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TREE vol. I, no. 1, July
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Pathogens and parasites are fascinating to
epidemiologists and ecologists alike; as well
as causing disease in individual species,
they can perturb the normal functioning of
a community and bus give insights into
the way that the community ‘functions’.
Several recent studies on diseases in
animal populations have confirmed the
importance of pathogens and parasites as
components of ecological systems, while
also revealing the underlying structure of
complex multispecies communities.
The importance of parasites and
pathogens as normal components
of the ecology of individual animal
species seems finally to have been
fully accepted with the appearance
parasites
and
of chapters
on
pathogens in two major new ecology textbooks’*2. These
chapters
suggest that ecologists are now
seriously considering pathogens as
factors which are commonly present in animal and plant populLike
ations.
competition
and
A. P Dobson is at the Department of Biology,
Princeton University, Princeton, N108544, USA. P. 1.
Hudson is at The Game Conservancy, Grouse Research Project, Crubenmore Lodge, Newtonmore,
Inverness-shire, PH20 IBE, UK.
Parasites,Diseaseandthe Structure
of EcologicalCommunities
A. P. Dobson and P. J. Hudson
predation, parasites are now seen
to operate in a density-dependent
manner and thus may serve to
regulate the density of a species.
This contrasts with the more traditional view of pathogens, which
tended to consider them to operate infrequently
in a more random,
density-independent
manner.
Roy Anderson and Robert May3,4
have suggested that parasites can
be divided into two broad classes:
the microparasites (viruses, bacteria and protozoa) and the macroparasites
(helminths
and other
metazoa). It is possible to compare
parasitism
with competition
and
predation, in a way that resembles
the artificial distinctions between rand K-selected species5,6. Table 1
crudely attempts this comparison
by suggesting several properties of
interspecific
interactions
these
along an artificial spectrum from
microparasite to predator. Although
the comparison is coarse, the parameters which are most important
in determining
the dynamic properties
of simple
mathematical
models of such systems tend to
vary systematically in the way suggested by Table
I ‘.3f4. Thus, in
most models of parasite-host
systems we would expect the parasite
population to be characterized by
higher intrinsic growth rates than
that of its host, while in predatorprey relationships the victim usually has the higher intrinsic growth
rate. Similarly, while one or more
parasite species may live in one
host speciesa, a predator usually
uses several different prey species
to complete its own development.
The introduction
or elimination
of a parasite may affect the interactions between a whole range of
species in the community. The rest
of this article considers three recent studies where the action of
pathogens and the diseases they
cause have been shown to be
important. The first example illustrates how a pathogen may become
TableI. Comparisonof somelife histoy characteristicsof macmand mictuparaslteswith thoseof other interspecificregulatory
agents”
Life history
characteristic
Ratio of mean
expected
lifespanb
Microparasite
Macroparasite
Parasitoid
Competitor
Predator
<l
<l
-1
-1
>1
Ratio of body sizes
much smaller than
hosts
smaller than hosts
mature stages
similar
similar size
larger than prey
Intrinsic growth rate
of population
much faster than
hosts
faster than hosts
comparable but
slightly slower
similar or almost
identical
usually slower than
Interaction with host
individuals in
natural
populations
one host usually
supports several
populations of
different species
one host supports a
few to many
individuals of
different species
one host can
support several
individuals
individuals reduce
the proportion of
available
resources
many prey items are
needed to feed
each predator
Effect of the
interaction on the
host individual
mildly to fairly
deleterious
variable; not too
virulent to
definitive, can be
intermediate
eventuallyfatal
not usually fatal
usually immediately
fatal
Ratio between
numbers of
species at the
population level
many species of
parasite within
each host
individual
many species of
parasite from
each host
population
most hosts harbour
one or
occasionally
several
parasitoids
several species may
utilize one
common
resource
each predator uses
several prey
species
Degree of overlap of
the two species
ranges
occur as diffuse foci
throughout
host’s range
occur as diffuse foci
throughout
host’s range
usually present
throughout
host’s range
ranges overlap dut
usually not
entirely
range is usually
greater than
prey’s
a Adapted from Ref. 7, chapter I.
bAll ratios expressed as exploiter/victim.
prev
50
r
R
76 77
Fig.
I. The
moors
decline
ldotsl
reported
78
79
130 81 a2
of grouse
on the
and the number
in sheep
by ministry
North
of cases
vets
Yorkshire
of louping
ill
Ibarsl.
important
when interactions
between other species make conditions favourable for its establishment. The second shows how a
pathogen
may
determine
the
abundance and structure of a community of species, and the third
examines the reverberations which
may run through a complex community once a pathogen is artificially controlled or eliminated.
Ticks and loupingill virus In red grouse
Recent studies on the red grouse
(Lagopus lagopusscoticus)in the north
of England have demonstrated that
the parasitic nematode Trichostongyle tenuis reduces the breeding
production
of grouse’ and can
account for the observed
shortcyclic patterns
of
host
time
Fig. 2. A grouse
at the
grouse
12
chick carrying
base of the
bill.
Inset.
a low infestation
an adult
sheep
of ticks;
tick;
only
abundance”,’ ‘. In some areas there
has been a longer term decline in
grouse density
(Fig. I), due to
another factor, namely an increase
in the prevalence of the tick borne
virus, louping ill12. The virus is
normally found in sheep but the
nymph stage of the tick will transmit the disease to the highly susceptible grouse chicksI
(Fig. 21.
The increase in the incidence of the
disease
appears to have been
caused by a change in the competitive
interaction
of two plant
species in the moorland community: heather (Calluna wulgarisl, on
which the grouse depend as their
major food source; and bracken
(Pteridium aquilinum). that provides a
humid mat layer and a suitable
habitat for ticks14. In the past,
bracken was restricted to the edges
of the moorland, where it was carefully managed and harvested as
bedding for livestock. Now cutting
has stopped, and the bracken has
started to spread; in some moorland areas it is replacing heather at
a rate of I% per annum. Mature
heather resists invasion but is tra-
note the tick at the front
the
immature
stages
of the eye and another
of the tick are found
on
ditionally burned to provide young
nutritious shoots for the grouse and
sheep. The burning reduces the
competitive ability of the heather
and allows the bracken, with its
fast-growing rhizome system, to colonize and replace it. Bracken provides a better habitat for the ticks
than heather, and it is suggested
that the spread of the bracken has
increased the exposure of grouse to
louping ill and led to the fail in
grouse densities.
Current
models
indicate
that
since louping ill is so pathogenic
the grouse population cannot maintain the virus without the presence
of sheep, the only other host to
produce
a viraemic
response.
Theoretically, the vaccination of the
sheep should eliminate the disease and lead to the return of the
grouse.
In some areas the loss of grouse
has resulted in a fall in sporting
revenue and land values, so tracts
of moorland habitat have been sold
for commercial afforestation.
The
replacement of moorland by sitka
spruce and lodgepole pine results
in the
total
disappearance
of
grouse and other specialized upland animals valued by conservationists.
Avianmalaria and the structureof
Hawaiian land bird communities
A large proportion
(over twothirds) of the endemic bird species
of the Hawaiian islands have become extinct since their discovery
by Captain Cook in 1778 (Ref. 151. A
recent study” on the birds of these
islands has elegantly confirmed an
earlier hypothesis that introduced
avian malaria is a major determinant of the present distributions
and
abundances
of
native
bird
species on these islands. WarnerI
originally suggested that the presence of avian malaria was restricting the remaining endemic species
of Hawaiian land birds to mountain
tops higher than 600 metres, above
which the mosquito vector of the
pathogen, C&x quinquefasciutus,was
rarely found. The new experiments
on Plasmodium relicturn capistranoae”
have confirmed the ability of avian
malaria to act as a barrier to the
movement of the native bird species. When
individuals
of these
species are challenged with the
malaria, their
resistance
to the
pathogen is directly proportional to
TREE vol. I, no. 1, July
1986
10.0 -
:’ ‘...y.dors
0
0
7.5 -:.
...
0
O
malaria
o’parasitemias
0
??
??
0
??
0
??
??
Relative
:
O O O Q,,o
their present day abundance on
0
‘--._
native bird
0
0
.’
the islands. Thus species such as abundance
species
‘
.
o
0.
the Laysan finch (Telespgza cantons),
5.0 - o” \
which lives on a mosquito-free
iso introduced
“.
b
..)l
??
bird species
land and therefore has never been
0
0
0
o’..
0
.
exposed
to malaria, completely
2.5 0
lack any natural resistance to the
Q.0
o
O
..
() o
disease. Challenged birds always
??
. O o”o
0
“...O
??
‘.....
oooo
develop high parasitemias and all
‘...,.
10.
.
10
I
individuals die within two to three
1350
0
450
900
1800
weeks.
In
contrast,
introduced
species tend to be resistant or only
Altitude
(metres)
to produce low parasitemias when
Fig. 3. Schematic representation of the relative densities of native and introduced bird species Icircles)
with
challenged
malaria,
and
at different altitudes on Mauna Loa in the Hawaiian Islands. Also illustrated are the relative densities of
deaths are less common.
the insect vector of avian malaria (dots1 and the rates of infection (stars1 of avian host species with
malaria. The scales of abundance are arbitrary but coarsely relative within each group.
In surveys of birds at regular
altitudinal
intervals,
the highest
in
attempts
to
eradicate
the
prevalences
of malaria infection
Rinderpest virus in the Serengeti
were observed in the zone where
A final
example
of how a disease27,24. This has led to a corresponding
decline in the prevavector and native bird distributions
pathogen may act as an unseen but
overlap (Fig. 3). Charles van Riper”
important component of an ecol- lence of the disease in the wild
proposes that a bimodal extinction
ogical community
occurs in the
ungulates. A primary result is that
process is responsible for this preclassic ‘predator-prey’
system of the numbers of several species of
sent distribution.
The earlier losses
ungulate have increased spectaculthe Serengeti. Here the elimination
arly over the last 20 years: wildeof species from the lower altitudes
of a disease has allowed a natural
beest have increased from 0.25 milwere mainly due to the impact of
experiment,
during
the
course
lion to 1.4 million25, while buffalo
of which
some
the agricultural
practices of the
species
have
(Sgncerus caffer) showed an initial
settlers on these islands from the
increased,
others
have
while
increase26 from 30 000 to 75000.
12th to the 19th centuries. Addiapparently declined. A variety of
Zebra (Equus burchelli), in contrast,
tional factors were the introduction
studies have emphasized the imhave maintained
a fairly steady
of rats and mongooses,
which
portance of grazing facilitation’8~‘9
population
density
over
this
and predation20,2’ as major factors
preyed
on the very accessible
period25. Recent studies2’
have
nests of the now extinct lowland
in determining the interspecific inspecies, and the presence of feral
suggested that predation may be
teractions
between the different
ungulates, which ate many of their
more important than either comlarge vertebrate
species in this
food plants15. Although the mospetition
or grazing facilitation
in
ecosystem. In addition, as early as
quito, C. quinquefasciutus, was introdetermining the zebra numbers.
the 1960s Talbot and Talbot”
had
duced in 1826 and rapidly spread
The increase in prey density is
demonstrated that although - 36%
amongst the islands, there were no
of young wildebeest
(Connochaetes matched by an increase in numbers
cases of avian malaria detected in
by some predators
in the ecotaurinus) were killed by predators,
surveys of bird blood in the early
system; the number of lions has
- 48% were dying from infections
20th century. However, many spealmost doubled and the number of
with ‘yearling disease’ or rinderpest
cies of birds were introduced to the
hyaenas increased by 50% (Ref. 21 I.
(a virus which is essentially
the
islands between 1900 and 1930 in
equivalent of human measles). As
However, there has been a serious
an attempt to repair the damage
decline in the numbers of hunting
this pathogen is also a major cause
caused by agricultural practices in
of mortality
in cattle in Africa, a dogs (Lgcaon pictus) in the area (Figs
the lowlands. An organization, the
number
of
vaccination
4 and 51. This decline may be due
large
Hui Manu, existed solely for the
to an increase in mortalities due to
schemes have been implemented
purpose of introducing exotic birds
to Hawaii. It seems likely that one
loo Q., % Wildebeest and
2
1.. Buffalo with
or more of these species was
Wildebeest
s
“-.e.. Rlnderoest
x106
responsible
for introducing
P. r.
% indi”i&a,s 75
numbers of
capistranoaeinto the islands. As the
,:’
individuals
with
introduced species became estabI
.:’
, in Serengetl
Rinderpest so
lished and moved from the lower
‘A,.
..‘.
‘.(, _:’
National Park
antibody
parts of the island to higher elev,,.,..
.:::Y.,_ *
ations, they were able to introduce
1
.,.....J
25
malaria to the endemic species
in
areas where suitable vectors were
t
present. The remaining
endemic
I
I
1
species are now restricted to the
1976
1983
1962
1969
1955
mountain tops where vector densiFig. 4. The numbers of wildebeesP (dots and error bars1 and hunting dog? (open triangles) in the
ties are low and few introduced
Serengeti. Also illustrated are the percentage of wildebeest and buffalo with antibodies to rinderpesP
species are present as carriers of
(circles and diamonds). The left scale gives the prevalence of infection. The right scale shows the
the pathogen.
density of wildebeest and wild dogs.
I
ii
13
TREE vol. I, no. 1, July 1986
ious implications
for conservation
and management. However, in each
case the presence of the pathogen
was only confirmed after its effects
had been studied in some detail.
Molecular biologists and immunologists are developing many new
techniques for detecting the presence of pathogens
in infected
hosts, and collaboration with ecologists should permit routine studies of the effects of parasites in
other ecological communities.
kknowkdgements
We would
many
like
helpful
to thank
unpublished
material:
S. I. McNaughton,
van Riper
the
discussions
following
or for
J. Ginsberg,
for
access
to
R. M. May,
A. M. Lyles, W. Plowright,
Ill. P. Rossiter.
A. R. E. Sinclair
C.
and
C. A. Toft.
Fig. 5. A family of hunting
dogs ILycaon pictus). Photograph
canine distemper, a disease quite
closely related to rinderpest. At the
conclusion
of the last detailed
study of hunting dogs in 1977 (Ref.
281, no pups had been successfully
reared to age one for over two
years. This suggests that the presence of rinderpest in the Serengeti
may have been advantageous to
the wild dogs, either by increasing
the susceptibility
of their prey to
predation, or by continually exposing them to pathogens which may
be antigenically similar to canine
distemper. The latter effect might
stimulate production of antibodies
in the hunting dogs, which would
enhance their immunological ability to resist infection by canine distemper, although the evidence for
cross-immunity
between
canine
distemper
and rinderpest
is still
equivoca129. While somewhat speculative, this is a useful anecdotal
example of how the interactions
between the more obvious species
in a community may be mediated
by the presence
of organisms
whose influence is not always apparent until the ecosystem is perturbed by man.
Following
relaxation of vaccination rates of domestic cattle in
areas around the Serengeti in the
last few years, there have been
several outbreaks of rinderpest
in
the game reserve. The major outbreak seems to have been restricted to buffalo in the northern
region of the Serengeti
National
Park in Tanzania, adjacent to the
Masai
Mara Game Reserve
in
Kenya3’. Although evidence from
14
by joshua
Ginsberg.
serological studies of buffalo in the
neighbouring Masai Mara region of
Kenya suggest that the viral strain
may be fairly mild (P. Rossiter, pers.
commun.), the containment of the
outbreak to a restricted area may
be due to an ‘unnatural’ experiment of a type increasingly familiar
to ecologists working in tropical
areas. The most recent survey of
buffalo numbers in this section of
the reserve
suggested
that the
levels of poaching of buffalo are
now so high that the population has
been reduced to around 15-25% of
its level in 1970 (Ref. 30). It is
conceivable that the population
densities
of buffalo in the area
where the outbreak occurred were
below the threshold density necessary to sustain an outbreak3,4,7.
As the Serengeti remains one of
the most spectacular wildlife concentrations
on earth,
it seems
sensible to recommend that vaccination rates of cattle in surrounding areas be stepped up. This will
not only prevent the virus from
being introduced to wild animals,
but might also be used as a political lever to encourage poachers to
concentrate on rearing their own
cattle, rather than capitalizing on
the shortages of domestic protein
in Tanzania by taking animals from
the wild.
Conclusion
These examples illustrate
how
parasites
and
pathogens
form
the
important
components
in
structure
of ecological communities, and how they may have ser-
References
I
( 1985)
Toft. C. A.
(Diamond.
in Community
463. Haroer
pp. 445-
& Row
2 Begon: M., Harper,
II9861
Ecology
I, edsl,
1. and Case, T.
I. L. and Townsend.
Ecology: Individuals, Pop&lions
C. R
and
Communities. Sinauer
3 Anderson,
R. M. and May, R. M. (19791
Nature 280.361-367
4 May, R. M. and Anderson,
R. M
( I9791
Nature 280.455-461
5 MacArthur,
R. H. and Wilson,
E. 0. II9671
Tke Theory 01 Island Biogeography, Princeton
University
Press
6 Parry, C. D. I1981 ) Oecologia 48,26&264
7 Anderson,
R. M. and May, R. M.. eds
(I9821
Tke Population Biology of Infectious Diseases,
Dahlem
Workshop
No 25, SpringerVerlag
8 Dobson.
A. P 119851 Parasitology 91,3 17-348
9 Hudson.
P. I. 11986)
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Anim. Ecol. 55,85-92
IO Potts, C. R.. Tapper,
S. C. and Hudson.
P
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(19841 I. Anim. Ecol. 53.21-36
I I Hudson.
D.
I I9851
P. I., Dobson.
Interactions IRollinson.
edsl,
A. P. and Newborn,
in Ecology and Cenelits of Host-Parasite
pp. 79-89,
I2 Hudson.
D. and Anderson,
Academic
P. I. II9861
and Management
R. M..
Press
Red Grouse: The Biology
ofa Wild
Camebird. Game
Conservancy
I3 Duncan,
1. S, Reid,
1. D. P. and Watson,
H. W, Moss, R.. Philips.
A. II9781
I. Wildl. Manage.
42,500-505
I4 Hudson.
P. I II9861
and Taylor.
I. A., edsl.
I5 Moulton.
M. P.and
in Bracken (Smith.
Parthenon
Pimm.
R. T
Press
S. L. (I9831
Am.
Nal. I2 I, 669-690
16 van Riper,
C.. Ill, van Riper,
S. C.. Gaff. M.
i
L. and Laird. M. 1986) Erol. Monogr. (in press)
I7 Warner, R. E. (1968) Condor 70. 101-120
I8 Vesey-Fitzgerald.
D. F. (I9601
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Mammal.
41, 161-170
I9 McNaughton,
259-294
20 Schaller,
Chicaeo
S. I. (1985)
C 6 11972) The Serengell Lion.
Universitv
21 S&air.
Press
A. R. Eland
Norton-Griffiths.
ofan
( 1979) Serengeti. Dynamia
Chicago
22 Talbot,
Etol. Monogr. 55.
University
M.
Ecosystem,
Press
L. M. and Talbot,
M H II9631
Wddl.
Monogr. 12, l-88
23 Plowright.
50, l-28
W. (I9821
Symp. Zool Ser. LDndon
TREE’vol.
7, no. 7, July
24 Plowright.
W. II9851
1986
Ann.
Med. Vet. 129,
9-32
25 Sinclair,
A. R. E.and
Norton-Griffith%
M.
f 1982) Oecologia 53,364-369
26 Sinclair.
A. R. 6. (1977)
Buffalo,
The industry of man has led to
changes in the chemical climate
of many nations in the northern
hemisphere. Ozone f03) is an example of a gaseous pollutant dispersed over much of the United
States, Britain, and Central Europe.
Studies with a wide range of crop
species’, as well as with native
plants
and trees*, suggest that
ambient O3 levels suppress plant
growth and development. Gaseous
pollutants
such as sulfur dioxide
(SO*), oxides of nitrogen (NO,), and
other
chemicals
from
anthropogenic sources, are also deposited in rain, snows, and fog, often
with biological consequences for
plants. Research over the past 80
years has shown the magnitude of
crop losses due to air pollutants.
More recently, research has focused on trees and forest because of
concern that air pollutants are contributing
to excessive
mortality,
suppressed
growth, reproductive
failure and reduced vigor in forest
stands throughout
eastern North
America, California, and parts of
Germany (Fig. I L
Studies
on the
physiological
mechanisms
which
underlie
air
William Winner and Christopher Atkinson are at the
laboratory for Air Pollution Impact to Agriculture
and Forestry, Department of Plant Pathology,
Physiology, and Weed Science,Virginia Polytechnic
Institute and State University, Blacksburg, VA
2406 I, USA.
Elsevler
29 Plowright.
899-918
30 Sinclair,
28 Frame,
The Afrian
There is now great concern that air pollutants (especially sulfur dioxide, owne, and
oxides of nitrogen) can after tire p6ysiological processesof plants, thereby affecting
patterns of growth. Air pollutants cause
damage to leaf cuticles and affect stomata1
condudance.They can also have direct
effects on photosynthetic
systems, leaf
longevity, and patterns of c&on allocation
within plants. Pollutants
interact with
other environmental factors, and may after
plant-environment
relationships on a regional scale. In this article, Winner and
Atkinson summarize current knowledge of
the effects of air pollutants on plant growth
and physiology, and indicate the new
directions of research now under way in
North America and Europe.
@1986.
Chicago University Press
27 Sinclair, A. R. E. (I 985) 1. Ania. Ecol. 54,
sc,encePubilshers
6
v
Amsterdam
L. H., Malcolm,
and Lawick,
1. R., Frame,
G. W.
H. V. 11979) Z. Tierpsythol. 50.
225-249
Report
W. 11968) Virol. Monogr. 3.25-l
A. R. E. and Dublin.
to Tanzania
National
IO
H. 119851
Parks, lanuary
I985
Absorptionof Air Pollutionby Plants,
andConsequences
fur Growth
William E. Winner and Christopher J. Atkinson
pollution-caused
changes in plant
growth are taking on new importance. They have helped to clarify
the role of stomata and cuticles in
regulating pollutant absorption by
leaves and to establish a causeeffect
relationship
between
air
pollution deposition and plant response. Carbon allocation and leaf
longevity are also now recognized
as important
links
between air
pollution-caused changes in photosynthesis and growth. Environmental factors which alter conductance
and growth pattern can also alter
physiological response of plants to
air pollutants.
It appears that regional deposition of air pollutants
may change plant-environment
relationships by influencing both the
water use efficiency and the energy
balance of plants.
Air Pollution Uptake by Leaves
The leaf cuticle is an effective
Fig. 1. This
deposition
difficult
0169%5347/66/$0
spruce-fir
stand at Mt. Mitchell,
North
may be contributing
to the excessive
to prove.
200
barrier to CO2 and Hz0 exchange,
and is thought to be a barrier
to absorption
of air pollutants4.
Gaseous pollutants and acidic precipitation
may reduce cuticular
integrity,
leading to appreciable
cuticular conductance of ions between depositions on leaf surfaces
and cytoplasmic
solutions5.
Pollutionxaused
reductions in the integrity of the cuticle may account,
in part, for the large differences
between
rainfall
and throughfall
chemistry observed in deciduous’
and evergreen’ forest canopies. In
general, throughfall from deciduous
canopies is lower in hydrogen ion
and nitrogen
concentration
than
rainfall, and may be enriched in
potassium. In contrast, throughfall
from coniferous canopies is often
more acidic than rainfall. Analysis
of ionic movement between leaf
mesophyll
and precipitation
requires a better understanding
of
Photograph
Carolina
is in a rapid state of change. Air pollution
mortality
and crown thinning,
but this has been
by Dr 1. Eisenbach.
15