were t h e most obvious i n d i c a t o r s o f
t h e e f f e c t of chronic air p o l l u t i o n o f
t h e Los Angeles t y p e .
Where t h e r e w a s
a m b i g u i t y i n t h e n i t r o g e n v a l u e s as i n
San Antonio Canyon, t h e n i t r o g e n t o phosphorus r a t i o was t h e b e s t i n d i c a t o r i n
t h i s species.
SIMULATED A C I D RAINFALL LEACHING
A l a b o r a t o r y experiment w a s conducted i n which samples o f a n e a r l y
c a t i o n s a t u r a t e d s o i l under t h e i n f l u e n c e
of ponderosa p i n e were l e a c h e d w i t h s o l u t i o n s c o n t a i n i n g s u c c e s s i v e i n c r e m e n t s of
H The s o i l samples were o b t a i n e d a t t h e
lower r a i n f a l l l i m i t o f ponderosa p i n e
where t h e s o i l was most l i k e l y t o b e
base saturated.
F i v e s e p e r a t e t e n gram
samples of t h i s s o i l were l e a c h e d by
s o l u t i o n s which were r e s p e c t i v e l y 500 m l
of d i s t i l l e d w a t e r , and s o l u t i o n s t o
w h i c h i n c r e m e n t s o f 'H as H C 1 e q u i v a l e n t
t o 20$, 40$, 808, of t h e exchange capac i t y o f t h e sample were added.
The
r e s u l t s p r e s e n t e d i n t a b l e 2 show t h e
l e a c h i n g of t h e exchange complex of s o i l s
t h a t t a k e s p l a c e w i t h added i n c r e m e n t s o f
a cation.
Presumably t h e a d d i t i o n s o f
i n c r e m e n t s of H i n a c i d r a i n f a l l would
have similar e f f e c t s which would have t o
be considered i n t h e context of other
c a t i o n s b e i n g c y c l e d by t h e f o r e s t , and
by t h e c o m p o s i t i o n o f c a t i o n s a l r e a d y on
t h e exchange complex of t h e s o i l . Followi n g t h i s l e a c h i n g , each s o i l p o r t i o n w a s
analyzed
for
remaining
exchangeable
metallic cations.
These d a t a show t h a t g i v e n t h e s t o chiometry o f t h e l e a c h i n g of c a t i o n s from
the
t h e s o i l exchange complex by H
e f f e c t s of increments of acid r a i n f a l l t o
a g i v e n s o i l may b e s i m u l a t e d w i t h s o l u t i o n s having compositions s i m i l a r t o t h a t
of t h e r a i n f a l l .
Also, as t h e increment
of H
i n the precipitation increased,
e i t h e r b e c a u s e o f c o n c e n t r a t i o n o r of
volume o f r a i n f a l l l e a c h i n g t h e s o i l
would t e n d t o become hydrogen s a t u r a t e d ,
d i s p l a c i n g b a s i c m e t a l l i c c a t i o n s i n proportion.
In the f o r e s t s i t u a t i o n these
would be l e a c h e d o u t o f t h e s o i l p r o f i l e
i n a b a s e s a t u r a t e d s o i l , o r t a k e n up by
the vegetation.
CONCLUSIONS
T h i s r e v i e w of t h e l i t e r a t u r e and
t h e p r e s e n t a t i o n o f some o r i g i n a l work i s
applicable t o the e f f e c t of chronic a i r
p o l l u t i o n on m i n e r a l element c y c l i n g of
forests.
The l i t e r a t u r e i s g e n e r a l ,
i l l u s t r a t i n g processes, but i s not s i t e
s p e c i f i c except f o r t h e l o c a t i o n of t h e
studies.
S i n c e e f f e c t s a t any s p e c i f i c
s i t e may b e i n small i n c r e m e n t s each
y e a r , but severe i n cumulative e f f e c t s
o v e r a number o f y e a r s , a major remaining
problem i s t o f i n d ways o f d e t e r m i n i n g
s i t e s p e c i f i c indications of detrimental
e f f e c t s of s u c h c h r o n i c p o l l u t i o n .
Some
p e r t i n e n t c o n c l u s i o n s from t h e l i t e r a t u r e
reviewed i n t h i s paper a r e :
t i o n r e a c t i o n wherein CO i s reduced t o
o r g a n i c compounds by Producers i n t h e
ecosystem, and s u b s e q u e n t l y o x i d i z e d i n
energy r e l e a s i n g s t e p s by t h e s e p l a n t s o r
by t h e Decomposers i n t h a t ecosystem.
4. The c y c l i n g of e l e m e n t s t a k e s p l a c e i n
t h e c o n t e x t o f t h e s e redox r e a c t i o n s , and
t h o s e e l e m e n t s which change s t a t e w i t h
redox p o t e n t i a l change a r e u s u a l l y i n t h e
reduced form i n t h e producer v e g e t a t i o n
and
subsequently
oxidized
in
energy
r e l e a s i n g s t e p s by t h e s e p l a n t s o r by t h e
decomposers on t h e s i t e .
5. Chronic a i r p o l l u t i o n a d d i t i v e s t o t h e
f o r e s t a f f e c t t h e c y c l i n g of e l e m e n t s n o t
o n l y by d i r e c t a d d i t i o n s of t h e p o l l u t i n g
e l e m e n t s t o t h e c y c l e s , b u t a l s o by
a f f e c t i n g t h e redox s t a t u s o f t h e absorbi n g p l a n t t i s s u e , and o t h e r p o r t i o n s o f
t h e s o i l - v e g e t a t i o n system.
6 . C o n c e n t r a t i o n p o i n t s and s i n k s f o r t h e
e l e m e n t s added i n c h r o n i c p o l l u t i o n e x i s t
i n t h e various p a r t s of t h e vegetation,
t h e s u r f a c e d e t r i t u s on t h e s o i l , and i n
t h e s o i l c a p a c i t i e s f o r a b s o r p t i o n on i o n
exchange; hydrous o x i d e complexes, and as
insoluble precipitates.
7. The e f f e c t s o f c h r o n i c p o l l u t a n t s
added t o a g i v e n f o r e s t and i t s e l e m e n t a l
c y c l i n g p r o c e s s e s w i l l be h i g h l y s i t e
s p e c i f i c ; depending upon c l i m a t e , d e g r e e
o f w e a t h e r i n g development of t h e s o i l ,
t h e t y p e of m i n e r a l s from which t h e s o i l
i s forming, t h e c h a r a c t e r i s t i c s o f t h e
f o r e s t s p e c i e s and t h e i r s t o c k i n g densities,
t h e topographic
s i t u a t i o n with
r e g a r d t o a i r f l o w , and t h e n a t u r e o f t h e
pollutant.
8.
Local s i t e s p e c i f i c i n d i c a t o r s o f
i n t e n s i t y of p o l l u t i o n e f f e c t may be
v i s u a l as i n appearance and s i z e o f f o l i age, f o l i a r analyses f o r p o l l u t a n t elements and t h e i r r a t i o s t o background s i t e
e l e m e n t s , and s o i l assessment o f c a p a c i t i e s t o a b s o r b t h e added elements.
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adds
elements
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S t e f a n Bialobok
2
A b s t r a c t : The breeding of t r e e s , p a r t i c u l a r l y c o n i f e r s ,
f o r c u l t i v a t i o n in r e g i o n s under t h e i n f l u e n c e of i n d u s t r y
i s of c o n s i d e r a b l e economic importance. The r o l e of g e n e t i c
polymorphism in t h e p r o c e s s of a d a p t a t i o n t o such environments i s d i s c u s s e d . R e s u l t s a r e p r e s e n t e d of r e s e a r c h on
t h e g e n e t i c v a r i a b i l i t y in S c o t s p i n e p o p u l a t i o n s growing
under t h e i n f l u e n c e of i n d u s t r y and i n r e g i o n s f r e e of
gaseous p o l l u t i o n . Methods of s e l e c t i n g t r e e p o p u l a t i o n s
t o l e r a n t t o i n d u s t r i a l emissions a r e discussed aimed a t
t h e i d e n t i f i c a t i o n of g e n e t i c markers of t o l e r a n c e .
I n o r d e r t o reduce l o s s e s in f o r e s t ecosystems
caused by i n d u s t r i a l emissions a t t e m p t s were made
t o determine t h e s e n s i t i v i t y of trees (depending
on t h e i r g e n e t i c p r o p e r t i e s ) t o a c u t e i n j u r y of
t h e a s s i m i l a t i o n a p p a r a t u s by t h e most common
gaseous p o l l u t a n t s . The degree of p l a n t i n j u r y
by g a s e s i s dependent a l s o on t h e system of
e c o l o g i c a l f a c t o r s o p e r a t i n g in t h e environment.
GENETIC VARIATION OF TOLERANCE BETWEEN AND WITHI N SPECIES
So f a r a wide s c a l e of g e n e t i c v a r i a b i l i t y was
observed w i t h i n v a r i o u s s p e c i e s of t r e e s and
shrubs i n t h e i r s e n s i t i v i t y t o airborne pollution.
The r e s u l t s l i s t e d i n reviews (Davis e t a l . , 1976,
Bialobok 1979) a r e only approximate. It appears
t h a t most t o l e r a n t a r e some s p e c i e s of broadleaf
trees. Coniferous t r e e s which a r e of g r e a t e r
economic importance a r e g e n e r a l l y c h a r a c t e r i s e d
by low t o l e r a n c e .
It was a l s o found t h a t t h e r e is g e n e t i c
v a r i a b i l i t y in response t o SO^, O3 and HF
w i t h i n one p o p u l a t i o n of Pinus s y l v e s t r i s ,
P. s t r o b u s , P. ponderosa and w i t h i n P i c e a a b i e s
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, June 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.
2 ~ r e eB i o l o g i s t , I n s t i t u t e of Dendrology, P o l i s h
Academy of S c i e n c e s , 63-120 Kornik, Poland.
a s w e l l a s i n some s p e c i e s of broadleaf trees
(Gerhold e t al,., 1977). The g r e a t e r t o l e r a n c e of
S c o t s p i n e and Norway spruce t o t h e a i r p o l l u t i o n
w i t h i n a population i s sometimes a s s o c i a t e d w i t h
t h e g r e a t e r r e s i s t a n c e t o low temperatures d i s e a s e s
a i d a xerothermic a d a p t a t i o n (Bialobok, 1979). A
suggestion a l s o e x i s t s t h a t t h e cause of t o l e r ance t o some gases may depend on mechanisms t h a t
reduce t h e a c c e s s of g a s e s t o t h e p l a n t organism
(Gerhold e t a l . , 1977).
However, i t h a s been experimentally e s t a b l i s h e d
o r deduced from r e l i a b l e evidence t h a t t h e r e
e x i s t g e n e t i c mechanisms c o n d i t i o n i n g h i g h e r
t o l e r a n c e t o i n d u s t r i a l emissions (Niemtur, 1979).
The l a t t e r i n v e s t i g a t o r s t u d i e d 58 progenies of
S c o t s p i n e from 4 provenances o b t a i n e d from s e e d s
c o l l e c t e d on remnant l i v i n g t r e e s in t h e h i g h l y
p o l l u t e d c o n d i t i o n s of t h e Upper S i l e s i a n indust r i a l region. He h a s shown t h a t t h e s e p r o g e n i e s
have a g r e a t e r t o l e r a n c e than t h o s e c o l l e c t e d
from t r e e s growing beyond t h e range of p o l l u t i o n .
POLYMORPHISM AND ITS ROLE
S t u d i e s on t h e g e n e t i c v a r i a b i l i t y of enzymes
in f o r e s t t r e e s developed s t r o n g l y a f t e r S t e m ,
(1974) p o i n t e d o u t t h e g r e a t importance of gene t i c polymorphism f o r t h e development of ecologi c a l g e n e t i c s , f o r e s t g e n e t i c s and t r e e breeding.
Thanks t o t h i s method i t i s p o s s i b l e t o
recognize t h a t g e n e t i c s t r u c t u r e of a p o p u l a t i o n
( a l l e l e f r e q u e n c i e s and degree of h e t e r o z y g o s i t y )
in space and time, t o conduct s t u d i e s on i n h e r i t ance and l i n k a g e , t o determine t h e g e n e t i c d i s t a n c e
between i n d i v i d u a l s and p o p u l a t i o n s , t o i d e n t i f y
mechanisms of a d a p t a t i o n t o an environment and
t o employ i t in p r a c t i c a l f o r e s t r y .
Polymorphism of f o r e s t trees which a r e longl i v i n g organisms r e p r e s e n t s a d a p t i v e s t r a t e g i e s
of p o p u l a t i o n s t o a changing environment ( S t e r n
e t a l . , 1974). I n t h i s g e n e t i c system heterozygotes a r e f a v o r e d and t h u s t h e population is
capable of e x i s t i n g i n a h e t e r o g e n i c environment
s u r v i v i n g numerous and major changes.
Tree p o p u l a t i o n s in i n d u s t r i a l r e g i o n s grow
,
under s i m i l a r c o n d i t i o n s a s t h e herbaceous
p l a n t s t h a t c o l o n i z e m i n e s p i l l s having h i g h
c o n c e n t r a t i o n s of heavy elements (Pb, Zn, Cu).
This phenomenon S t e m (1974) a l s o c o n s i d e r s a s
being a good example of t h e developing polymorphism.
I n c o n d i t i o n s where a t l e a s t a p a r t of t h e
t r e e s can s u r v i v e i n an i n d u s t r i a l environment
t h a t has n o t been t o o s t r o n g l y p o l l u t e d , t h e
p o p u l a t i o n a d o p t s t h e optimal s t r a t e g y i n react i o n t o t h e changes t a k i n g p l a c e . This, of
c o u r s e , i s t h e r e s u l t of t h e e v o l u t i o n a r y
a d a p t a t i o n p r o c e s s t o t h e new environmental
c o n d i t i o n s where t h e g e n e t i c system i s under a
c o n s t a n t s e l e c t i o n p r e s s u r e . T o l e r a n t genot y p e s appear t o have a c e r t a i n l e v e l of f i t n e s s
t o t h e i n d u s t r i a l environment. What i s most
important t o us i s t h a t t h e d r a s t i c changes in
t h e i n d u s t r i a l environment should n o t exceed
t h e l e v e l of g e n e t i c f l e x i b i l i t y of t h e populat i o n s of t h e most important f o r e s t forming
s p e c i e s . I n t h e acute" c o n d i t i o n s of change i n
an i n d u s t r i a l environment, t h e coded g e n e t i c
system w i t h i n a p o p u l a t i o n , t h a t c o n d i t i o n s i t s
adaptive capacity, gradually ceases t o operate
s i n c e t h e p o t e n t i a l of i n d i v i d u a l genotypes f o r
a d a p t a t i o n h a s been surpassed.
GENETIC VARIABILITY OF ENZYMES I N SCOTS PINE
POPULATIONS
The u s e of e l e c t r o p h o r e t i c a n a l y s i s of
enzymes f o r t h e i d e n t i f i c a t i o n of v a r i a b i l i t y
determining g e n e t i c t o l e r a n c e t o i n d u s t r i a l
p o l l u t i o n i s s o f a r o n l y i n an i n t r o d u c t o r y phase.
The r e s u l t s o b t a i n e d s o f a r a r e encouraging.
The s t u d i e s conducted on S c o t s p i n e a r e t r e a t e d
o n l y a s a model.
Mejnartowicz (1978) h a s s t u d i e d t h e v a r i a b i l i t y of izozymes of leucyloaminopeptidase (LAP)
and a c i d phosphotase (APH) in 19 p o p u l a t i o n s of
S c o t s p i n e from t h e whole range of t h e s p e c i e s
in E u r a s i a .
The Poland p o p u l a t i o n s were chosen
fromregions under i n d u s t r i a l i n f l u e n c e and from
r e g i o n s beyond p o l l u t i o n . I n a l l t h e p o p u l a t i o n s
APH was coded in l o c u s B w i t h 1 5 a l l e l e s , and
t h e r e was c o n s i d e r a b l e polymorphism in t h e
s t u d i e d p o p u l a t i o n s , and LAP was coded in 2
l o c i , LAP-A having 5 a l l e l e s and LAP-B 6
alleles.
It i s i n t e r e s t i n g t h a t t h e population of S c o t s
p i n e from Babki ( c e n t r a l Poland--strong indust r i a l p o l l u t i o n ) h a s had t h e lowest degree of
h e t e r o z y g o s i t y on l o c u s LAP-A, ha0.1124 and t h e
h i g h e s t v a l u e i n LAP-B, h=0.3970. Among i n d i v i d u a l s s e n s i t i v e t o SO2 t h e genotype APH-B4/B6
dominated and among i n d i v i d u a l s t o l e r a n t t o t h i s
gas t h e a l l e l e APH-B5 appeared commonly
(Mejnartowicz, 1977-78).
Szmidt (1978) when
studying t h e g e n e t i c polymorphism of c a t a l a s e i n
t h r e e p o p u l a t i o n s of S c o t s p i n e from i n d u s t r i a l
r e g i o n s and 5 p o p u l a t i o n s from r e g i o n s f r e e of
p o l l u t i o n , h a s found 7 phenotypes of t h e
c a t a l a s e . When comparing t h e p o p u l a t i o n s on t h e
b a s i s of h e t e r o z y g o s i t y he has shown t h a t populat i o n s from r e g i o n s f r e e of p o l l u t i o n were charact e r i z e d by g r e a t e r p a r t i c i p a t i o n of homomorphic
compared t o
i n d i v i d u a l s of t h e type C-l/C-1
p o p u l a t i o n s under t h e i n f l u e n c e of emissions.
Mejnartowicz, e t a l . , (1978) having taken
m a t e r i a l from p l u s t r e e s in a S c o t s p i n e seed
orchard e s t a b l i s h e d a l a c k of c o r r e l a t i o n between
t h e degree of h e t e r o z y g o s i t y of t r e e s i n LAP
l o c i and t h e degree of t h e i r s e n s i t i v i t y t o t h e
a c t i o n of SO2 in a l a b o r a t o r y t e s t .
These i n t r o d u c t o r y r e s u l t s i n d i c a t e t h a t t h e r e
i s d i f f e r e n t i a t i o n in t h e frequency of some
a l l e l e s in a p o p u l a t i o n depending on t h e i n c l u ence of i n d u s t r i a l emissions. The important
t h i n g i s t h a t an enzymatic marker b e found f o r
t o l e r a n c e which would b e independent of environmental i n Âl u e n c e s
.
INHERITANCE OF TOLERANCE TO INDUSTRIAL EMISSIONS
Not many i n v e s t i g a t o r s have attempted determini n g in g e n e r a t i v e progeny t h e combining a b i l i t y ,
h e r i t a b i l i t y and r e p e a t a b i l i t y of t o l e r a n c e t o
i n d u s t r i a l emissions. I n t h e c a s e of S c o t s p i n e
h e r i t a b i l i t y and r e p e a t a b i l i t y of t o l e r a n c e t o
Oq i s t o be found under a low o r medium g e n e t i c
c o n t r o l . However, some provenances have a h i g h e r
h e r i t a b i l i t y of t o l e r a n c e t o 03. Needle i n j u r y
in t h e s e p i n e s 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
t h e i n j u r i e s caused by SO2 (Gerhold e t a l . , 1977,
Demeritt, 1977). Bialobok e t a l . , (1978) have
a l s o found a s i g n i f i c a n t c o r r e l a t i o n between t h e
degree of n e e d l e i n j u r y on mother t r e e s and on
t h e i r progenies following treatment w i t h SO?.
However, t h e s e c o r r e l a t i o n s were n o t found followi n g treatment w i t h 03 o r a mixture of 03 and SO2.
The s e l e c t i o n of t r e e i n d i v i d u a l s t o l e r a n t t o
i n d u s t r i a l emissions i s being done by t h e r e l a t i v e l y simple methods of mass s e l e c t i o n , without
understanding t h e g e n e t i c b a s i s f o r t h e populat i o n s t r u c t u r e . T h i s s e l e c t i o n i s u s u a l l y being
conducted on s e e d l i n g s in l a b o r a t o r y c o n d i t i o n s .
Sometimes p o s i t i v e r e s u l t s were o b t a i n e d f o r t h e
p r a c t i c e which w i t h some p r o b a b i l i t y a r e being
u t i l i z e d in e s t a b l i s h i n g tree p l a n t a t i o n s o r
producing t r e e s f o r ornamental purposes
(Demeritt, 1977).
So f a r i t was n o t p o s s i b l e t o s o l v e t h e probl e m of breeding v a r i o u s p i n e s p e c i e s f o r c u l t i v a t i o n in f o r e s t s under t h e i n f l u e n c e of i n d u s t r i a l
emissions, and t h e r e i s no cheap way of propagat i o n of s e l e c t e d i n d i v i d u a l s .
Gerhold, (1977) h a s d i s c u s s e d s e v e r a l methods
of breeding trees more t o l e r a n t t o i n d u s t r i a l
e m i s s i o n s , i n which t h e u s e of s e e d s o r c h a r d s
e s t a b l i s h e d from t o l e r a n t c l o n e s i s envisaged.
It appears, however, t h a t i t would be v a l u a b l e
t o expand t h e i n v e s t i g a t i o n s of g e n e t i c v a r i a b i l i t y of enzymes in p o p u l a t i o n s of c o n i f e r o u s
trees endangered by i n d u s t r i a l p o l l u t i o n . W e
have c o n s i d e r a b l e information a l r e a d y on t h e
c o u r s e of m e t a b o l i c c y c l e s in t h e tree organism
exposed t o t h e a c t i o n of some gases. I b e l i e v e
t h e s e two s o u r c e s of information could be
combined, (biochemical g e n e t i c s and metabolic
changes) in o r d e r t o i d e n t i f y t h e enzymatic
g e n e t i c marker t h a t would be u s e f u l i n t h e
s e l e c t i o n of t o l e r a n t populations.
LITERATURE CITED
Bialobok, S t e f a n .
1979. I d e n t i f i c a t i o n of r e s i s t a n t o r t o l e r a n t
s t r a i n s and a r t i f i c i a l s e l e c t i o n o r product i o n of such s t r a i n s in o r d e r t o p r o j e c t
v e g e t a t i o n from a i r p o l l u t i o n .
Symp. on t h e
e f f e c t s of a i r b o r n e p o l l u t i o n on v e g e t a t i o n ,
Warsaw (Poland) 20-24 Aug. 1-16, 1979.
Demeritt, Maurice E. JK.
1977. Genetic Evaluation of Two-Year Height
and Ozone Tolerance in Scotch P i n e (Pinus
s y l v e s t r i s L.)
A Thesis i n Genetics.
The
Pennsylvania S t a t e U n i v e r s i t y .
.
Davis, Donald D. and Raymond G. Wilhour.
1976. S u s c e p t i b i l i t y of woody p l a n t s t o s u l f u r d i o x i d e and photochemical o x i d a n t s . EPA600/3-76-102. p. 72. U. S. Environmental
P r o t e c t i o n Agency, C o r v a l l i s , Oregon 97330.
Gerhold, Henry G., and Raymond G. Wilhour.
1977. E f f e c t of a i r p o l l u t i o n on Pinus
s t r o b u s L. and g e n e t i c r e s i s t a n c e . A L i t e r a t u r e Review. EPA-600/3-77-002
p. 45 Environmental P r o t e c t i o n Agency, C o r v a l l i s , Oregon,
97330.
Mejnartowicz , Leon.
1977-1978.
Genetic c h a r a c t e r i s t i c of some
S c o t s p i n e t r e e s s u s c e p t i b l e or somewhat
r e s i s t a n t t o t h e a c t i o n of SO^. Annual
Report from P r o j e c t PL-Fs-74 from U. S.
Department of A g r i c u l t u r e under PL-480.
Mejnartowicz, Leon.
1978. S t r u k t u r a genetyczna p o p u l a c j i sosny
zwyczajnej z terenow przemyslowych zanieczyszczonych przez S02. I n Proc. from:
Reakcje b i o l o g i c z n e drzew na e m i s j e
przemyslowe. Kornik 4-5 maj 1978.
Mejnartowicz, L., S. Bialobok and P.
Karolewski.
1978. Genetic c h a r a c t e r i s t i c of S c o t s p i n e
specimens r e s i s t a n t and s u s c e p t i b l e t o SO2
a c t i o n . Arboretum K o m i c k i e . 23: 233-238.
Mejnartowicz , Leon.
1979. Genetic v a r i a t i o n i n some isoenzyme
l o c i i n S c o t s p i n e (Pinus s i l v e s t r i s L.)
population. Arboretum K o m i c k i e . 24: 91104.
Niemtur, Stanislaw.
1979. Badania nad wewnatrzgatunkowym
zroznicowaniem o d p o m o s c i sosny zwyc z a j n e j (Pinus s i l v e s t r i s L.) n a e m i s j e
przemyslowe. Doctoral T h e s i s , Uniwersytet
&ski,
Katowice.
S t e m , K. and P e t e r M. A. T i g e r s t e t .
1974. Okologische Genetic. 98-p. 75 p. G.
Fischer.
Stuttgart.
Szmidt, Alfred.
1978. Zmiennosc k a t a l a z y w populacjach
sosny zwyczajnej znajdujacych s i e pod
wplywem zanieczyszczen przemyslowych.
In
Proc. from: Reakcje b i o l o g i c z n e drzew n a
e m i s j e przemyslowe. Komik 4-5 maj 1978.
Interactions of Air Pollutants and Plant Michael
reshow^
Abstract: Each i n t e r a c t i o n between an a i r polluP o l l u t a n t s may m i t i t a n t and d i s e a s e is unique.
gate d i s e a s e response or i n t e n s i f y i t ; and t h e
presence of c e r t a i n d i s e a s e s can modify the p l a n t s
response t o a p o l l u t a n t .
Air p o l l u t a n t s can a c t
d i r e c t l y on a fungus or b a c t e r i a i n h i b i t i n g parasitism.
They may a l s o a c t most s t r o n g l y on the h o s t ,
modifying i t s physiology and rendering i t e i t h e r
more or l e s s s e n s i t i v e t o a p l a n t pathogen. Where
t h e p l a n t i s weakened by the p o l l u t a n t s , it tends
t o be more s e n s i t i v e t o weak pathogens, but l e s s
sensitive t o obligate parasites.
Where the pollut a n t p h y s i c a l l y i n j u r e s t h e host, i n f e c t i o n may be
facilitated.
P o l l u t a n t i n t e r a c t i o n s have been
demonstrated both i n the l a b o r a t o r y and t h e f i e l d
a t ambient p o l l u t a n t concentrations.
Interactions
between p o l l u t a n t s and a b i o t i c s t r e s s a r e p a r t i c u l a r l y c r i t i c a l . Water regime, temperature r e l a t i o n s , mineral n u t r i t i o n and other parameters of
t h e physical environment play a major r o l e i n the
expression of a i r p o l l u t i o n i n j u r y .
Air p o l l u t i o n can k i l l p l a n t s . Even when t h e
concentrations of an a i r p o l l u t a n t a r e not
d i r e c t l y l e t h a l , they may be harmful, adversely
a f f e c t i n g growth, reproduction and myriads of
o t h e r b i o l o g i c a l processes ( M i l l e r and McBride
1975). One such process i s t h e i n t e r a c t i o n t h a t
r e s u l t s between t h e p o l l u t a n t and p l a n t
pathogens.
There a r e many ways i n which such i n t e r a c t i o n s might take place.
But do they? The most
obvious would be i f the p o l l u t a n t d i r e c t l y
a f f e c t e d the fungus, v i r u s , b a c t e r i a ,
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.
2 ~ r o f e s s o rof Biology, University of Utah,
S a l t Lake C i t y , Utah 84112.
i n s e c t or o t h e r pathogen.
I f some s t a g e of an
organism's l i f e c y c l e , o r some s t a g e of p a r a s i t i s m , were adversely impaired by a p o l l u t a n t , t h e
p o l l u t a n t e s s e n t i a l l y would be a c t i n g a s a
fungicide, b a c t e r i o c i d e or o t h e r biocide and
could be expected t o bring about some degree of
control.
The second way an a i r p o l l u t a n t might a c t
would be i n adversely a f f e c t i n g the growth o r
reproduction of the host p l a n t and thereby
influencing i t s s u i t a b i l i t y a s a host. There
a r e two ways i n which such a c t i o n could be
brought about. Most apparently, the p o l l u t a n t
might cause some physical i n j u r y t o the p l a n t
leaving l e s i o n s t h a t could serve a s i n f e c t i o n
c o u r t s f o r a fungus or bacteria.
O r , the p l a n t
might simply be weakened, thus lowering i t s
r e s i s t a n c e t o a prospective pathogen.
Presumably the weaker pathogens, the f a c u l t a t i v e
p a r a s i t e s , would b e n e f i t most by such
conditions. Obligate parasites, on the other hand, preferring a vigorous host, might respond quite differently and their development might even be discouraged in the weakened host. Conversely, the impact of various diseases or plant stresses on the plant's response to air pollutants has also been considered. It should be quite apparent that adverse climatic or edaphic factors might affect a plant's sensi- tivity to a pollutant, but the presence of certain biotic diseases may also increase or decrease a plant's sensitivity. A major question is not so much do such interactions take place, but what concentrations of an air pollutant are required to precipitate such effects, and how widely do such concentra- tions occur? Many of the interactions that will be dis- cussed have been demonstrated under laboratory conditions, often at pollutant concentrations known to be fairly widespread. Some of the interactions have been observed in the field. The literature treating such air pollutant- plant pathogen interactions has been reviewed most recently in 1978 (Laurence), 1975 (Treshow), and 1973 (Heagle); it is not the intent of this paper to once again provide an exhaustive review of this literature. Rather, I should like to first bring the literature up to date, briefly including that delving into the interactions of abiotic stresses on pollutant effects, and discuss the implication and pos- sible practical relevance of such interactions, especially concerning forest ecosystems. Pri-
marily I should like to develop some of the principles in pollutant-pathogen interactions. INFLUENCE OF POLLUTANTS ON DISEASE EXPRESSION Sulfur Dioxide There is no question that sulfur dioxide interacts with fungi, suppressing their growth and acting fungicidally. The only question concerns the SO2 concentrations at which such interactions occur. A few examples exist where SO2 has acted in such a way in the field, limiting the develop- ment of certain plant diseases. The examples provided by Scheffer and Hedgcock (1955) in which parasitic fungi generally appeared to be retarded or inhibited near smelters where SO2 was present is most often cited (Treshow 1975).
Suppressed disease development was especially apparent where rust fungi, Melampsora and Puccinia, or needle cast fungi were involved. Linzon (1973) also discusses the reduced heart rot and blister rust (Cronartium ribicola) near a smelter. But such incidents are becoming more infre- quent as ground level SO2 concentrations become reduced by modern control technology or use of tall stacks. Higher SO2 concentrations, often exceeding 1 ppm for extended periods, now tend to be of only historic record. We are now interested in the possible impact of SO2 concen- trations in the 0.1 to 0.5 ppm range or even lower in cases of prolonged duration. Where such concentrations still exist near smelters, power plants, or large urban centers, some pollutant-pathogen interaction might be sought. There is some evidence from laboratory and <
field research that certain pathogenic fungi respond to SO2 in this concentration range. Weinstein and others (1975) for instance, have demonstrated that SO2 concentrations of 0.14 to 0.15 ppm, continuous for 7 days, while not visibly injuring plant foliage, affected the bean rust fungus, Uromyces. The incidence and severity of the rust as measured by the abun- dance of uredia was decreased as were both the size and percent germination of the uredo- spores. Hence the reproductive potential of the pathogen was reduced. The results suggested that the effect on the pathogen was indirect; perhaps involving an 802-induced chemical change in the resistance of the host and its suitabil- ity as a habitat for the fungus. The authors speculated that production of phytoalexins or supply of metabolites might have been altered, or compounds derived from SO2 might have accumu- lated. One of the most comprehensive field studies of the interactions of industrial air pollu- tants, especially SO2, with plant disease was conducted by A. Grzywacz and J. Wazny (1973). The study was notable since it dealt with eco- nomically significant diseases of a coniferous forest, specifically Scots pine (Pinus sylvestris L.).
Interactions with six fungi were considered: Armillaria mellea, Fomes annosus, Lophodermium pinastri, Microsphaera alphitoides, Melampsora pinitorqua, and Cronartium flaccidium. --
In an overall study, comparisons were made of disease presence in industrial areas and forests throughout Poland. In a more detailed approach, disease presence was compared at increasing distances from an industrial town, Torun, with one major SO2 source. The general comparisons showed that Armillaria was present in 3.7 percent of the trees in the area damaged by SO2 compared with only 1.38 percent in all forests. Lophodermium also tended to be more serious in the industrial areas, but the results were indefinite. This was consistent with earlier findings of Donabauer (1966) that high SO2 concentrations increased the intensity of Armillaria root rot. Fomes showed the reverse trend and occurred in 0.87 percent of the areas affected by indus- trial pollution compared with 1.5 percent in the country as a whole. Fomes, as in the overall study, was least prevalent in areas of highest SO2 concentrations. Grzywacz and Wazny (1973) found that stumps close to the SO2 source were sound. Related, decomposition fungi were also less abundant closest to the source. Only 50 percent of the stumps showed signs of decom- posing, and 10 percent strongly decomposing, compared with 30 percent strongly decomposing farther out. However, Gryzwacz (1978) later reported that stands influenced by air pollution were more subject to decomposition by brown, white or soft rot fungi. Sufficiently high SO2 concentrations might suppress the fungal growth directly. Such was the case where Mejstrik (1978) showed SO2 concentrations as low as 84 ug/m3 (.03 ppm) inhibited growth of Flamulina velopes, Nematoloma fasciculare, and Pleurotus ostreatus from 34 to 39 percent. Lophodermium injury was least significant near the SO2 source. At distances beyond 1 km injury appeared on up to 70 percent of the needles. There was a slight decrease beyond this. When annual SO2 concentrations averaged below 0.2 ppm, disease incidence was essentially the same as in the control group. Fungus devel- opment was noticeably affected. Within 1 km, reproduction was largely by pycnidia; further distant, apothecia were common. The numbers of needles with both the sexual and asexual stages increased with distances. Closest to the SO2 source, apothecia were only 15 percent the length of controls deformed, collapsed, under- developed, closed or even dried up and with ill- developed asci. Chiba and Tanaka (1968) however reported high SO2 concentrations of 2 ppm for 14 hours caused increased infection of injured pine needles (P. densiflora) by Rhizosphoera
kalkhoffii. Weidensaul and Darling (1979) inoculated Scots pine seedlings with the fungus Scirrhia acicola. The plants were inoculated either 5 days before or 30 minutes after fumigation for 6 hours with 533 ug/m3 (0.20 ppm) SO2).
After 8 weeks, the seedlings inoculated 5 days before fumigations had more lesions incited by the fungus than those inoculated 30 minutes after fumigations in the control group. It was postu- lated that since the needle blight fungus pene- trates through the stoma, the ability of the SO2 to keep the stoma open facilitated entry of the fungus. The pollutant-disease interaction may vary with the host species. Ham (1971) found that when loblolly pine served as the host, the brown spot fungus (5. acicola) was not measurably
affected by SO2 in the 0.5-0.9 ppm range for 2-3 hours even when SO2 caused visible injury. Simulated rain, acidified with sulfuric acid has also been shown to influence pollutant- pathogen interactions (Shriver 1974).
Although not involving forest species, the work did demonstrate the way in which plant species might be affected. Kidney beans (Phaseolus vulgaris var. red kidney) and willow oak (Quercus phellus) were exposed to simulated rain acidified to a pH of 6.0 or 3.2 for 10 minutes each day for 30 to 60 days. The acid "rain" caused an 86 percent inhibition in the number of telia produced by Cronartium fusiforme on willow oak, a 66 percent inhibition in the reproduction of the root knot nematode (Meloidogyne hapla) on beans in the field, and a 29 percent decrease in the percent of leaf area of field "erown beans
- - - affected by Uromyces phaseoli. Exposures to pH 3.2 "rain" completely destroyed the integrity
of the cuti- cular waxes in both oak and bean. Exposures to the pH 6.0 solution did not visibly alter the cutin. Shriver postulated that damage to the cutin facilitated leaching of carbohydrates from the leaf including those that might inhibit hyphal growth of Botrytis cinerea thus predis- posing plants to infection. -
--
- - -
This is consistent with the findings of F. A.
Last and 0. D. Fowler at the Institute of Terrestrial Ecology at Penicuik, Scotland (per- sonal communication) who showed that the cuticle of Scots pine was gradually broken down by low concentrations,of S02. Sulfur dioxide, perhaps largely as acid rain, may have an effect on soil microorganisms (Wainwright 1978).
Sulfur-oxidizing micro- organisms, including Alternaria tenuis, Auriobasidium pullulans and Cephalosporium sp., were isolated from leaves, litter and soils polluted with high levels of S02. The predomi- nant autotroph on leaf surfaces was Thiobacillin thioparis. Hibben and Taylor (1975) found that S02- pathogen interaction depended on the infection stage. Conidial gemination and the appres- sorial stages of Microsphaera =were
most sensitive to S02. Since infection was not reduced when leaves were previously fumigated, the effect was thought to be mostly fungicidal. Ozone There is considerable evidence that photo- chemical pollutants, most notably ozone, affect plant pathogens and fungus-host interactions. The interaction may be positive or negative depending on the 03 concentrations and the 03 sensitivity of the host. In one such study, Miller and Elderman (1977) showed that fumigation of ponderosa and Jeffrey pine seedlings with ozone enhanced infection by Fomes annosus. Average infection of the two species increased from 57 percent to 78 percent when the seedlings were exposed to 431.2 p g / ~ 3 (.25 ppm) ozone. They also found that ozone injury increased the susceptibility of pine stumps to colonization by Fomes annosus. In the laboratory, wood from trees slightly damaged by oxidants was more decay-susceptible than wood from severely damaged trees. flavonoids that are toxic to microorganisms. According to Laurence and Wood (1978), ozone inhibited infection of soybean by Pseudomonas glycinea presumably because of a bacteriostatic compound, possibly an isoflavinoid compound, produced in response to ozone. Fluoride Far more research has involved powdery mildew (Heagle and Strickland 1972, Heagle 1975, Scheutte 1971), and the negative impact of ozone on disease. Even ozone concentrations in the 5 to 50 pphn range reduced infection when conidia were exposed. According to Scheutte, appresoria formation was largely affected. Also, some epidermal cells, hypersensitive to ozone, were killed thereby reducing infection. Eight hour exposure to 50 pphm ozone reduced formation of secondary hyphae 66 percent and 4 hour exposure reduced 41 percent. Ozone impaired formation of the penetration peg thus inhibiting subsequent development of a functional host-parasite rela- tionship. While ozone impacted certain critical stages of infection under controlled conditions, in the field such effects would be less apparent since all stages of parasitism would be present simul- taneously. Interactions of facultative parasitic and saprophytic fungi with their hosts may also occur and are most pronounced when the plants are weakened or injured by ozone (Manning 1975).
Obligate parasitism appears to be retarded by ozone and ozone-injured host tissue. Colonization of ozone-injured white pine needles by Lophodermium pinastri was reduced while colonization by the saprophyte Aureobasidium pullulans was increased. Ozone-
injured lilac leaves were rarely infected by powdery mildew Micosphaera
a. When the fungus is especially sensitive to ozone the impact may be mostly fungicidal there- by reducing infection. Sporulation and germina- tion of the weak parasite Botrytis cinerea was significantly inhibited by 2, 6 hour ozone exposures at a concentration of 30 pphm (Krause and Weidensaul 1978).
There was also less infection, based on total lesion area, when plants were exposed to 15 pphm. Ozonation of conidia produced in vivo and in vitro decreased germination of conidia, germ tube length, and pathogenicity. The authors postulated that the mode of action was to alter the permeability of the conidia membrane. Ozone may increase the conidiophore respiration causing prematurely- formed and non-viable conidia. Ozone also may inhibit, directly or indirectly, enzyme activity of the fungus and cause less maceration of the host cells resulting in a decreased infection. Curtis and others (1976) found that plants exposed to ozone produced peroxidases and iso- Fluoride is accumulated in the foliage of plants and affects many metabolic processes. Consequently, it is reasonable to presume that pollutant-pathogen interactions can be influenced, perhaps to a greater extent than with any other pollutant. This was confirmed with viruses by some of the early work reviewed by Heagle (1973) and Treshow (1975). Host-fluoride interactions also have been demonstrated for fungi (McCune and others 1973) although not on forest species. Studying the interactions of 7 to 10
with 3 diseases of bean and 2 diseases of tomato, HF consist- ently reduced uredial formation as the foliar fluoride content increased. Tender green beans exposed to HF and inoculated with powdery mildew conidia developed fewer foliar lesions than non- fumigated control plants; 4.4 compared with 48.7 on fumigated leaves having an average of 399 ppm F. Powdery mildew was reduced proportionate to the length of the exposure period. Early blight lesions on tomato were similarly reduced by the presence of fluoride. INFLUENCE OF DISEASE ON POLLUTANT SEVERITY Not only may the presence of a pollutant influence pathogenicity, the reverse may be true~presenceof diseases influence the degree of pollutant injury. This has best been demon- strated with viruses. None of these involved forest species though, and there has been no new results published since last reviewed by Laurence (1978). Also, in the forest, variation in pollutant resistance among individual trees would far exceed any disease and pollutant interaction, and any impact of a disease on pollutant sever- ity probably wouldn't be measurable. ABIOTIC STRESS Severity of air pollution injury is deter- mined not only by the dose of the pollutant to which plants are exposed but on the predisposi- tion of the plant. Predisposition is determined by any environmental parameter to which the plant is subjected. It has been discussed more in passing than as a major concern (Heck and others 1965, Heck 1968, Treshow 1970, Taylor 1974), but the interactions of abiotic stress or disorders with any pollutant is far more significant than with biotic pathogens. Moisture stress, the light regime, edaphic factors and temperature relations all influence the sensitivity of plants to every pollutant. conditions allowed only slight to moderate foliar injury on tomato leaves, damage was enhanced by cadmium treatment especially at higher concentrations. Unusually high or low temperatures prior to exposure tend to reduce plant sensitivity to ozone, for instance. A normal high light inten- sity renders plants more sensitive. High humid- ity, by encouraging open stomates, also
increases sensitivity. In dry air, plants are more tolerant of ozone than at higher humidi- ties, and PAN injury is most severe in the Los Angeles area when the relative humidity exceeds 50 percent. Along the same line, low concentrations of SO2 affected metal uptake, increasing zinc and cadmium susceptibility of bean plants. Foliar injury caused by heavy metals was significantly enhanced by SO2 (Krause and Kaiser 1977). Any factor favoring moisture stress and reduced water uptake would cause stomatal clo- sure and favor resistance to pollutant uptake and injury. In this way, plants in more saline soils are more tolerant of certain pollutants (Oertli 1958) and there is little to no ozone or PAN injury when soil moisture is deficient. Ozone injury may be negligible when ambient air temperatures during and after exposure are below 90Â F., yet may be severe when tempera- tures exceed 90' F. (Taylor 1974). Effects of low atmospheric and soil moisture on tolerance or sensitivity of plants to SO2 injury are well known; suffice it to note that plants are far more sensitive under higher moisture conditions. Mineral nutrition also plays arole in pollu- tant sensitivity. Vegetable crops are known to be most susceptible to ozone when nitrogen nutrition is adequate although some reports suggest injury is greatest when nitrogen is low. Sulfur dioxide sensitivity is reported to be greatest with increased sulfur nutrition. Stomata1 behavior may be involved since a defic- iency of nitrogen, potassium or phosphor,us may decrease stomatal opening. Plants low in sulfur had the lowest stomatal capacity, thus less capacity for gas absorption (Leone and Brennan 1972). Toxicity from heavy metals also plays an interesting role with air pollutants. Ormrod (1977) has found that ozone toxicity was en- hanced on pea plants growing in elevated concen- trations of cadmium or nickel. However, when cadmium concentrations were sufficiently high to adversely affect growth,100 umol of CdS04, then ozone injury was less than that of control plants. Harkov and others (1979) found that the amount of ozone injury depended on the cadmium and ozone levels as well as other environmental conditions. Where environmental conditions were not conducive to ozone injury (e g. bright
sunlight), cadmium had little effect on the amount of leaf damage. When environmental .
Lamoreaux and Chaney (1978) also found sig- nificant interactions between cadmium and S02. While cadmium or SO2 alone reduced net photosyn- thesis and transpiration of excised silver maple leaves, the reduction in cadmium-treated leaves was greatest in the presence of S02. CONCLUSIONS Virtually every environmental parameter, biotic and abiotic can interact with air pollu- tants to aggravate or mitigate the extent of pollution damage. The significant question then becomes, to what extent and at what concentra- tions? Is the net impact real, and if so, how meaningful is it under field conditions? All pollutants don't interact the same. Sulfur dioxide, for instance, appears primarily to act fungicidally reducing disease and decom- position activity. It is also postulated though that SO2 induces chemical changes imparting resistance to certain pathogens. Ozone tends to act more on the host, weakening it and accentu- ating disease activity. Research with vegetable crops at low ozone concentrations indicate that pollutant-disease interactions do occur with some diseases and very likely occur in forest stands weakened by photochemical pollutants. Ozone has increased susceptibility to Fomes and rendered trees more susceptible to decay. Each interaction is unique since every fungus has its own sensitivity as does each plant. Thus the potential for interaction is enormous. Pollutants such as fluoride that accumulate significantly in plants would likely have the greatest interaction. While the trend is to inhibit disease development, the concentrations at which this has been demonstrated are now infrequent in the field. The significance of abiotic stress and pollu- tant interactions is often taken for granted, but it should be emphasized that this is of paramount importance. Climatic and edaphic factors are often determinants in the expression of pollutant damage. While the abiotic environ- ment strongly influences the severity of air pollution damage, air pollutants influence the severity of plant diseases caused by biotic pathogens. It would appear that as in all life systems, every environmental parameter has some influence on every other. In the case of pollutants and pathogens, this interaction can be significant. LITERATURE CITED Chiba, 0. and K. Tanaka. 1968. The effect of sulfur dioxide on the development of pine needle blight caused by Rhizosphaera kalkhoffii Bubak (I). J. Jap. For. Soc. 50: 135-139. Curtis, C. R., R. K. Howell and D. F. Kremer. 1976. Soybean peroxidase from ozone injury. Environ. Pollut. 11:189-194. Donabauer, E.
1966. Secondary damage to forest caused by industrial exhaust fumes. Mitt. Forst. Bundesvers. 73:lOl. Grzywacz, A. 1978. Interactions between air pollutants and decaying fungi of pine wood. In. 3rd Internat. Congress of Plant Pathology. Munchen. 1978. Grzywacz, A. and J. Wazny. 1973. The impact of industrial air pollutants on the occurrence of several important pathogenic fungi of forest trees in Poland. Eur. J. For. Path. 3:129-141. Ham, Donald L. 1971. The biological interactions of sulfur dioxide and Scirrhia acicola in loblolly pine. Ph.D. Thesis, Duke Univ., No. Carol. 75 p. Harkov, R., B. Clarke and Eileen Brennan. 1979. Cadmium contamination may modify re- sponse of tomato to atmospheric ozone. J. Air Poll. Control Assoc. 29: 1247-1249. Heagle, A. S. 1973. Interaction between air pollutants and plant parasites. Ann. Rev. Phytopathol. 11:365-388. Heagle, A. S. 1975. Response of three obligate parasites to ozone. Environ. Pollut. 9:91-95. Heagle, A. S. and Alice Strickland. 1972. Reaction of Erysiphe graminis f. sp. hordei to low levels of ozone. Phytopathol. 62:1144-1148. Heck, W. W.
1968. Factors influencing expression of oxidant damage to plants. Ann. Rev. Phytopathol. 6:165-188. Heck, W. W., J. A. Dunning and I. J. Hindawai. 1965. Interactions of environmental factors on the sensitivity of plants to air pollution. J. Air Poll. Control Assoc. 15:511-515. Hibben, C. R. and M. P. Taylor. 1975. Ozone and sulfur dioxide effects on the lilac powdery mildew fungus. Environ. Pollut. 9:105-114. Krause, G. H. M. and H. Kaiser. 1977. Plant response to heavy metals and sulfur dioxide. Environ. Pollut. 12:63-71. Krause, C. R. and T. C. Weidensaul. 1978. Effects of ozone on the sporulation, germination, and pathogenicity of Botrytis cinerea. Phytopathol. 68:195-198. Lamoreaux, R. J. and W. R. Chaney. 1978. Photosynthesis and transpiration of excised silver maple leaves exposed to cadmium and sulphur dioxide. Environ. pollut. 17:259-268. Laurence, J. A. 1978. Effects of air pollutants on plant- pathogen inteactins. 71st Ann. Mtg. Air Poll. ControlAssoc. Houston, Texas. 1978. Laurence, J. A. and F. A. Wood. 1978. ~ffects of ozone on infection of soy bean by Pseudomonas glycinea. Phytopathol. 68:441-445. Leone, I. A. and Eileen Brennan. 1972. Sulfur nutrition as it contributes to the susceptibility of tobacco and tomato to SO2 injury. Atmos. Environ. 6:259-266. Linzon, S. N.
1973. The effects of air pollution on forests. Pap. 4th It. Chem. Cong. Conf. 1973 pp. 1-18. Manning, W. J. 1975. Interactions between air pollutants and fungal, bacterial and viral plant pathogens. Environ. Pollut. 9: 87-90. McCune, D. C., L. H. Weinstein, J. F. Mancini, and P. van Leuken. 1973. Effects of hydrogen fluoride on plant- pathogen interactions. Internat. Clean Air Congress, Dusseldorf. Mejstrik, V. 1978. Influence of sulfur dioxide on the growth of some fungus species. Zbl. Bakt. I1 Abt. 133: 464-467. Miller, Paul R., and Joe R. McBride 1975. Effects of air pollutants on forests. In Responses of plants to air pollution. J.
Brian Mudd and T. T. Kozlowski, eds. p. 192- 235. Academic Press, New York. Miller, Paul, R. and M. J. Elderman. 1977. Photochemical oxidant air pollution effects on a mixed conifer ecosystem. Ecological Research Series EPA 60013-77-104. Taylor, 0. C.
1974. Air pollution effects influenced by plant-environmental interaction. Amer. Chem. Soc. Sympt. Ser. 3:l-7. Oertli, J. J.
1958. Effect of salinity on susceptibility of sunflower plants to smog. Soil Sci. 87:249- 251. Treshow, M. 1970. Environment and plant response. 422 p.
McGraw-Hill Co., New York. Ormrod,
1977.
and
and
D. P.
Cadmium and nickel effects on growth ozone sensitivity of pea. Water, Air Soil Pollut. 8:263-270. Saunders, P. J. W. 1971. & Ecology of Leaf Surface Microorganisms,
pp. 81-89, T. F. Preece and C. H. Dickinson. Academic Press, London. Scheffer, T. C., and G. G. Hedgcock. 1955. Injury to northwestern forest trees by sulfur dioxide from smelters. U.S. Forest Serv. Tech. Bull. 1117, 1-49. Scheutte, L. R.
1971.
Response of the primary infection process of Erysiphe graminis f. sp. hordei to ozone. Ph.D. Thesis, Univ. Utah, Salt Lake City, 71 p.
Shriver, D. S.
1974. Effects of simulated rain acidified with sulfuric acid on host-parasite inter- actions. Ph.D. Thesis, N. Carolina State, Raleigh, N.C. Treshow, M.
1975. Interactions of Air Pollutants and Plant Disease. InResponses of plants to air pollution. J. Brian Mudd and T. T.
Kozlowski, eds. p. 307-334. Academic Press, New York. Wainwright, M. 1978. Sulphur-oxidizing microorganisms on vegetation and in soils exposed to atmos- pheric pollution. Environ. Pollut. 17:167- 174. Weidensaul, T. C. and S. L. Darling. 1979. Effects of ozone and sulfur dioxide on the host-pathogen relationship of Scotch pine and Scirrhia acicola. Phytopathol. 69:939-941. Weinstein, L. H., D. C. McCune, A. L. Aluisio and P. van Leuken. 1975. The effect of sulphur dioxide on the incidence and severity of bean rust and early blight of tomato. Environ. Pollut. 9:145-155. Studies on Relationship Between Air
Pollutants and Microorganisms in
Japan1
Kiyoshi ~ a n a k a ~ Abstract: A review of the literature on the interaction of air pollutants with parasitic and epiphytic microorganisms is pre- sented with a brief outline of air pollution problems in Japan. Some fungi such as Cercospora sequoiae, Pucciniastrum styracinum, Puccinia kusanoi, Melampsora coleosporioides, Trichoroma matsutake, and some epiphytic bacteria disappeared in the areas affected by air pollutants, and Rhizosphaera kalkhoffii
increased its activity due to SO2 in the air. Fungi, bacteria, viruses and nematodes, as well as insects are all responsible for bringing a cer- tain species of higher plants into equilibrium with its environment (Treshow 1968). The effect of air pollutants on population trends of various micro- organisms, therefore, is extremely important in all ecological systems. Further, air pollutants may affect plant disease development in different ways. Pathogenicity may be influenced through a direct effect of the pollutants on the parasite, or the effects may be indirect through pollution-induced changes in physiology of the host plant eagle 1973). confused with the similarities between the symptoms of many types of pollution damage and those of in- fectious diseases sometimes leading to incorrect diagnoses. Fortunately, each of the common air pollutants produces a characteristic injury pattern, and the sensitivity of many species differs suffi- ciently for the trained eye to determine the caus- ative agent dams and Salzbach 1961)
.
This paper will review the literature on: 1) the modification of parasitism and the population changes of epiphytic microorganisms induced by air pollutants; 2) attempts to make reliable guides in distinguishing among symptoms caused by air pollu- tants and parasites, and those occasionally pro- Prior to 19601s, the interaction of microorgan- isms with pollutants in the air had received limit- duced by saprophyfcic fungi. These subjects are ed attention in Japan. But during the past decades, considered in conjunction with a brief outline of a series of experiments has been conducted in order air pollution effects on forest ecosystems in Japan to explain the effect of air pollution on
dis-
ease development, and only recently, some attempts SULFUR DIOXIDE have been made to understand the change of popula- tions of microorganisms for use as biological indi- In Japan, towards the end of 19th century, air cators of air pollution. pollution was reported to be harmful to forests From the beginning of recognition of the signifi- around ore smelters that emitted large amounts of SO2. Plume behavior resulted in pollutants disper- cant and sometimes devastating effects of air pol- sion in the surrounding area, killing all the veg- lutants on vegetation, plant pathologists have been etation (mainly Cryptomeria japonica D.Don and Pinus densiflora Sieb. et Zucc.) and causing ero- sion of topsoils following the death of the plants presented at the Symposium on Effects of Air (Doi 1919). The concentration of SO2 of the smoke Pollutants on Mediterranean and Temperate Forest was reported to be 1 ppm at 1 mile from a large ore Ecosystems, June 22-27, 1980, Riverside, smelter located in Ashio, Tochigi Prefecture, and California, U.S.A. occasionally reached as high as 8 to 10 ppm at the 2~orestPathologist, Kansai Branch, Forestry
ground level (Doi 1919)
and Forest Products Research Institute, Momoyama, Fushimi, Kyoto 612 Japan. .
Raising the height of stacks in order to reduce the concentration of SO at the ground level was
the first and primitive2control measure, new tech- nology involves the installation of sulfur recov- ery devices. In 1915, one ore smelter in Hitachi, Ibaraki Prefecture, built a new stack on a hill rising about 350 m above sea level; the stack was nearly 170 m high, so that the smoke was discharged at an elevation of approximately 520 m. Although smelter smoke is released from high stacks, it tends to diffuse rather slowly, and the SO., there-
fore, reaches the ground in harmful concentrations even after a considerable length of time and dis- tance. Observations made three years after the replacement of stacks revealed the fact that the severity of damage in the area near to the smelter was markedly reduced,while the total damaged area increased as large as 24,000 ha ( ~ o i1919). The reduction of the concentration of S O in the area in the vicinity of the ore smelter on account of the change of stack height was good enough to resume the seedling production of Cryptomeria Japonica in nurseries. Kaburagi (1930) was im- pressed with the absence of a needle blight of Cryptomeria ,japonica caused by Cercospora sequoiae Ell. et Ev. in the nurseries located in the recov- ered area close to the higher stack. The needle blight is one of the most destructive diseases in forest nurseries producing Cryptomeria seedlings, and has spread rapidly throughout Japan except Ho- kkaido. The causal fungus was introduced from North America in the end of 19th century, and Iba- raki Prefecture including the ore smelter is con- sidered to be the epicenter of the introduced dis- ease (Ito 1976). Kaburagi (1930) suggested that a strong correlation existed between SO in the air 2
and the absence of the disease. This is believed to be the first report on the effect of air pollu- tion on diseases caused by parasites in Japan. Ka- buragi's observation is strongly supported by the following hypotheses that: 1) SO might act direct?
ly upon the fungus on the surfaces of host plants; and 2) the reduction of disease severity resulted in a decrease of inoculum for new infection. Some of the acute type of damage by the emis- sions from smelters still continues in areas near to sources. In the 19601s,widespread SO, air pol- lution damage to ornamental trees had become appa- rent to the public; this increase was due to urban- ization and industrialization. The one most appa- rent episode in and around Tokyo was the stunting and death of a large number of Zelkova serrata Mak., widely used as shade trees throughout Japan (yambe 1973). With a considerable increase in public awareness of the chronic type of pollution in many parts, automatic SO recorders were set up by the national 2
and the prefectural agencies to determine the con- centrations, frequency, and the duration of atmo- spheric SO exposures. The number of measuring locations $ad increased from the beginning at the 15 strategic locations in 1965 to as many as 1473 locations in 1979, forming an extensive sampling system for SO2 (The Japanese Environmental Agency The analysis of air provides a framework of knowledge, and a foundation for developing air quality management strategies, and for prompting the enactment of the Clean Air Act in 1967, and its amendments made in 1970. Figure 1. Mean value of annual concentrations at 15 strategic locations. Figure 1 shows annual changes in average concen- trations of SO at 15 strategic locations between 2
1965 and 1977, the concentration increased until 1967, and then declined gradually. The decline has proved the continuing effectiveness of regula- tion of air pollution sources by the national and the prefectural governments based on the act. During the summers in the middle of 19601s,the worst average concentrations of SO2 were experienc- ed. In this period, an unrecorded needle blight of Japanese red pine, Pinus densiflora, occurred throughout the normal range of that species, pre- dominantly in central Japan. Up to that time the disease had been little known and of little concern to forest pathologists. A specific fungus domi- nantly found on blighted needles was investigated by Kobayashi (1967), and he identified it as Rhizosphaera kalkhoffii Bubak which had been known as a causal fungus of a needle blight of spruce and fir in northern Europe and North America. The results of inoculation experiments to Japanese red pine seedlings proved that the pathogen- icity of the causal fungus was considerably weak for pines, and the disease would scarcely occur if pines grew under normal conditions anak aka and Chi- ba 1971). The unusual incidence of the disease occurring in the early s m e r of 1.965 might be re- lated to abnormal weather conditions--extremely little rain fell in early spring followed by heavy rain in May (Chiba and Tanaka 1968). Although the disease has not occurred so widely as in 1965, severe damage has been observed in the vicinity of ore smelters or industrial areas. In addition, Japanese red pine is highly sensitive to S O (Ino- ue 1973), and the distinction between the needle blight symptoms caused by the disease and those caused by SO is exceedingly difficult (Tanaka 1975, Therefore exhaustive experiments
Tanita 1976)?
were conducted to examine the relationship of SO,,c-
with disease development. A t o t a l of 163 two-year-old seedlings of Japane s e r e d pine were exposed t o 2.0 ppm SO f o r 1,2,3,
2
and 4 hours i n a fumigation chamber before
or after
inoculation i n t h e middle of J u l y , with a water
suspension of conidia of t h e fungus produced on
PDA p l a t e s .
Damage was more severe i n t h e treatment combini n g t h e fumigation with inoculation, e s p e c i a l l y
i n o c u l a t i o n before fumigation, compared with t h o s e
i n t h e treatment of fumigation without inoculation.
Numerous pycnidia of t h e fungus were produced i n
l a r g e l e s i o n s on needles t r e a t e d by fumigation
a f t e r i n o c u l a t i o n a s well a s fumigation f o r longer
duration before i n o c u l a t i o n , no obvious change i n
t h e appearance of needles was detected on t h e seedl i n g s inoculated with t h e fungus without fumigation.
Symptoms produced on t h e SO t r e a t e d needles, name2
l y , l a r g e l e s i o n s with numerous pycnidia, were
i d e n t i c a l t o symptoms of t h e needle 'blight occurr i n g i n t h e f i e l d ( ~ h i b a nd Tanaka 1968).
Most pine seedlings displayed acute symptoms of
i n j u r y following exposure t o 2.0 ppm SO f o r 2
hours. The SO concentration used i n this study
2
was s e v e r a l times higher than t h a t found i n t h e
ambient a i r . It was necessary t o e l u c i d a t e t h e
r e l a t i o n s h i p between SO and d i s e a s e development a t
2
lower concentrations because such conditions a r e
f r e q u e n t l y encountered i n r u r a l and f o r e s t regions.
Therefore, three-year- o l d seedlings of Japanese
r e d pine were exposed f o r 2 weeks i n chambers t o
0.2 ppm SO
t h e l e v e l of SO i s l i k e l y t o be found
2
i n t h e ambient a i r (Tanaka 1576a).
I n t h i s experiment, s p e c i a l emphasis was placed
on t h e e f f e c t of SO fumigation a f t e r inoculation
i n comparison with $he treatment before inoculation.
The t r e a t e d needles with SO2 fumigation a f t e r inocul a t i o n were more s e v e r e l y a f f e c t e d by t h e fungus,
compared with t h o s e fumigated by SO gas before
i n o c u l a t i o n . This r e s u l t i s c o n s i s t e n t with findings of t h e 2.0 ppm SO fumigation (Chiba and Tana2
ka 1968). S O i n j u r y appeared t o f a c i l i t a t e t h e
spread and reproduction of t h e fungus within tissues of needles r a t h e r than t o i n c r e a s e t h e i n i t i a l
r a t e of i n f e c t i o n by t h e fungus.
To f u r t h e r examine t h e s e findings from a r t i f i c i a l SO exposure of seedlings i n chambers, f i e l d
2
experiments were planned and conducted during t h e
summers of 1972 and 1973 by using a t r a n s p l a n t i n g
method anak aka e t a l . 1974a) and a f i l t e r e d a i r
method (Tanaka e t a l . 1974b) i n Hiroshima Prefect u r e . I n t h e t r a n s p l a n t i n g study, two experimental
p l o t s were e s t a b l i s h e d . One was i n Fukuyama c i t y
c l o s e t o a l a r g e s t e e l r e f i n e r y . Especially i n
t h i s a r e a , d i s t i n c t SO damage markings on t h e
needles of Japanese r e g pine were v i s i b l e . The
o t h e r was i n a r u r a l a r e a i n Miyoshi c i t y . It was
l o c a t e d about 60 km n o r t h of a highly i n d u s t r i a l i z e d
a r e a along t h e Seto Inland Sea including Fukuyama
c i t y . I n t h e r u r a l a r e a , t h e d i s e a s e caused by
Rhizosphaera k a l k h o f f i i had not been noted i n
recent y e a r s . A t o t a l of 900 p o t t e d seedlings of
Japanese r e d pine used i n t h e t r a n s p l a n t i n g study
were cultivated, previously i n t h e n u r s e r i e s i n t h e
r u r a l a r e a i n Miyoshi c i t y . Seedlings were divided
i n t o 12 groups a s shown i n f i g u r e 2 according t o
t h e combination of t r a n s p l a n t i n g and inoculation.
SO concentrations of both a r e a s were determined
2
by means of t h e l e a d peroxide method. Needles were
analyzed f o r sulfate-S and f o r t o t a l - S dry b a s i s
i n order t o determine t h e accumulation of s u l f u r
i n t h e needles. F o l i a r symptoms were r a t e d from
0 t o 5 , according t o t h e degree of injury,and t h e
average of t h e s e i n d i v i d u a l indexes provides t h e
disease s e v e r i t y f o r each group.
After being t r a n s p o r t e d from t h e r u r a l a r e a t o
t h e i n d u s t r i a l i z e d a r e a , s e v e r a l seedlings exhibi t e d t y p i c a l symptoms and signs of t h e d i s e a s e ,
while o t h e r s remaining i n t h e r u r a l a r e a displayed
no evidence of i n j u r y , even though they received
t h e c o n i d i a l spraying of t h e c a u s a l fungus ( f i g u r e
2).
In t h e experiment using a f i l t e r e d a i r method,
an experimental p l o t was e s t a b l i s h e d i n an a r e a
i n Mihara c i t y c l o s e t o a powdered-coal-burning
power p l a n t . I n t h i s a r e a , a l a r g e number of need i e b l i g h t e d Japanese red pines were found, and
they displayed gradual reduction i n shoot and wood
growth. The previous y e a r ' s annual mean contents
of s u l f u r compounds i n t h e a i r was 1.04 mg SO 1100
3
cm2 PbO2 per day.
P l a n t s were grown i n p l a s t i c covered chambers.
One chamber ( 2 x 4 ~ 2m ) was equipped with carbon f i l t e r s and blowers, and t h e c o n t r o l o r ambient a i r
chamber was provided with blowers. The a i r passed
through each chamber a t a r a t e of about one a i r
change / min. SO2 concentrations of t h e ambient
a i r were determined by means of an automatic recorder, and SO concentrations i n chambers were
2
measured, by t h e l e a d peroxide method.
The experimental design was s i m i l a r t o t h e t r a n s p l a n t i n g experiment i n Fukuyama and Miyoshi, t h a t
i s , a t o t a l of 300 seedlings were divided i n t o 12
groups according t o t h e combination of exposure t o
SO2 and inoculation of t h e c a u s a l fungus, then seedl i n g s were placed i n chambers t o determine whether
some p r o t e c t i o n from i n f e c t i o n could be obtained
when t h e a i r drawn i n t o t h e chamber was f i l t e r e d .
There was a l a r g e reduction i n t h e s e v e r i t y of t h e
disease i n t h e f i l t e r e d a i r compared with t h a t of
t h e disease i n t h e ambient a i r . These findings by
f i e l d s t u d i e s furnished t h e evidence t h a t SO2 i n
t h e a i r was responsible f o r t h e development of t h e
disease. The s u l f u r content e s p e c i a l l y sulfate-S
i n t h e needles of t h e t r e e s exposed t o SO2 was s i g n i f i c a n t l y g r e a t e r than t h a t of untreated needles
both i n t h e t r a n s p l a n t i n g and t h e f i l t e r e d - a i r experiments.
An increasing i n disease:severity may.be expected
when a i r p o l l u t a n t s weaken t r e e s , making them more
s u s c e p t i b l e t o i n f e c t i o n by weak p a r a s i t e s , o r reduced vigor t o a degree t h a t p l a n t s become predisposed t o a t t a c k by f a c u l t a t i v e p a r a s i t e s , such a s
Rhizosphaera k a l k h o f f i i , and B o t r y t i s cinerea Pers.
Conversely, Linzon (1958 )
( ~ a n n i n ge t a 1 1970 )
.
.
!i
(U
CO 4
0
2sp j
--2j,6;/
0
J
A
S
D
J
A
S
D
J
A
S
D
5.11
transportation inoculation J
A
S
P
J
T
!
J : Jun 20
A:Aug
1
S: Sep 13
-0-0-0-0
J
A
S
D
JAS
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0-J
Figure 2. Effect of SO2 on the development of needle blight of pine caused by Rhizosphaera kalkhoffii found that smelter emissions decreased the inci- dence of Cronartium ribicola C.J.Fis.,and there are additional reports that aggressive or obligate para- sites, such as Microsphaera alphitoides Griff. et Maubl. ( ~ o c h1935) , and Melampsorella cerastii Wint ,
Peridermium coloradense Arth. et Kern, and some species of Melampsora and Gynmosporangium (Scheffer and Hedgcock 1955) were less abundant in areas ad- jacent to smelter zones or to industrialized areas. ltol found a similar case in Tokyo that a"close re- lationship existed between the increase of distance from the metropolitan area and the increase of the incidence of willow rust disease caused by Melampsora coleosporioides Dietel and a leaf rust disease of Styrax japonicum Sieb. et Zucc. caused by Pucciniastrum styracinum Hirat. The complex of air pollutants was brought about by urbanization and industrialization, typical of the mixture of pollutants occurring in and around Tokyo, but SO2 was considered to be principally responsible for reducing the abundance of these fungi. OXIDANTS MAINLY OZONE ( 0 )
Beginning in the 19701s, changes from solid to liquid and gas fuels, and especially increasing use of motor vehicles, have caused a reduction of the SO type of urban pollution and an increase of "ozone" pollution. Personal communication from S. Ito, University of Tokyo, January 15, 1980. On July 18, 1970, Zelkova serrata trees in a yard of a senior high school located in Suginami Ward in Tokyo showed unusual shedding of their leaves, and strawberry leaves showed white spots clearly indicating the effects of oxidants. In addition to the damage to plants, 45 students of the school were hospitalized for treatment of irri- tated eyes, sore throats and difficulty in breath- ing. From this evidence, the Metropolitan Govern- ment issued the statement that the damage to humans and vegetation was caused by photochemical air pol- lution (The Tokyo Metropolitan Government 1971), and this was thought to be the first episode of 'Los Angeles type smog" in Japan. But as a result of later investigations it was found that there were differences between Tokyo and Los Angeles air pollution, since SO2 concentration and humidity in Tokyo were much higher than in Los Angeles; fur- thermore, it was confirmed that there was forma- tion of sulfuric acid in the air (The Tokyo Metro- politan Government 1971). These findings suggest that the complex of photochemical oxidants and sulfuric acid might exert a far greater influence on humans and vegetation than any other alone at that time. In the latter half of 19701s,with continuous increasing industrialization and transportation, every major city in Japan has experienced an in- creasing in photochemical oxidants even though there was a slow but steady decline in the concen-. tration of SO2,in the ambient air (figure 1).
Photochemical oxidants , mainly ozone (0 ) ,continue to cause the defoliation of broad leaf trees. Especially, in the Kanto district, at the center of Tokyo, unusual defoliation of Zelkova serrata still continues, since it is sensitive to both SO2
(Inoue 1973) and 0 (Kadota and Ohta 1972). While, in the Kansai dist?ict,at the center of Osaka, there is a high incidence of defoliation of poplar trees in the early summer in the parks, the gardens or the yards of schools throughout the district. In addition to the measuring system of SO2
throughout the country, a number of automatic oxi- dant recorders were also set up by the national and the prefectural agencies, but there is still a shortage of satisfactory apparatus for monitoring the low ambient concentrations. To make up for the shortage of an instrumented system, plants have been used extensively as bioindicators of air pollu- tion. The use of bioinaicators has long been ac- cepted, since damage to green plants is usually one of the first signs that air pollution is becoming a serious problem e err^ 1964); their usefulness in this capacity is based primarily on the sensitivity of selected plant species and varieties for speci- fic pollutants (Heck 1966). Many clones, species and varieties of poplars were selected as bioindicators because of their high sensitivity to oxidants and their wide distri- bution, especially in the Kansai district. They also have enounnous advantages in that they are fast growing, easy to propagate vegetatively by c u t t i n g s , and a r e uniformely
injury.
s e n s i t i v e t o oxidant
Despite t h e s e advantages, poplars a r e frequently
plagued by various kinds of i n s e c t s and diseases
t h a t degrade t h e usefulness of poplar clones as
p o l l u t i o n i n d i c a t o r s . For example, i n t e r p r e t a t i o n
of t h e response t o oxidants i s made d i f f i c u l t by
l e a f diseases caused by Marssonina brunnea (El1.et
Ev.) Magnus, S e p t o t i n i a podophyllina Mhetz. and
Melampsora l a r i c i - p o p l u l i n a Kleb. A r e l i a b l e guide
t o d i s t i n g u i s h among symptoms caused by a i r pollut a n t s , i n s e c t s , and diseases has been developed and
The d e f o l i a t i o n caused by
published ( Tanaka 1975 )
Marssonina brunnea i s one of t h e most serious diseases. It occurs wherever poplars grow, and i s not
r e s t r i c t e d t o urban regions, but frequently occurs
with s e v e r i t y i n urban areas. The disease develops
t i n y spots with l i g h t margins about 1 mm i n diameter over t h e e n t i r e surface of t h e l e a f . These
s u p e r f i c i a l spots a r e not so d i f f i c u l t t o d i s t i n guish from t h e symptoms caused by ozone by p l a n t
p a t h o l o g i s t s with a t r a i n e d eye, but many people
who want t o use poplars a s i n d i c a t o r s a r e confused
with t h e s i m i l a r symptoms produced by ozone and t h e
disease (Tanaka 1975). I n addition, t h e disease
causes premature lower l e a f abscission,and t h e def o l i a t i o n progresses upward toward t h e t i p s of t h e
shoots from t h e l a t e spring through t h e summer
months. The unsightly appearance of a f f e c t e d t r e e s
discourages poplars' use as i n d i c a t o r s of oxidants.
.
A number of i n v e s t i g a t o r s suspected t h a t absciss i o n was not due d i r e c t l y t o t h e pathogen but res u l t e d i n s t e a d from increased r a t e s of ethylene
production from t h e i n f e c t e d p l a n t s (Abeles 19731,
f u r t h e r , ozone-induced abscission of leaves of varying maturity was c l o s e l y c o r r e l a t e d with r a t e s of
ethylene production ( ~ b e l e s1973). From t h e s e
reasons, Tanaka (1976~))hypothesized t h a t increased
r a t e s of ethylene production caused by t h e synerg i s t i c e f f e c t s of t h e i n f e c t i o n of t h e fungus and
ozone was responsible f o r t h e incidence of t h e disease i n t h e urban area.
Fortunately, t h e r e i s s t r i k i n g v a r i a b i l i t y i n
s u s c e p t i b i l i t y of poplar clones t o t h e fungus and
ozone. Clones were s e l e c t e d t h a t a r e s e n s i t i v e t o
ozone and r e s i s t a n t t o t h e disease. The s e l e c t i o n
o f f e r s one of t h e best means of increasing t h e usab i l i t y of poplar clones a s ozone i n d i c a t o r s (Tanaka
1977a). Table 1 presents t h e r e l a t i o n s h i p between
ozone s e n s i t i v i t y and disease r e s i s t a n c e of poplar
clones (Tanaka 1 9 ~ ~ a )The
. data of r e s i s t a n c e of
poplar clones t o t h e disease a r e based on t h e t h r e e
years' observation made i n Osaka using 38 clones of
young rooted c u t t i n g s t an aka 1 9 7 ~ a ) ,and t h e d a t a
of ozone s e n s i t i v i t y of them a r e based on t h e res u l t s from t h e exposure experiments with 0.15 ppm
ozone f o r 40 hours i n chambers conducted by Enoki
(1977).
Populus maximowiczii cv. O J 115 and cv. OJP 1,
P m a x i m o ~ i ~ c h o c a cv
r ~ OaP 41, P .maxino& z i i x 2.nigra pl&tierens cv.0P 52, and P.nigra
i t a l i c a x ~.maximowiczii,cv.Kamabuchia r e promising
clones f o r ozone i n d i c a t o r s because they a r e sensit i v e t o ozone and r e s i s t a n t t o t h e d i s e a s e ( t a b l e 1 ) .
.
.
Yambe (1978) a l s o attempted t o f i n d a possible
usefulness of t h e change of microbial f l o r a on bamboo leaves a s i n d i c a t o r s f o r a i r p o l l u t i o n . He
found t h a t Puccinia kusanoi D i e t e l and epiphytic
b a c t e r i a on t h e l e a f surfaces of bamboo decreased
sharply i n number i n t h e urbanized and i n d u s t r i a l ized areas.
Table 1. Relationship between c l o n a l s u s c e p t i b i l i t y of poplars t o 0
3
I
S u s c e p t i b i l i t y t o Marssonina brunnea
Highly
resistant
resistant
Resistant
(R)
and t o Marssonina brunnea.
1
Resistant
Moderately
resistant
HE 2, OP 26,
Serotina
Susceptible
NR 19,
MR 32
Highly
susce'otible
I 45/51
I
Moderately
resistant
Gerlica
I 154, I 214
Highly
susceptible(ss^
I 72/51, Kamabuchi,
O J 115, OJP 1, OJP 2,
OJP 3, OJP 4, OJP 5,.
OP 4 1
I 262
I 77/51,
I 488
OTHE8 POLLUTANTS
p a r a s i t e y Rhizosphaera k a l k h o f f i i (Chiba and Tanaka 1968).
I n a d d i t i o n t o SO and oxidants, s i g n i f i c a n t and
2
sometimes devastating e f f e c t s of o t h e r a i r pollut a n t s have long been recognized i n Japan. Fluoride
compounds have a long h i s t o r y a s p o l l u t a n t s i n t h e
v i c i n i t y of ceramic i n d u s t r y , and more r e c e n t l y ,
p l a n t i n j u r y r e s u l t e d from f l u o r i d e s has gradually
increased because of t h e expansion of i n d u s t r i e s
such a s aluminum r e f i n e r i e s m d f e r t i l i z e r manuf a c t u r e s ( ~ a t u u r aand Kokubu 1972). Chlorine (Tanaka 1977b), ethylene, a c i d i c dust from s t a c k s , and
a l k a l i n e dust from cement k i l n s (Inoue 1972a and
1972b) have a l s o been recognized a s agents of dmage t o v e g e t a t i o n y but t h e damaged a r e a s a r e r e l a t i v e l y r e s t r i c t e d because most of them a r e emitted
from point sources o r by a c c i d e n t a l s p i l l s .
The i n t e r a c t i o n of t h e s e minor p o l l u t a n t s with
fungi and b a c t e r i a has received only minor a t t e n t i o n , but Inoue (1972a and 1972b) found t h a t t h e
number of f r u i t i n g bodies of Tricholoma matsutake
Singer was s i g n i f i c a n t l y reduced i n t h e heavily
dusted f o r e s t s i n t h e v i c i n i t y of cement works compared t o l e s s severely dusted o r non-dusted port i o n s of f o r e s t s . According t o t h e r e s u l t s of
hand-dusted experiments,he concluded t h a t t h e alkal i n e s o l u t i o n from t h e dust severely decreased t h e
formation of t h e f r u i t i n g bodiesy and reduced t h e
development of t h e fungus colonies.
Although p l a n t i n j u r y caused by s p e c i f i c polluand f l u o r i d e s has gradually
t a n t s such a s SOpy 0
been abated by enginJering improvements o r by-products recovery, chronic i n j u r y caused by a complex
of urban a i r p o l l u t a n t s has assumed a d d i t i o n a l i m portance a s urbanization and t h e use of motor veh i c l e s have increased.
I n j u r y t o green p l a n t s i s usually one of t h e
f i r s t s i g n s t h a t a i r p o l l u t i o n is becoming a s e r i o u s
problem, and s e v e r i t y of s p e c i f i c d i s e a s e s i n poll u t e d a r e a s must be regarded a s an a d d i t i o n a l expression of unbalanced n a t u r a l conditions. These
s p e c i f i c diseases and t h e change of composition of
l e a f surface microorganisms provide a i d s f o r monit o r i n g a i r p o l l u t a n t s y e s p e c i a l l y i f they a r e sens i t i v e t o very low concentration of a i r p o l l u t a n t s .
These diseases and microorganisms should be considered a u s e f u l supplement t o t h e more expensive
techniques and instruments used f o r t h e i d e n t i f i c a t i o n of chronic a i r p o l l u t a n t e f f e c t s .
Acknowledgments: I thank D r . Paul R. M i l l e r ,
P a c i f i c Southwest Forest and Range Experiment Stat i o n , U.S. Dep. A g r i c a Yf o r h i s c r i t i c a l readings
of t h e manuscript.
CONCLUSIONS
L1T.ERATURE CITED
The i n t e r a c t i o n of p o l l u t a n t s with p a r a s i t i c and
epiphytic microorganisms has received l i m i t e d a t t e n t i o n i n Japan. The e x i s t i n g r e p o r t s a r e only
a s s o c i a t e d with t r e e s and bamboos and no r e p o r t
with annual p l a n t s was found i n a search of a v a i l able l i t e r a t u r e .
Some p o l l u t a n t s a r e d i r e c t l y t o x i c t o microorganisms on t h e l e a f surface. They might possibly
impair t h e i r growth o r reproductiony and change t h e
population and community composition of mCcroorgani s m s on t h e h o s t p l a n t s , s i n c e t h e s e n s i t i v e spec i e s t o a i r p o l l u t a n t s would be gradually replaced
by more t o l e r a n t s p e c i e s (Treshow 1968). Especiall y y aggressive o r o b l i g a t e p a r a s i t e s such a s Cercospora sequoiae (Kaburagi 1930), Pucciniastrum
racinum and Melampsora coleosporioides ( 1 t o 1 ) ~ and
Puccinia kusanoi (Yambe 1978) a r e l e s s abundant i n
polluted a r e a s y and t h e d i s e a s e s e v e r i t y they induce?
i s s h a r p l y reduced.
m-
On t h e o t h e r hand, i n f o r e s t stands under i n f l u ence of i n d u s t r i a l and urban a i r p o l l u t i o n , some
f o l i a r pathogens counted by p a t h o l o g i s t s i n t h e
group of so-called ' f a c u l t a t i v e p a r a s i t e ' a r e of
g r e a t e r importance because a i r p o l l u t a n t s i n j u r e
l e a f t i s s u e and predispose
t r e e s t o a t t a c k by
f a c u l t a t i v e p a r a s i t e s . A c l o s e c o r r e l a t i o n has
been found between SO i n t h e a i r and a high i n c i dence of needle b l i g h z of pine caused by a weak
'
Personal communication from S. It0
of Tokyo, January
1980.
University
.
.
.
Adms $D,F and C W. Sulzbach
1961. Nitrogen deficiency and f l u o r i d e susceptib i l i t y of bean seedlings. Science 133: 1425-1426.
Abeles ,F.B.
1973. Ethylene i n p l a n t biology. 302pp. New York.
Berry,C.R.
1964. Eastern white pine, a t o o l t o d e t e c t a i r
p o l l u t i o n . Southern Lumberman 209(2609):164,166
Chiba,O. and K.Tanaka.
1968. The e f f e c t of sulphur dioxide on t h e development of pine needle b l i g h t caused by Rhizospha e r a k a l k h o f f i i Bubk. I. J.Jap.For.Soc. 50:
135-139
-
Doi ,T.
1919.
orest st
p r o t e c t i o n ) . b09pp. Tokyo.
.
Enoki ,M
1977. (Clonal s u s c e p t i b i l i t y of poplars t o ozone).
Ann. ~ e p1976.
.
,Osaka Agr Centr :117-119.
.
.
Heagle,A.S.
1973. I n t e r a c t i o n s between a i r p o l l u t a n t s and
p l a n t p a r a s i t e s . Ann.Rev.Phytopath. 11:365-388.
Heck,W.W.
1.966. The use of p l a n t s a s i n d i c a t o r s of a i r poll u t i o n . A i r Water Poll.1nt.Nat.J. 10:gg-111.
Inoue,I.
lg72a. Studies on the influence of smoke-dust from a cement plant on the vegetation of pine forests, especially on Tricholoma matsutake. I. Trans .Mycol.SOC.Jap. 13:196-214. Inoue,I.
1972b. Ditto 11.
Tanaka,K. 1976b. Tree diseases in air polluted areas and their usability as indicators. a : 51-56. Tanaka,K. 1977a. Pest problems in the use of poplar clones as indicator plants for photochemical oxidnats
Trans.88th Mtg Jap For.Soc :419-421.
.
.
.
. .
M:215-288.
Inoue T
1973. (Tree injury caused by sulfur dioxide). Plant Protection 27:8-12. Tanaka,K.
1977b. Accidental chlorine gas damage to ornamen- 4l5-4l7.
tal woody plants.
It0,K. TanakayK.,T.Okada and K.Hako. 1974a. Effect of SO2 on the development of needle blight of pine caused by Rhizosphaera kalkhoffii, Transplanting experiment. Trans.86th Mtg Jap .For.
Soc.:290-292. 1976. Blight and canker of Cryptomeria Japonica D.Don. caused by Cercospora se uoiae Ellis et Everhart. Ann.Phytopath. Soc Jap 2 :234-236.
.-%-
Japanese Environmental Agency. 1979. (White paper on environment for 1979)
2163pp. Tokyo. .
w:
.
Tanaka,K.,M.KuwakiBT.Okada and K.Hako. 1974b. A plastic covered chamber with activated carbon filters. =:211-213. Kaburagi,T. 1930. (Smoke damage to plants). Iwanami Lectures for Bioloa. 1-39. Tanaka,K. and 0.Chiba. 1971. On a needle blight ~f pine caused by Rhizo- sphaera kalkhoffii--Life historyy physiological Kobayashi>T. characteristics and pathogenicity of the causal 1967. Critical revision on the genera Rhizosphaera fungus. J.Jap .For,Soc 53:279-286.
Mangin et Harriot and Rhizophoma Petrak et Sydow, a little-known fungus group associated with Tanita,S
needle disease of conifers. Bul1.Gov.For.Exp. 1976. Histological effects of air pollutants and Sta. 204 :91-112,
pathogens on Pinus thunbergii. Trans 88th Mtg. Jap .For.Soc :373-37k.
Kadota,M. and K.Ohta. Tokyo Metropolitan Government. 1972. Ozone injury to some Japanese woody plant species in summer. J.Jap.For.Soc 54:226-229.
1971. ~okyofights pollution. 2 6 7 ~ ~Tokyo.
. .
.
.
.
K6ch9G. 1935. Eichenmehltau und Rauchgasschaden. Z.Pf-
lanzenkr 45 :44-45.
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Treshow, M. 1968. m e impact of air pollutants on plant popu- lations. Phytopathology 58:1108-1113.
Linzon,S.N. Ymbe, Y. 1958. The influence of smelter fumes on the growth 1973. decline of trees in Tokyo. Bul1.Gov.For. Exp.Sta. 257:lOl-107. of white pine in the Sudbury region. Can.Dep. Agr Publ. ,Ontario Dep.Lands Forests. 45pp.
Ymbe, Y. Matuura,S. and N.Kokubu. 1978. Decline of trees and microbial florae as the index of pollution in some urban areas. Bull. 1972. Fluorine, its distribution and role in nature. 150pp. Tokyo. For.& For.Prod.Res.1nst. 301:llg-129. .
Scheffer,T.C. and G.G.Hedgcock, 19.55. Injury to northern forest trees by sulfur dioxide from smelters. UDSA,For.Serv.Tech.Bull. 1117:49pp.
Tanaka,K.
1975. The similarity between symptoms caused by air pollutants, insects, and diseases. Agr. and Hort. 5O:Preface. Tanaka ,K. 1976~~.
m e effect of low-level SO fumigation on the development of needle bligh$ of pine caused by Rhizosphaera kalkhoffii. Anr1.Rep.1975.~m e range of tolerance of biological indicators to pollutants :5-9.
Sensitivity of Lichens to Air Pollution
with an Emphasis on Oxidant Air
Pollutants1
Thomas H. Mash I11 and Lorene L. Sigal^ Abstract: The hypothesis that lichens are sensitive indicators of air pollution is now well established for oxidants, sulfur dioxide, hydrogen fluoride and trace ele- ments. From field studies differential sensitivity of dif- ferent lichen species around pollution sources is evident. Laboratory studies with the particular air pollutant general- ly confirm the same degree of differential sensitivity. LICHENS AND THEIR ECOLOGY Lichens, which strictly speaking are called lichenized fungi, are composite plants represent- ing a symbiotic union of algae and fungi to form morphological entities unlike either component (Ahmadjian 1967, Hale 1967). Although a few species survive in aquatic environments, most are found in terrestrial habitats, occurring on soil, rocks and as epiphytes on other plants. All lichens are perennial plants with life spans varying from a few decades to reportedly thousands of years (Weber and Andrews 1973). Essentially all lichens are autotrophs because of the photo- synthetic activity of the algae. Metabolic activity in general is limited to period's when the lichens are moist, a condition which varies in concert with atmospheric moisture conditions as lichens have no roots by which moisture might be absorbed from the substrate. Thus lichens are prominent examples of poikilohydric plants (Larcher 1973) which also include bryophytes and some lower vascular plants, such as desert species of Selaginella and ferns. Because of moisture presented at the Symposium on Effects of Air Pollutants on Mediterranean and Temperate Forest Ecosystems, June 22-27, 1980, Riverside, California, U.S.A. '~r. Nash is associate professor of botany, Dept. of Botany, Arizona State University, Tempe, Arizona 85281 USA; Dr. Sigal is a research scien- tist, Environmental Sciences Division, Oak Ridge National Laboratory, P.O. Box X, Oak Ridge,. Tennessee 37830 U.S.A. constraints on photosynthetic activity, primary productivity assignable to lichens is generally small compared to higher plants. Nevertheless lichens may be important in ecosystem functioning. For example, lichens are generally recognized as important pioneer plants of xeric successional sequences because of their role in biologically controlled weathering (Syers and Iskandar 1973). In addition, lichens are important in mineral cycling, not only because of their ability to alter precipitation chemistry (Ianq and others 19761, but also from the ability of blue-green algae contain- ing lichens to fix atmospheric nitrogen. Den son (.1973) has estimated that lichens are respons ble for 50 percent of the nitrogen fixed in the Douglas-fir forests of the Pacific Northwest. Lichens are morphologically divided into 3 major growth forms: crustose, foliose and fruticose. Crustose species are generally small, tightly attached to (or imbedded in) their substrate and poorly differentiated. Foliose species are gen- erally larger, loosely attached to their substrate and stratified into several distinct layers. In contrast to the basically 2-dimensional foliose species, fruticose s~eciesare strongly 3-dimen- sional and grow out from their substrate. Most fruti'cose species are also differentiated into distinct layers. Of these morphological forms fruticose species are generally considered to be the most sensitive to air pollution (Fenton 1964), a fact which may be related to the high surface- to-volume ratio of this form. LICHENS IN RELATION TO AIR POLLUTION Different species of lichens are well-known to be differentially sensitive to air pollution (Nash 1976). A few species actually grow better in urban environments where air pollution levels are high in contrast to their performance in rural areas. Most species, however, exhibit varying degrees of sensitivity to air pollution and some are more sensitive than higher plants. Thus by documenting variations in abundance and species richness of lichen communities, it is frequently possible to identify poliution sources and to document the magnitude of the air pollution probla, Patterns within lichen communities may be attribut- able to many environmental factors other than air pollution, of course, and consequently it is extremely important that studies be made within a multivariate context, including both pollution factors and non-pollution factors. The fact that lichens are differentially sensi- tive to air pollution is based on a series of field observations and laboratory experiments extending back over the past 130 years. Grindon (1859) and Nylander (1867) noted that lichens were disappearing from city centers. Later Arnold (1892) documented that lichens transplanted from rural areas to the center of Munich were not able to survive. Subsequently this "city effect" has been reported for many cities in Europe and North America (Hawksworth 1971). By air pollution most workers of the 1800's generally meant coal soot and related particulates. However, over the past decades a number of invisible gases, such as sulfur dioxide and ozone, have been identified as the major causes of air pollutant injury to plants. Experiments with these air pollutants over the past two decades have also demonstrated differential sensitivity among different lichen species. In general, the sensitivity patterns demonstrated in the laboratory have remarkably Corresponded to the patterns observed in the field around pollution sources. Perhaps the strongest evidence supporting the contention that lichens are sensitive to air pollution comes from studies documenting lichen recovery following pollution abatement. For example, Seaward (19761 has docu- mented that Lecanora muralis fairly rapidly reinvaded an urban complex in southern England following amelioration of air pollution in the area. Californian mountains* The study was centered in the San Bernardino Mountains, utilizing the sites mployed by the University of California (Riverside and Davis] ecosystem study of air pollutant effects in contrast to sites in a control region, Cuyamaca Rancho State Park in southern San Diego County. In addition, there was an excellent historical record of the lichens of the San ~ernardinosbased on collections made by H. E. Hasse at the turn of the century. Of the 91 foliose and fruticose lichen species reported by Hasse (1913) in his lichen flora of southern California, only 34 species were found during three sunnners of study throughout southern California. Thus there has been a significant reduction in the number of species present. To obtain quantitative data on lichen variation, both conifers (Ab2es concolor, Pinus ponderosa, Pinus jeffreyi and Pseudotsuqa macrocarpa) and California black oak (Quercus kelloggii) were sampled for lichen cover at breast height. In the case of conifers Hasse (1913) reported the presence of 16 foliose and fruticose lichen species in the San Bernardino Mountains. In our recent study [Sigal and Nash 19801 only 8 of these species were found in the San Bernardino Mountains and 4 of these were only present in vestigial quantities. In contrast, at sites to the north and to the south K'uyamacasl 15 of the 16 species reported by Hasse were found. Thus in the San Bernardinos which lie adjacent to the Los Angeles Bash, there has been a SO percent decline in species richness of lkhens on conifers. Of the species which do occur in the San Bernardinos only two (Letharia Vulpina and Hypogymnia entero- momha) occur commonly. The latter species, although it is common, is definitely showing signs of deterioration (Table 1) when randomly selected thalli from the San Bernardinos are compared with a similar set from the Cuyamacas. The San Ber- nardino population has a much higher percentage Table 1-- Morphological characteristics of recent collections of Kypogymnia enteromorpha from the San Bernardinos and the Cuyamacas. Percent Bleaching In the following sections specific evidence related to various types of air pollutants w211 be reviewed. Forest 38
Oxidant Air Pollutants Oxidant air pollutants, including ozone and peroxyacetplnitrate (PANI, are a group of gases
characteristic of the oxidizing atmospheres found in the Los Angeles type smog (Pitts and Finlayson 1975). Although the effects of these compounds have been studied extensively with higher plants (National Academy of Sciences 19771, relatively few studies have been conducted with lichens. Probably the only field study in which lichens have been shown to be sensitive to oxidants is that of Sigal and Nash (1980) for the southern 59
41 Percent Convoluted Forest 38
38
47
15 of bleached and convoluted thalli. In addition, there was a decrease of approximately 50 percent in overall thallus dimensions in the San Bernardino population and a decrease in fertility of 42 the San Bernardinos. Among the 20 species which
occurred in common there was a general shift from
high frequency in the Cuyamacas to relatively low
frequency in the San Bernardinos. In the case of
cover of the 6 most common species, no significant
difference was observed between the two mountain
ranges except for Collema nigrescens, the only
nitrogen fixing lichen in the groupi which was
completely absent from the San Bernardinos. Further analysis revealed that Parmelia subolivacea,
the most common lichen, was a successional species.
Because older trees occurred in the Cuyamacas, a
significantly higher value for this species in the
Cuyamacas was predictable. Further evidence supporting the hypothesis that the dominant species
was in fact respondhg to oxidants was obtained
by running ordinations (princiwal component analysis) of the sites within the San Bernardinos and
relating the observed variation in species composition to oxidant dose estimates and other
environmental variables (fig. 1).
An initial
ordination (not shown) included all sites sampled
within the San Bernardinos. It exhibited a small
cluster of low cover sites which occurred at the
percent. Thus there are marked trends between the
San Bernardinos and the Cuyamacas of reduced
species richness and species vitality in the former area. Within the San Bernardinos themselves,
significant variation exists. Below approximately
150 ppm-h oxidant dosage, cover of both Letharia
and Hypogymnia is normal in comparison with other
areas. At higher dosages of up to 285 ppm-h
lichens are almost completely eliminated from
conifers.
Comparisons of trends of lichens occurring on
black oak between the San Bernardinos and Cuyamacas
also indicated that a deterioration was occurring
in the San Bernardinos, but the trends were not as
dramatic as in the case of lichens occurring on
conifers. No direct comparison with the Hasse
material was possible because Hasse did not note
the species of oak in his collections. From our
sampling 39 species of lichens were found on black
oak in the Cuyamacas and 30 specie3 in the San
Bernardinos. Fourteen of the species found in the
Cuyamacas were not found in the San Bernardinos
whereas three species were found exclusively in
.
12.1
COO.
10.2
7.6
TOTAL % COVER
ALL L I C H E N S
12.9
13.5
ucc
12.1
I
15.7
BF.
Bp
CA
230.8
186.7
i33.2
% COVER
PARMELIA SUBOLIVACEA
8.2
BF
GVC 4
DWA
T2
184.9.
COO.
134.7
,,cc
145.8
175.0
D
OXIDANT DOSE ESTIMATES
183.2
BF.
SAN BERNARDINO NAT'L
STUDY - S I T E LOCATIONS
FOREST
Fig. 1--Principal component analysis ordination of 10 sites in the San Bernardino Mountains using cover data for the 5 most important lichen species occurring on Quercus
kelloggii. Eighty percent of the variation is explained by axis one (the abscissa).
Figure 1A shows the positioning of the sites on the ordination plot with respect to total cover of all lichens; figure lBf the same ordination but with cover values for
melia subolivacea; figure lC, the same ordination, but with oxidant dose estimates
(ppm-h); figure IDf the geographic location of the sites within San Bernardino National Forest.
=-
highest elevations where summer fog is infrequently observed. Consequently these sites and one other site on the desert side of the San Bernardinos were excluded from the subsequent analysis. The 10 sites plotted in figure 1 are thus homogeneous with respect to altitude and position along the Los Angeles side of the San Bernardinos (fig. 1Dl. In the subsequent ordination (fig. lA, 1B and lC), 80 percent of the variation is explained by axis 1 (the horizontal axis). From figures 1A and 1B it is clear that the primary source of variation is the percent cover of all lichens, which in turn corresponds closely to the percent cover of E.
subolivacea. Furthermore, there is an inverse relationship between percent cover of E.
olivacea (fig. 1 ~ )and oxidant dose estimate (1C).
This inverse relationship was substantiated by running a Speaxman rank correlation between the two variables. The test was significant with an alpha value of 0.007. For the other 4 species no relationship between oxidant dose estimates and cover values were found. Thus some species have been completely eliminated from the San Bernardinos, other species have probably declined in abundance and a few species are apparently unaffected. s-
Preliminary ozone fumigations have shown dif- ferential responses in photosynthesis reduction between Pamelia sulcata and Hypogymnia entero- morpha with the former species exhibiting greater sensitivity (Nash and Siyal 19791. The Parmelia, which grows on black oak, is absent from the San Bernardinos whereas the Hypogymnia is present, but is exhibiting signs of deterioration. For these species, at least, the pattern of sensitivity observed in the field and the laboratory are com- plementary. A similar pattern of response for the two species was observed after fumigations with PAN (Sigal and Taylor L979). Further stud2es with both ozone and PAN should be run, but the current evidence strongly supports the assertion that oxidants are a major cause of the decline of the lichen flora in the San Bernardino Mountains. Sulfur Dioxide Sulfur dioxide is released into the atmosphere by combustion reactions involving products con- taining the ubiquitous element sulfur, such as coal and oil. It has long been recognized as a phytotoxic agent in general (Daines 1968). Lichens are well known to be sensitive to sulfur dioxide (Nieboer and others 19761. Most of the field studies in northern Europe and North America have involved sites where sulfur dioxide was a major factor (Hawksworth 1971). One of the classic studies by Rao and LeBlanc (1967) demon- strated a severe decline in lichen abundance along a 70+ km transect NNE of Wawa, Ontario where an
iron sintering plant is present. Because there is essentially no human development in the affected region, air pollution, and particularly sulfur dioxide, is undoubtedly a major cause of the de- cline in the reqionts lichens. Other studies have shown that lichens accumulate sulfur (Olkkonen and Takala 1975, Laaksovirta and Olkkonen 1977) in situations where the presumed source of sulfur is sulfur dioxide. The gas readily dissolves in water forming a sulfite or bisulfite solution depending on the pH. As a con- sequence acidification of the substrate frequently occurs, as has been shown in Stockholm where Skye (19681 found that urban tree bark had a pH of more than two units less than corresponding trees from the country-side. Acidification strongly affects the ability of lichens to survive, in part because sulfur dioxide is much more toxic at lower pH's (Tuerk and Wirth 1975). Gilbert (1965 and 1970) has clearly demonstrated the ability of lichens to penetrate into central Newcastle on basic sub- strates when they are absent from acidic ones. In the laboratory studies, photosynthetic decline in response to short term sulfur dioxide exposures as low as 0.2 ppm have been demonstrated (Tuerk and others 19741. In aqueous experiments with reputedly lower concentrations, effects have also been documented Baddeley and others 1973, Puckett and others 19741.. In addition to reduction of photosynthesis, bleaching of lichen thalli may occur due to phaeophytinisat2on of the chloro- phyll~ (Nash 1973, Puckett and others 19731. More recently potassium efflux from lichens exposed to sulfur dioxide has been shown to be the most sen- sitive criterion of response (Tomassini and others 1977). Alteration of membrane permeability may thus be an immediate response to sulfur dioxide exposure. Subsequently it is suggested (Nieboer and other 1976, Puckett and others 1974) that interference in electron flow in photosystem I and I1 will occur'and that proteins will be affected through sulfur dioxide$ ability to cleave disul- phide linkages. Thus there is very strong evi- dence from both field and laboratory studies that lichens are sensitive to sulfur dioxide. Hydrogen Fluoride Hydrogen fluoride is extremely volatile and is released into the atmosphere during aluminum and rare earth metal refining, fertilizer production and glass and ceramic manufacturiny. Patterns of lichen decline are well demonstrated around alumi- num factories (Martin and Dacquard 1968, Gilbert 1971, LeBlanc and others 1972, Horntredt 1975) and around a titanbn plant (Nash 19711 and around a phosphate plant (Takala and others 19781. In these areas fluoride accumulat~onby the lithens has been demonstrated with decline in the lichen cornunities being associated with elevated fluo-
ride levels. Transplants of healthy lichens into the impoverished zones resulted in fluoride accu- mulation and subsequent death of the transplants. Gilbert suggested that the critical fluoride level lay between 20 and 50 ppm and Nash independently suggested that the value lay between 30 and 80 ppm. Schoenbeck (1969) found that his transplants died near a fluoride source, but that new transplants survived well for several months following cessa- tion of the fluoride emissions. In a laboratory study with exposure to approximately 5 ppb fluoride over a 9-day period Nash (1971) found that lichens accumulated 84-115 ppm fluoride in contrast to control levels of 14-25 ppm and that the fumigated samples developed chlorotic and necrotic symptoms similar to the injury observed in the field trans- plants. Thus fluoride as the probable cause of the injury was confirmed. Trace Elements Lichens have a well demonstrated ability to accumulate elements from dilute aqpeous solutions (Nieboer and others 1977)# a fact probably related to their apparent dependence on atmospheric sources for mineral nutrition. As a consequence of this ability to retain elements# the study of trace element concentrations in lichens is fre- quently useful in demonstrating "fallout" patterns of particulates and aerosols. For exampleI mercury is found in elevated concentrations near a chlor- alkali works in Finland (Lodenius and LaaJcsovirta 1979); lead is elevated in lichens adjacent to highways (Laaksovirta and other 1976# Lawrey and Hale 1979); and a number of elements are present in high concentrations in citiesI such as Tel Aviv (Garty and others 1977) and Sendalp Japan (Saeki and others l977lI near the nickel complex at SudburyI Ontario (Tomassini and others 1976)I near
a coal-fired power plant (Gough and Erdman 1977) and in coal mine ecosystems of Ohio (Lawrey and Rudolph 19751. In none of these cases is toxicity of the accumulated elements demonstrated. Toler-
ance to high concentrations of elements may occur if the elements are relatively insoluble and are localized extracellularly. For exampleI Noeske and others (1970) showed that iron and copper were encrusted on the surface of lichens which grew on metal rich substrates in the Harz Moun- tains of Germany. FurthermoreI Garty and others (1979) have shown that particulates in Tel-Aviv are incorporated extracellularly within the lichen thallus. In contrast to the above studies "trace" ele- ments do occasionally occur in toxic concentra- tions. Lawrey and Hale a9791 have shown accumu- lation of approximately 1000 ppm lead in a lichen growing near an expressway in the vicinity of WashingtonI D.C. They demonstrated that.lead accumulation is correlated with reduction in growth of the speciesI but they have neither demonstrated experimentally that lead was the cause of the reduced growth nor demonstrated that other factors associated with automobile emissions were unimportant. Probably the most convincing study documenting trace element toxicity is that of Nash (1975) around a zinc smelting complex in eastern Pennsylvania. In the vicinity of the smelting complexI lichen species richness was reduced to 7 in contrast to the 77 species found in a control area (Nash 1972). The zone of lichen impoverishment extended for a distance of 15 km W and 10 km E of the smelting complex (fig- 2). Although detectable and potentially toxic levels of sulfur dioxide were found adja- cent to the smeltersI the distribution of elevated levels of sulfur dioxide did not extend as far as the lichen impoverishment zone extended- The relative unirnprtance of sulfur dioxide was further documented by the lack of acidification of the bark of oak trees and by the fact that the 2oE
10
DISTANCE FROM
low
0
EAST SMELTER
(kml
Fig. 2 ~ T h e
distribution
of the lichen-impover- ished zone (Nash 1972) at Palmerton# PennsylvaniaI in relation to the zones of modified forest (Jordan 1975)# to detectable levels of ambient sulfur dioxide (Nash l975lI and to elevated levels of cadmium and zinc in surface soils (Buchauer 1973). company had installed and subsequently contin- uously used an acid plant at the time that zinc sulfide ores were initially processed. In con- trast# metal concentrations in the soil duff were as high as 1351000 ppm zinc and 1750 ppm cadmium
at a site adjacent to the smelting complex Duchauer 1973). The concentration of zinc and cadmium decreased exponentially with distance from the smelters until background concentrations were found at 20 to 25 km E and 16 km W of the smelters (fig. 21. Physiological studies demonstrated that zinc and cadmium were toxic to the lichens when concentrations reached 300-500 ppm in the thallus. Since zinc was present in concentrations 100 times that of cadmium and since zinc is approximately as toxic as cadmiumI zinc was in- ferred to be the most important pollutant. ¶i points beyond the li'chen impoverishment zone zinc concentrations ranged from 20-200 ppm and cadmium from 1-30 ppmI where both sets of values were demonstra5ly non-toxic. LITERATURE CITED Ahmadjian, V. 1967. The lichen symbiosis. 152 p, Ginn Co. (Blaisdell ) Boston.
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r a n g i f e r i n a (L.) Harm. New Phytol 79: 147155.
Tuerk, R. and V. Wirth.
1975. The pH dependence o f SOn damage t o
lichens. Oecologia ( B e r l i n ) 19: 285-291.
-9
-
and 0. L. Lange.
1974. CO,,~Gaswechsel-Untersuchunqen z u r SOo~ e s i s t e d zvon Flechten. o e c o l o ~ i a( B e r l .?
15: 33-64.
Webber, P. J. and J. T. Andrews.
1973. Lichenometry : a commentary.
Alp. Res. 5 ( 4 ) : 295-302.
Arct.
.
-9
K. J. Puckett, E. Nieboer, D. H. S. Richardson and B. Grace.
1976. Determination of copper, iron, n i c k e l ,
and sulphur by X-ray fluorescence i n l i c h e n s
from t h e Mackenzi e Val 1ey, Northwest T e r r i
t o r i e s , and t h e Sudbury D i s t r i c t , Ontario.
Can. J. Bot. 54: 1591-1603.
-
Acknowledgments : This research was supported
National Science Foundation
by t h e U.S.
grants DEB-7610244 and DEB-7921953.
Influence of Air Pollution on Population
Dynamics of Forest Insects and on
Tree Mortality1
Donald L. Dahlsten and David L. ~owney2 Abstract: Weakened trees are often predisposed to injury or death by insects, and in forest ecosystems particularly by bark beetles. In the San Bernardino National Forest the interaction between photochemical oxidant weakened ponderosa pine and the western pine beetle (WPB) was examined in de- tail. The major results from this study suggest that oxi- dant damaged trees attacked by WPB produce about the same total brood with lower initial attacks compared to healthier trees. This higher productivity trend is most evident in generation 1 trees Generation 2 trees, both damaged and healthy, are under much greater moisture stress and produce much less WPB brood than generation 1 trees regardless of oxidant damage. The implication of these results is that in stands with a higher proportion of damaged trees, a given population of WPB could kill more trees and increase at a greater rate than in a stand with a lower proportion of damaged trees. Simulation modelling with these results and other factors that affect ponderosa pine mortality should provide a basis for predicting long term effects of air pollution on the WPB population and pine mortality. Most of the work on air pollution damage has
focused on direct injury to the plant and
Kozlowski (1980) gives a good review of the impact of air pollution on forest ecosystems. By
comparison, little has been done on the indirect
effects such as the predisposing of plants to
insects or pathogens. Watt (1969) speculated on the effects of air pollution on population fluctuations of insects and Heagle (1973) reviewed
the interaction between air pollutants and plant
parasites. More recently the occurrence of
diseases and insect pests of trees in air
polluted regions of North America has been
recorded (Dominik 1978).
'presented at the Symposium on Effects of Air
Pollutants on Mediterranean and Temperate Forest
Ecosystems, June 22-27, 1980, Riverside,
California, U.S.A.
professor of Entomology and Statistician in
Entomological Sciences, respectively, University
of California, Berkeley, Calif.
There have been some studies on the direct effects of air pollution on insects. Feir (1978) studied the effects of air pollutants on insect growth and reproduction and Hillmann and Benton (1972) looked at the reactions of honey bees to sulfur dioxide. Bromenshenk (1976, 1978) has studied the effects of coal-fired power plant emissions on a variety of insects. In another study, Gilbert (1971) looked at the indirect effects of air pollution on several bark inhabiting insects. Air pollution may be the cause for the scarcity of all orders of insects in New Jersey (Muller 1971). The effects of insects in pine stands influ- enced by air pollution, particularly xylophagous insects, have been studied (Sierpinski 1972, 1977). In California on the San Bernardino Mountains, ponderosa pine shown to have advanced symptoms of oxidant injury were most frequently infested and killed by western pine beetle (Dendrocbonias'-brevicabis)
, and mountain pine
beetle (2. ponderosae) (Stark et al. , 1968). The
purpose
of this study was to look a little closer at the interaction between the western pine beetle and oxidant affected ponderosa pine, to see what effect diseased trees would have on the dynamics of bark beetle populations and to look for dif- ferences between beetle population parameters in diseased and healthy ponderosa pine. MATERIALS AND METHODS Field Procedures Beginning about the first week in July, the San Bernardino mountain areas with substantial ponderosa pine stands were searched for first generation western pine beetle attacked trees. These areas are generally on the southern side of the mountains at about 1500-1800 m elevation, and are areas where high oxidant air pollution levels occur. Second generation trees were located in mid-August to raid-September, depending on the timing of the first generation. Trees under attack were detected by pitch tubes or frags in bark crevices. Attacked trees were checked with an axe at the base to see which species were attacking and to check the staqe. Trees with mixed brood (2. ponderosae and 2. brevicomis) and
trees with strip attacks (one side only) were relatively uncommon and were not selected for this study. Trees with
spp. in the tops were selected, but sampling for western pine beetle was stopped at the base of infestation of the Each suitable tree located was used in the
study until the required number were found (12 per generation in 1973 and 1974, 6 per generation in 1975 and 1976). In the time period allowed for sampling the initial WPB stages there was no practical way to locate all the attacked trees in the area and thenpick a random subsample for the study. z.
Sampling Prior to sampling, the major tree character- istics were recorded: location, height, DBH, height of first green branch, and estimated tree damage due to air pollution. The air pollution damage was rated by rating upper and lower crown needle retention, needle condition, needle length, and branch mortality. Needle condition and re- tention were difficult to rate on the sample trees because in many cases, fading and needle loss due to the bark beetle attacks had begun. For 1973 only one needle length rating was made for the entire tree, so the needle length rating for the other years was combined to be consistent in the analysis ( in nearly all cases the upper
and lower crown needle length was the same). Samples for all procedures except where noted later were taken at 1.5 meter intervals over the length of the western pine beetle infestation. Two 88 cm2"discs taken on opposite sides of the tree at 1.5 meter intervals gave the desired level of precision. The samples were taken from the tree using a modified ortable 4.5 kg gas powered drill D
l P r e c o n Multiple Control, Ridgewood, New Jersey). A standard circular hole saw with an 11 can diameter blade was used in the chuck of the drill. This saw cuts an area of approximately 88 cm2. At each sample height the circumference was measured, then the two discs were cut. With the egg discs it was desirable to take a portion of the xylem with each disc to protect the galleries. After a disc was removed it was examined by the climber for insects, which were identified and called down to the notetaker. During the last larval sample emergence car- tons were placed on the trees at each sample height. These cartons were not removed until well after brood emergence. Laboratory Procedures Once the samples had been returned to Berkeley, they were placed in cool storage until analyzed. X-rayed samples were placed into rearing imme- diately after the radiographs were taken. Basically there were four laboratory analysis procedures for sample discs. Egg Disc Analysis To determine egg mortality discs were taken at 3.0 meter intervals approximately two to three weeks after the mass attack period. Sampling at every 3.0 m interval gave 4 or more heights for each tree. Egg discs were taken only once, at the time of the first larval sample. This avoids an additional climbing of the sample tree, assures that maximum egg hatch has occurred and mortality can still be determined. If xylem tissues still remained on the disc it was carefully removed so that the galleries in the phloem tissue were not disturbed. Gallery length was measured with a metric map reader and all attacks were recorded. Each disc was then exam- ined with a dissection scope (10-20x) along the length of all the adult galleries. Each egg niche was evaluated asempty or as containing a viable egg or nonviable egg in addition to re- cording larval eclosion. The difference between the total number of egg niches recorded and the total number of larvae hatched was calculated as egg mortality. X-ray Analysis The first samples to be x-rayed were taken con- currently with the egg discs (egg discs are des- troyed during analysis so they can not be placed into rearing). For generation one, an additional x-ray sample was taken late in the brood develop- ment period, usually in mid to late July. For the second generation, x-ray samples were removed on two later occasions: once in mid-September to October to check for early emergence of brood and adult re-emergence, and finally in the following spring (March to April) after brood development was nearly complete, but before spring emergence. oblique to the surface of the bark and often have pitch as a remnant of a pitch tube. Field Emergence Cartons The discs to be x-rayed were tkken from cold storage as soon as possible and removed from the plastic bags. The average bark thickness of each disc was measured with a metric caliper and the percentage woodpeckering on each disc was re- corded. The two 88 cm2 discs from each height were placed on one sheet of 8" x 10" Industrial ~odak@AA-2 film and exposed with a picker@ radiograph machine. The samples were then re- bagged and transported to a large storage shed f a rearing (see below). X-rays were interpreted for western pine beetle, live and dead parent adults, brood adults, pupae, and larvae, parasitoids, predators and miscellaneous. The miscellaneous category included buprestid and cerambycid larvae, weevils, *,and unknowns, of which there were
many judging from the rearing of these discs. A light table was used for interpretation and all inclusions were marked with a grease pencil by the interpreter, counted and then erased. A sec- ond interpreter then repeated the process, thereby reducing error and bias. The x-rays from each tree were then stored in envelopes as a per- manent record. Laboratory Rearing Each x-rayed disc was placed in a 1/2 gallon ice cream carton with a small 2 or 3 dram glass vial pushed through the lid. Since the insects in the discs are positively phototropic at least in the adult stage, and since very few beetles or other insects bore through the sides of the car- tons, this was a suitable rearing procedure. The cartons were stored in racks in a large unheated warehouse where Berkeley's mild, cool climate provided an ideal rearing environment. The emerging insects were collected from the vials three to five times per week. Most of the specimens could be identified with a lox hand lens and then recorded on a data sheet by collec- tion date. Only the parasitoids and the western pine beetle were sexed. All specimens have been identified by taxonomic experts and specimens were sent for verification regularly; the col- lection is updated as necessary. Approximately 130 different insects were recorded. In this paper, only WPB, 4 predators (Enoclerus lecontei, Temnochila chlorodia, Aulonium longum, Medetera &
J
X
aldrichii) and 4 parasites (Roptrocerus phagorum, Dinotiscus burkei, Eurytoma conica, Coeloides sp. nr. brunneri) are considered. Sample discs were kept in rearing for nine months and at the end of this period the cartons were examined for any remaining insects; the discs were then discarded. The gallery length and number of attacks were recorded for each disc prior to discarding. Attack holes can be dis- tinguished from emergence holea as they are As an additional check on emergence, a pro- cedure for rearing in situ on the sample trees was also used. One quart squat ice cream cartons that cover 88 cm2 of bark were painted silver on the outside and prepared with a screened ventilation hole. Stikem specialawas placed on the inside of the cartons to discourage insects from boring out or from going back into the bark. A groove was cut in the bark with the sampling saw into which the lip of the carton was placed; a nail was driven through the bottom of the carton and into the tree to increase stability. The cartons were placed on the tree at the time the last x-ray or brood sample was taken (to coincide with the pupal and/or callow adult stages n place for up to of the brood) and were left i
three months, until well after beetle emergence and the collection of all associated insects had taken place. The second generation cartons were nofc placed on the tree until early spring since cartons do not weather well and therefore cannot be left ort the trees for four to six months over winter. The cartons were split open and examined under the microscope and then discarded. The same insects that-wererecorded for laboratory rearing were recorded for the sticky emergence carton. RESULTS AND DISCUSSION Attacked tree characteristics and variation by year and generation: The tree heights of the 71 attacked trees sampled over the four year period varied from 13 to 44 meters, but most trees were in the 20-30 meter range (Fig. 1). Tree DBH, stem volume, and infested bark area varied more widely, but exhibited no significant trends with regard to year and generation. Western pine beetle attack and emergence density, however, both showed sig- nificant differences (P < -05) by generation.
Year differences were not significant for these variables except for a lower attack density for generation one trees of 1976 compared to the gen- eration one trees of the other three years. Effect of tree oxidant damage on beetle popu- lation :
In order to determine if damage to the sample trees had an effect on the western pine beetle populations, the individual components of the damage score were analyzed with respect to beetle attack density. Each individual component of the score can be regarded as an interval level vari- able, so multiple regression techniques were used to determine their relationship to attack density. The technique used was a full screen analysis Fig. 1. Western pine beetle attacked tree characteristics, attack density and emergence density by generation and year for 71 ponderosa pines in the San Bernardino National Forest, California. (dashed lines = mean +
one standard deviation) Most other generation one beetle variables were not significantly different between short aid long NL trees, except for eggs per attack and emerged brood per attack (Table 1). This prob-
ably indicates that the attacking beetles for generation one were more productive when the trees had lower attack density and less compe-
tition within the trees. The short NL generation 1 trees, with lower attack densities, had essen-
tially equal numbers of eggs and emerging brood compared to the long NL trees. /,* ,
,
1 2
1 2
74
75
GENERATION
L :
,
1 2
1 2
74
75
GENERATION
which calculated p2 values for all possible linear combinations of the score components, year, and beetle generation for the attack den-
sity dependent variable. The results of this analysis indicated that only the needle length (NL) component (upper and lower crown combined) of the score was significant (P < -05) along with
beetle generation. The effect of any other com-
ponents was insignificant when added to the equa-
tion containing NL and generation. Some of the other components which have been significant in other studies - needle retention and needle condition - probably were unreliable for these trees
as they were examined in a partly faded condition some weeks after being mass attacked by bark beetles. In subsequent analyses the needle length (NL) was used to distinguish between trees highly affected by air pollution (NL=O) and less affected trees (NL=l). Table 1 gives mean values of the attack density and other western pine beetle variables for each generation and needle length category. In our sample of trees significantly fewer short NL trees were found in generation one (7 of 36) compared to generation two (16 of 35), but due to the practical limita-
tions of our sample selection procedure, it is uncertain whether this difference holds true for the entire population of attacked trees; The attack density was significantly higher for long NL trees compared to short NL trees for both generations, while generation two trees had lower attack densities than generation one re-
gardless of ML.
The trend toward high productivity in the lower attack density, short NL trees for generation 1 was not evident for generation 2. The beetles in the short NL trees had essentially the same eggs/attack and emerged brood/attack as those in long NL trees (Table 1). Total eggs, hatched eggs, and late larval densities were all significantly lower in the lower attack density, short NL trees. Mortality proportions for each life stage sampled seemed relatively independent of NL although they were higher in generation 2 compared to generation 1. Table I--Western pine beetle variable means by gen-
eration and tree a: pollution injury(needle lerytH Generation 1 Generation 2
Short Long
Short
Long
Injury: NL
ML
NL
NL
No. of trees
~ttacks/~~~
Gallery length/^^^
Total eggs/~M2
Eggs/attack
Hatched eggs/Dll
(1st instar
larvae/~~2
)
Egg mortality
2
Late larvae/DM
Larval mortality-early to late
larvae (LM)
Emerged WPB
(REAR)
Mortality-late
larvae to emergence (REAR) (BPI)
Mortality-eggs to
emergence (REAR)
Emerged brood
per attack /Dd
*significant differences between NL classes, P < .05.
Needle length was also used to compare differ- ences in predator and parasite densities for each generation (Table 2).
Predators included the 4 common species: Enoclerus lecontei, Temnochila chlorodia, Au1oniw.1 longum, and Medetera aldrichii. Parasites included Roptrocerus
phagorum, Dinotiscus burkei, Eurytoma conica and Coeloides sp. nr. brunneri. For generation 1, only emerged (REAR) predators/dm2 were signifi- cantly higher for the long NL trees. For genera- tion 2, initial parasitized larvae/dm2 were higher for short NL trees, but late parasitized larvae/ dm2 were higher for long NL trees. A much larger increase in numbers of parasitized larvae occurred for the gen. 2, long NL trees. Increased woodpeckering, along with a higher final larval density for the long NL trees may explain the increased numbers of parasitized larvae. A similar proportion (about 1%) of initial larvae were parasitized in both cases. The consequences of bark beetle activity in an area are summarized in Table 3 and show that attack rates are lower on oxidant affected trees, but the output of brood is essentially the sane in healthy and diseased trees.
Bark beetles, assuming no direct deleterious effects of air pollution,should increase in areas with high ozone damage and tree mortality will also in- crease in these areas. The possible interactions of air pollution, ponderosa pine, and western pine beetle and the effects on forest succession are shown in Table 4. e-
-
Table 2--WPB predator and parasite means by gen- eration and tree air pollution injury class (needle length).
Generation 1
Generation 2
Short
Long
Short
Long
Injury:
NL
NL
NL
NL
2
29
No. trees
7
1.910
Initial pred./~~2 0.962
0.36
Initial para0.20
sitized lar./DM
2.75
Late predators/~~21.83
0.61
Late parasitized
0.56
larvae/~ll^
Emerged (REAR)
0.73*
1.50
predators/~~^
0.42
Eraer (REAR)para/D~2 0.48
0.8%
% area samples wood-0.1%
peckered
*Significant difference between
injury classes, P < .05
.
.
16
0.53
0.18*
19
0.30
0.08
0.80
0.26*
0.84
0.48
0.25
0.27
0.22
7.0%
0.28
11.0%
Table 4~Interactiontable: air pollution, ponderosa pine, and western pine beetle. Causes a change in VPB 1 Ponderosa Forest
pop. pine mortal- succes- level ity caused sion by WPB An increase In: air pollution
soil water
foliar injury
soil nutrients
mature tree growth
root disease
forest succession
WPB pop. level
pine mort. caused by WPB
+
+
?
?
+
?
++
+
+
?
?
?
?
?
?
+
+
+
0
++
+
?
0
+
-
-
0
Key: 0 = unrelated or not possible
+ = moderate increase
++ = large increase
= a large decrease
? = unknown, needs more investigation
-
means of smog LITERATURE CITED Kozlowski, T. T. 1980. Impacts of air pollution on forest eco- systems. BioScience 30:88-93. Table 3--Ozone effects table: western pine beetle in ponderosa pine. tree mort
.
low
long
4.0
3.9
consbat constant or deor de- creasing creasing high
short
2.4
3.7
increaskq increasing Motes: (1) Effect depends on individual tree character- istics. (2) Based on both generations combined and multi- plying female adult attacks by two to account for males. (3) Based on both generations combined. (4) Assuming constant no. of damaged pines/stand. Watt, K.E.F. 1969. Prospective effects of air pollution on insects. Can. Entomol. 101:1235-1238. Heagle, A. S. 1973. Interactions between air pollutants and plant parasites. Annu. Rev. Phytopathol. 11: 365-388. Dominik, J. 1978. Investigations of the occurrence of diseases and insect pests of North American trees in the regions of different degrees of air pollution caused by the industry. Final Report of Investigations covering the period of August 1, 1973-June 30, 1978. Warsaw: Sin., 1978. 91, 21 leaves: 111. Feir, D. 1978. Effects of air pollutants on insect growth and reproduction. Physiologist 21:36. Hillman, R. C., and A. W. Benton.
1972. Biological effects of air pollution on insects emphasizing the reactions of the honey bee, e m e l l i f e r a to sulfur dioxide. J.
Elisha Mitchell Sci. SOC. 88:195. Muller, J. 1971. Is air pollution responsible for melanism in Lepidoptera and for scarcity of all orders of insects in New Jersey, U.S.A. J. Res. Lepid. 10:189-190. Gilbert, 0. L. 1971. Some indirect effects of air pollution on bark living invertebrates. J. Appl. Ecol. 8: 77-84. Bro~~ienshenk,
J. J. 1976. Biological impact of air pollution on insects. Ecol. Res. Ser. 600/3-76-013: 295-312. Bromenshenk, J. J. 1978. Investigation of the impact of coal-fired power plant emissions upon insects: entomo- logical studies at the zonal air pollution systems. Ecol. Res. Ser. 600/3-78-021:473-507. Sierpinski, 2.
1972. The economic importance of secondary noxious insects of pine on territories with chronic influence of industrial air pollution. Mitt. Forstl. Bundes-Versuchsanst Wein. 97: 609-615. Sierpinski, Z. 1977. Economic significance of noxious insects in pine stands under the permanent impact of the industrial air pollution. Slyvan. .64:59-71. stark, R.W., P.R. Miller, F.W. Cobb, Jr., D.L. Wood, and J.R. Parmeter, Jr. 1968. Photochem- ical oxidant injury and bark beetle (Coleop- tera: Scolytidae) infestation of ponderosa pine. I. Incidence of bark beetle infestation in injured trees. Hilgardia 39:121-126. Air Pollutants and Their Effects on
Wildlife with Particular Reference to
the House Wren (Delichon urbica)'
James R. Newman, P ~ . D . ~
A b s t r a c t : I n j u r y and death t o w i l d l i f e from a i r
emissions have been recorded s i n c e before the
t u r n of the c e n t u r y . A i r p o l l u t i o n can d i r e c t l y
a f f e c t w i l d l i f e ( i . e . , cause d e a t h ) , or can
i n d i r e c t l y a f f e c t w i l d l i f e ( i . e . , cause h a b i t a t
l o s s ) . A r e c e n t i n v e s t i g a t i o n on t h e chronic and
s u b l e t h a l e f f e c t s of a i r p o l l u t i o n on t h e house
m a r t i n (Delichon u r b i c a ) h a s shown t h a t a i r
v
emissions can s i g n i f i c a n t l y a f f e c t t h e n e s t i n g
ecology of t h i s s p e c i e s .
INTRODUCTION
S i n c e t h e end o f t h e 19th c e n t u r y , over
100 a i r p o l l u t i o n episodes have been r e p o r t e d
i n v o l v i n g i n j u r y and death t o animals (Newnan
1975, 1979). Although t h e m a j o r i t y o f t h e
i n c i d e n t s involved domesticated animals, a number
o f i n c i d e n t s have been r e p o r t e d f o r w i l d l i f e
s i n c e t h e 1880's ( t a b l e 1 ) . O v e r a l l , t h e few
r e p o r t s i n v o l v i n g w i l d l i f e appear t o be more a
f u n c t i o n o f economic b i a s t o r e p o r t i n j u r y and
d e a t h o f domestic animals than some i n n a t e
r e s i s t a n c e o f w i l d l i f e t o a i r p o l l u t i o n . For
example, i n t h e e a r l y 1900's a r s e n i c emissions
from a smelter caused t h e i n j u r y and death o f
s e v e r a l thousand c a t t l e and h o r s e s i n r u r a l
Montana arkin ins and Swain 1908). No mention was
made o f i n j u r y o r d e a t h t o deer o r o t h e r w i l d l i f e
p l e n t i f u l i n t h e a r e a , a 1 though deer and r a b b i t s
a r e known t o b e v e r y s e n s i t i v e t o a r s e n i c
emissions ( P r e l l 1936; Hais and Masek 1969).
Eighty-five percent o f t h e w i l d l i f e i n c i d e n t s
h a v e been recorded i n the l a s t 25 y e a r s . The
i n c r e a s e i n the number o f w i l d l i f e i n c i d e n t s
a p p e a r s t o be due n o t o n l y t o an i n c r e a s e i n a i r
emissions but t o a b e t t e r understanding o f a i r
p o l l u t i o n e f f e c t s , broader communications, and a
g r e a t e r i n t e r e s t i n r e p o r t i n g such problems.
Table I-The
number of reported a i r p o l l u t i o n
i n c i d e n t s involving w i l d l i f e and af f e c t e d groups
(adapted Newman 1979)
Period
Before
1900
1900-1950
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.
^sen2ior E c o l o g i s t , P r o j e c t Operations,
Environmental Science and Engineering, Inc
P.O. Box ESE, G a i n e s v i l l e , F l o r i d a 32602.
.,
1951-1970
1971 t o
Present
TOTAL
Number of
I
W i l d l i f e Groups
consumer Groups
Inci
Game \ one game IPrim. [secondary
1
dents 1
1
1
1
1
Recent Federal l e g i s l a t i o n , namely t h e 1977 Clean
A i r Act Amendments, now r e q u i r e formal
c o n s i d e r a t i o n o f t h e e f f e c t s o f a i r emissions on
w i l d l i f e and o t h e r components o f e c o l o g i c a l
systems.
The purpose o f t h i s paper i s t o summarize some
o f t h e known e f f e c t s o f a i r emissions on w i l d l i f e
and p r e s e n t p r e l i m i n a r y f i n d i n g s on t h e
e c o l o g i c a l e f f e c t s o f a i r emissions on t h e house
m a r t i n ( ~ e l i c h o nu r b i c a ) , an i n s e c t i v o r o u s b i r d .
For t h i s p a p e r , d i s c u s s i o n i s l i m i t e d t o
t e r r e s t r i a l wild1 i f e and v e r t e b r a t e consumers
Previous s p e a k e r s h e r e d i s c u s s e d t h e e f f e c t s on
i n v e r t e b r a t e consumers.
.
a B r i t i s h Columbia pulp m i l l which emitted high
c o n c e n t r a t i o n s of H2S and o t h e r p o l l u t a n t s .
The dead b i r d s showed i n t e r n a l hemorrhaging i n
t h e l u n g s and l i v e r . 3
Adsorption of a i r emissions i n v o l v e s t h e
adhesion of g a s e s o r p a r t i c u l a t e s t o t h e e x t e r n a l
s u r f a c e s o r e x t e r n a l membranes, e . g . , cornea of
eyes. Light (1973) r e p o r t s a high i n c i d e n c e of
b i i n d n e s s i n bighorn sheep (*canadensis)
found i n mountain a r e a s of C a l i f o r n i a with heavy
o x i d a n t l e v e l s . Oxidants a r e known eye
i r r i t a n t s . Investigators i n ~ z e c h o s l o v a k i a ~
have observed e a r l y aging of t h e cornea i n h a r e s
( ~ e p u seuropaeus) found i n a r e a s with heavy
SO2 and p a r t i c u l a t e d e p o s i t i o n from power
p l a n t s and o t h e r i n d u s t r i e s .
GENERAL EFFECTS OF A I R EMISSIONS ON WILDLIFE
One of t h e e a r l i e s t w i l d l i f e i n c i d e n t s (1887)
i n v o l v e s t h e d e a t h of f a l l o w d e e r (Dama dama)
from a r s e n i c emissions from a s i l v e r foundry i n
Germany (Tendron, 1964). As e a r l y a s 1900 t h e
Royal S o c i e t y of London was charged t o i n v e s t i g a t e t h e phenomenon of i n d u s t r i a l melanism. T h i s
i n c i d e n t i s recognized more f o r i t s demonstration
o f " n a t u r a l " s e l e c t i o n than a s an environmental
problem. Recently, g e n e t i c changes i n small
mammals because of a i r p o l l u t i o n have been
r e p o r t e d (Newman 1980).
One of t h e ' e a r l i e s t d e t a i l e d d e s c r i p t i o n s of
t h e harmful e f f e c t s of a i r emissions on w i l d l i f e
i s from Germany. Arsenic emissions were the cause
o f widespread d e a t h of game animals i n t h e
Tharandt f o r e s t of Germany i n 1936. S i x t y t o
s e v e n t y p e r c e n t of t h e red deer (Cervus e i e p h u s ) ,
r o e d e e r (Capreolus c a p r e o l u s ) , and wild r a b b i t s
( ~ r ~ c t o l a g uc su n i c u l u s ) d i e d . The d e e r e x h i b i t e d
d e f e c t i v e h a i r growth and a n t l e r formation,
c i r r h o s i s of t h e l i v e r and s p l e e n , and emaciation
( P r e l l 1936).
Adverse e f f e c t s of a i r emissions on w i l d l i f e
have been r e p o r t e d from North America, Euro-pe,
and A s i a , and have included game and nongame
animals; b i r d s and mammals; primary and secondary
consumers; and h e r b i v o r e s , omnivores, and
c a r n i v o r e s ( t a b l e 1 ) . The e f f e c t s on w i l d l i f e
have included d i e - o f f s and o t h e r population
reductions, physiological abnormalities, disease,
p h y s i c a l i n j u r y , and bioaccumulation. The
m a j o r i t y of w i l d l i f e i n c i d e n t s r e p o r t e d involve
d e e r and small b i r d s (~ewman 1979). These groups
a r e not n e c e s s a r i l y more s e n s i t i v e but a r e more
l i k e l y t o be monitored, e s p e c i a l l y d e e r , which
i s a widely managed game s p e c i e s . The s t a t u s of
s m a l l b i r d s i s n o t o n l y of s c i e n t i f i c concern,
b u t a l s o of more widespread p u b l i c i n t e r e s t .
Pathways of contamination by a i r emissions f o r
w i l d l i f e a r e : i n h a l a t i o n , a d s o r p t i o n , and
i n g e s t i o n . Wellings (1970) r e p o r t e d t h e
o c c u r r e n c e of pulmonary a n t h r a c o s i s i n urban
sparrows ( P a s s e r domesticus) compared t o r u r a l
p o p u l a t i o n s i n C a l i f o r n i a . One of t h e most
s t a r t l i n g examples of contamination by i n h a l a t i o n
involved t h e d i e - o f f of 200 t o 500 s o n g b i r d s near
I n g e s t i o n i s t h e most commonly r e p o r t e d mode
o f contamination f o r w i l d l i f e . I n j u r y and d e a t h
t o w i l d l i f e from i n g e s t i o n o f contaminated food
and water have been r e p o r t e d f o r numerous animal
s p e c i e s i n c l u d i n g r a b b i t s and deer from a r s e n i c
emissions ( P r e l l 19361, d e e r from f l u o r i d e
emissions (Karstad 1967; Robinette and o t h e r s
1956; Newman and Yu 19761, and sparrows from
cadmium emissions (Nishino and o t h e r s 1973).
There a r e many r e p o r t s of t h e bioaccumulation of
a i r p o l l u t a n t s i n w i l d l i f e . With a few
e x c e p t i o n s , t h e e f f e c t s of t h i s bioaccumulation
a r e n o t known (Newman 1980).
A i r emissions may not be l e t h a l t o w i l d l i f e
b u t may lower t h e h e a l t h and r e s i s t a n c e of
w i l d l i f e s o t h a t n a t u r a l s t r e s s such a s cold and
s h o r t a g e of food may r e s u l t i n f u r t h e r i n j u r y o r
d e a t h . S t u d i e s on t h e h e a l t h of wild h a r e s
(Lepus europaeus) l i v i n g i n a r e a s of h i g h a i r
p o l l u t i o n i n Czechoslovakia showed p h y s i o l o g i c a l
r e s p o n s e s s i m i l a r t o animals with i n f e c t i o n s o r
a l l e r g i c r e a c t i o n s . There were a l s o changes i n
t h e normal age s t r u c t u r e of t h e h a r e p o p u l a t i o n s
( ~ o v a k o v a 1969). The g e n e r a l h e a l t h of d e e r
p o p u l a t i o n s a f f e c t e d by f l u o r i d e emissions i s
poor ( ~ o b i n e t t eand o t h e r s 1957; Karstad 1967;
Newman and Yu 1976; Newman and Murphy 1979). The
s u r v i v a l of t h e s e d e e r d u r i n g times of n a t u r a l
s t r e s s i s q u e s t i o n a b l e . Hais and Masek (19691,
r e p o r t t h a t a r s e n i c contamination of red and r o e
d e e r caused emaciation and l o s s of h a i r so t h a t
many of t h e animals f r o z e t o d e a t h d u r i n g t h e
winter.
I n j u r y o r d e a t h t o v e g e t a t i o n caused by a i r
emissions can have s i g n i f i c a n t i n d i r e c t e f f e c t s
on w i l d l i f e . The l o s s of food r e s o u r c e s and
h a b i t a t can occur a s t h e r e s u l t of i n j u r y o r
3 ~ n p u b l i s h e dr e p o r t , R.D. Harris 1971.
B i r d s Collected (Die Off) a t P r i n c e Rupert, B.C.
Canadian W i l d l i f e S e r v i c e , P r i n c e Rupert, B r i t i s h
Columbia.
4 ~ e r s o n a lcommunication from E l i s k a
Novakova, I n s t i t u t e o f Landscape Ecology, Prague,
Czechoslovakia.
d e a t h t o v e g e t a t i o n which provides c o v e r ,
r e p r o d u c t i v e h a b i t a t , o r food f o r w i l d l i f e . Many
examples e x i s t o f e x t e n s i v e damage t o ecosystems
from a i r e m i s s i o n s . Large a r e a s o f t h e mixed
c o n i f e r o u s f o r e s t o f s o u t h e r n C a l i f o r n i a (over
40,000 h e c t a r e s ) have been k i l l e d o r i n j u r e d from
photochemical o x i d a n t s ( ~ a y l o r1973). No o v e r a l l
assessment h a s been made a s t o t h e l o s s o f
w i l d l i f e whose f o r e s t h a b i t a t h a s been d e s t r o y e d .
S i m i l a r l a r g e w i l d l i f e h a b i t a t l o s s e s have
o c c u r r e d i n Montana, Tennessee, B r i t i s h Columbia,
and O n t a r i o , Canada (~ewman 1980).
ECOLOGICAL EFFECTS OF AIR EM IS S IONS
ON THE HOUSE MARTIN
With few e x c e p t i o n s , t h e r e i s l i t t l e
i n f o r m a t i o n a v a i l a b l e on t h e e f f e c t s o f c h r o n i c
exposure o f w i l d l i f e t o a i r emissions (Newman
1980). Since 1976, RNDr. E l i s k a Novakova, CSC,
from t h e I n s t i t u t e o f Landscape Ecology, Prague,
and myself have been s t u d y i n g t h e e c o l o g i c a l
r e s p o n s e s o f t h e house m a r t i n (Delichon u r b i c a )
t o chronic a i r pollution.
In t h i s p o r t i o n of t h e
t a l k I would l i k e t o p r e s e n t some o f our
preliminary findings.
The house m a r t i n b e l o n g s t o t h e family
H i r u n d i n i d a e . It i s an i n s e c t i v o r o u s b i r d lAiich
f e e d s p r i m a r i l y on a p h i d s and d i p t e r e a n s . A
m i g r a t o r y s p e c i e s , t h e m a r t i n summers throughout
Europe and w i n t e r s i n A f r i c a . As a c o l o n i a l
n e s t i n g s p e c i e s , i t b u i l d s mud n e s t s on t h e w a l l s
o f b u i l d i n g s . The n e s t i n g l o c a t i o n s a r e used
e a c h y e a r , o f t e n by t h e same b i r d s .
Previous s t u d i e s have i n d i c a t e d t h a t 2. u r b i c a
i s s e n s i t i v e t o a i r p o l l u t i o n . Fer iancovaMasarova and Kal ivodova ( 1965) observed changes
i n t h e s p e c i e s d i v e r s i t y o f b i r d s , i n c l u d i n g the
house m a r t i n , i n t h e a r e a o f an aluminum p l a n t i n
Czechoslovakia. Cramp and Gooders (1967)
observed a c o r r e l a t i o n with i n c r e a s e d n e s t i n g of
D . u r b i c a and a d e c r e a s e i n smoke p o l l u t i o n i n
London. A follow-up s t u d y (~ewman 1977) i n t h e
v i c i n i t y o f t h e same aluminum p l a n t s t u d i e d by
Feriancova-Masarova and Kalivodova i n 1965 showed
t h a t 2. u r b i c a decreased i t s n e s t i n g d e n s i t y with
increased a i r emissions.
--
I n 1978 d i r e c t c o u n t s o f a c t i v e n e s t s were
made i n 141 v i l l a g e s and towns l o c a t e d i n
i n d u s t r i a l i z e d (contaminated) and
n o n - i n d u s t r i a l i z e d ( c o n t r o l or. background) a r e a s .
Of t h e 141 n e s t i n g l o c a l i t i e s censused,
101 v i l l a g e s and towns were i n f l u e n c e d by a i r
e m i s s i o n s from v a r i o u s i n d u s t r i a l s o u r c e s .
Power p l a n t s and a s s o c i a t e d s u r f a c e mines,
chemical p l a n t s , l o c a l h e a t i n g p l a n t s ( c o a l
b u r n i n g ) , cement p l a n t s , and g e n e r a l urban
e m i s s i o n s s o u r c e s were t h e major a i r emission
i n f l u e n c e s . Censusing was conducted a t predetermined upwind and downwind l o c a t i o n s from an
e m i s s i o n s o u r c e . This census r e p r e s e n t e d
Records
o b s e r v a t i o n s o f over 20,000 b u i l d i n g s
were kept o f t h e number o f a c t i v e n e s t s . A
.
s t a n d a r d n e s t i n g d e n s i t y measure was d e r i v e d a s
w e l l a s measures o f t h e occupancy o f a n e s t i n g
The environmental
l o c a t i o n and colony s i z e
a t t r i b u t e s o f e a c h n e s t i n g l o c a l i t y was
c h a r a c t e r i z e d . Comparisons o f background n e s t i n g
l o c a l i t i e s were then made t o e c o l o g i c a l l y
s i m i l a r , b u t contaminated, n e s t i n g l o c a l i t i e s
.
.
The mean n e s t i n g d e n s i t y o f 2. u r b i c a from
c o n t r o l a r e a s was 0.56521.94 n e s t s per s i d e . The
r a n g e i n colony s i z e was 1 t o 33 a c t i v e n e s t s per
occupied s i d e , w i t h an average c o l o n y s i z e o f
2.721.1 a c t i v e n e s t s per occupied s i d e . The
a v e r a g e occupancy ( t h e number o f occupied s i d e s
per s u i t a b l e s i d e ) f o r t h e 32 background n e s t i n g
a r e a s was 2 1 . 0 3 . 1 p e r c e n t .
The o v e r a l l n e s t i n g d e n s i t y f o r 1.u r b i c a from
contaminated a r e a s was 0 . 3 9 3 3 . 7 3 4 a c t i v e n e s t s
per s u i t a b l e n e s t i n g s i d e . This n e s t i n g d e n s i t y
( 3 0 p e r c e n t ) was s i g n i f i c a n t l y lower
= 3.674, df = 8968) when compared t o
^0.002
background n e s t i n g s i t e s . Occupancy was o n l y
1 3 . 6 p e r c e n t . Attempts a t n e s t i n g were a l s o
l o w e r , w i t h o n l y 0.74 a t t e m p t s per contaminated
v i l l a g e compared t o 1.12 a t t e m p t s per background
v i l l a g e . Colony s i z e was s i g n i f i c a n t l y lower
(2.1+1.5 a c t i v e n e s t s per occupied s i d e ) .
-
The house m a r t i n responds a l s o t o t h e l e v e l of
a i r emissions. The o v e r a l l n e s t i n g d e n s i t y f o r
downwind l o c a t i o n s was 0.23720.378 (n = 4891)
n e s t s per s i d e compared t o 0.41521.603 (n = 1969)
n e s t s per s i d e f o r upwind l o c a l i t i e s . This
d i f f e r e n c e was s i g n i f i c a n t (P < 0.001; t = 7.263;
d f = 6808). The o v e r a l l upwind n e s t i n g d e n s i t y
was not s i g n i f i c a n t l y d i f f e r e n t from background
areas.
Colony s i z e and occupancy a l s o changed with
p r o x i m i t y t o emission s o u r c e s . Upwind colony
s i z e s averaged 2.521.0 n e s t s per occupied s i d e
compared t o 1.820.8 n e s t s per occupied s i d e f o r
downwind l o c a t i o n s . These d i f f e r e n c e s were
s i g n i f i c a n t (P < 0.001; t = 3.492 d f = 99).
Upwind occupancy (18.828.9 p e r c e n t ) was a l s o
s i g n i f i c a n t l y h i g h e r (P < 0.001, t = 5.70,
d f = 99) when compared t o downwind occupancy
(9.1+7.7
- percent).
The n e s t i n g d e n s i t y f o r downwind l o c a t i o n s
decreases s i g n i f i c a n t l y a s the distance to the
emission s o u r c e d e c r e a s e s ( t a b l e 2 ) . For upwind
locations, the c l o s e r t o the source, the higher
the nesting density; f o r increased distances,
n e s t i n g d e n s i t i e s d e c l i n e d . The upwind n e s t i n g
d e n s i t i e s c l o s e s t t o emission sources were n o t
s i g n i f i c a n t l y d i f f e r e n t from background n e s t i n g
d e n s i t i e s . Colony s i z e was lower a t a l l downwind
d i s t a n c e s , b u t o n l y s i g n i f i c a n t l y lower a t t h e
two c l o s e s t d i s t a n c e s . Occupancy was s i g n i f i c a n t l y lower f o r a l l d i s t a n c e s censused downwind.
For t h e two c l o s e s t upwind d i s t a n c e groups ( o u t
t o 6 tan) , b o t h colony s i z e and occupancy were n o t
s i g n i f i c a n t l y d i f f e r e n t from background
conditions
.
Table 2--Comparison of n e s t i n g d e n s i t y of
D.
- -u r b i c a a t v a r i o u s d i s t a n c e s upwind and
downwind from emission sources
Sample
Size
( , N ~ . of
Sides )
Locat i o n
Downwind
Upwind
Me an
Nesting
Density
Percent
D i f f e r e n c e From
Background
I
I
S i g n i f i c a n t , P < 0.025.
^ o t S i g n i f i c a n t , P<O.O5
The a i r d i s p e r s i o n p a t t e r n s a s s o c i a t e d with
t h e s t a c k h e i g h t s i n f l u e n c e d the observed
e f f e c t s . For s o u r c e s w i t h h i g h s t a c k s ( g r e a t e r t h a n
100 m e t e r s ) t h e adverse e f f e c t s on n e s t i n g were
observed i n b o t h downwind and upwind l o c a l i t i e s .
For downwind l o c a t i o n s , t h e lowest n e s t i n g
d e n s i t y d i d n o t occur c l o s e s t t o t h e emission
s o u r c e , b u t a t an i n t e r m e d i a t e d i s t a n c e ( 3 t o
6 km). Nesting d e n s i t y was s i g n i f i c a n t l y .
d e p r e s s e d out t o 12 km. For low s t a c k s o u r c e s
( l e s s t h a n 100 m e t e r s ) , t h e lowest n e s t i n g
d e n s i t y , c o l o n y s i z e , and occupancy occurred a t
t h e c l o s e s t d i s t a n c e s ( 0 t o 3 km). Average
n e s t i n g d e n s i t i e s were 20 p e r c e n t o f background.
In c o n t r a s t t o h i g h s t a c k s o u r c e s , t h e n e s t i n g
d e n s i t y i n f l u e n c e d by low s t a c k s o u r c e s was n e a r
normal a t t h e 9 . 1 t o 12 km d i s t a n c e c a t e g o r i e s .
For upwind l o c a l i t i e s , e m i s s i o n s from h i g h s t a c k
s o u r c e s have an adverse i n f l u e n c e , e s p e c i a l l y
c l o s e t o t h e s o u r c e . For low s t a c k l o c a l i t i e s ,
upwind n e s t i n g d e n s i t i e s were e i t h e r a t o r above
background l e v e l s a t a l l d i s t a n c e s censused.
When t h e house m a r t i n n e s t s i n optimum n e s t i n g
c o n d i t i o n s , such a s apartment b u i l d i n g s and
f e e d l o t s i n proximity t o water, the e f f e c t s o f
a i r e m i s s i o n s were m i t i g a t e d . The g r e a t e s t
a d v e r s e e f f e c t s on t h e n e s t i n g ecology o f
D . u r b i c a were observed surrounding power p l a n t s
and open s u r f a c e mines. Chemical p l a n t emissions
had t h e n e x t most s i g n i f i c a n t e f f e c t on the house
martin.
--
In summary, s u b l e t h a l and c h r o n i c l e v e l s o f
a i r emissions from i n d u s t r i a l s o u r c e s , such a s
power p l a n t s and chemical p l a n t s , a d v e r s e l y
a f f e c t t h e n e s t i n g ecology o f 2. u r b i c a ,
including a reduction of the nesting density,
colony s i z e , and occupancy o f t h i s s p e c i e s . The
g r e a t e s t e f f e c t s on t h e n e s t i n g p a t t e r n o f
D . u r b i c a were observed i n a r e a s downwind from
t h e emission s o u r c e s and a t d e c r e a s i n g d i s t a n c e s
from the a i r emission s o u r c e s ( f i g . 1 ) . For low
s t a c k emission s o u r c e s , g r e a t e s t e f f e c t s were
observed i n t h e immediate v i c i n i t y o f t h e s t a c k s
where the h i g h e s t emission l e v e l s a r e expected t o
o c c u r . For h i g h s t a c k s o u r c e s , g r e a t e s t e f f e c t s
were observed a t i n t e r m e d i a t e d i s t a n c e s from t h e
s t a c k s and a g r e a t e r d i s t a n c e than observed i n
low s t a c k l o c a l i t i e s .
--
Evidence s u g g e s t s t h a t w i l d l i f e p o p u l a t i o n s
l i v i n g i n optimal h a b i t a t c o n d i t i o n s a r e l e s s
a f f e c t e d by a i r emissions t h a n w i l d l i f e populat i o n s l i v i n g i n l e s s t h a n optimal c o n d i t i o n s .
T h i s o b s e r v a t i o n h a s p a r t i c u l a r importance f o r
t h e management and p r e s e r v a t i o n o f endangered
species.
O v e r a l l t h e e f f e c t s o f a i r p o l l u t a n t s on
w i l d l i f e can b e d r a m a t i c , such a s t h e d i e - o f f s ,
o r q u i t e s u b t l e , such a s s h i f t s i n t h e age
In many c a s e s t h e
s t r u c t u r e of populations.
e f f e c t s have been d e b i l i t a t i n g i n j u r i e s , o f t e n
contributing to the death of animals during
p e r i o d s o f n a t u r a l s t r e s s . A i r emissions can
a l s o reduce w i l d l i f e p o p u l a t i o n s n o t o n l y
d i r e c t l y , b u t i n d i r e c t l y through l o s s o f
habitat.
Acknowledgments:
S p e c i a l r e c o g n i t i o n i s given
t o RNDr. E l i s k a Novakova, CSc f o r c o l l a b o r a t i o n
o n t h e m a r t i n s t u d y . I wish t o thank National
Academy o f Science and t h e Czechoslovak Academy
o f Science f o r support o f t h e b i r d s t u d y and
Environmental Sc i e n c e and Engineering f o r
a s s i s t a n c e i n t h e manuscript p r e p a r a t i o n .
LITERATURE CITED
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1967. The r e t u r n of t h e house m a r t i n .
Lond. Bird Rep., No. 31:93-98.
Feriancova-Masarova, Z., and E. Kalivodova.
1965. Niekolko poznamok vplyve fluorovych
e x h a l a t o v v o k o l i H l i n i k a r n e v Z i a r i nad
Hronom na k v a n t i t u h n i e z d i a c i c h vtakov (The
e f f e c t s o f e x h a l a t i o n s from the aluminum
p l a n t i n Z i a r nad Hronom on the spectrum of
b i r d ' s p e c i e s i n t h e v i c i n i t y of t h e p l a n t ) .
B i o l o g i a ( B r a t i s l a v a ) 20: 341-346.
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