- Email: [email protected]
Parasites, disease and the structure of ecological communities
TREE vol. I, no. 1, July
reviews
7986
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
-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)
I
Anim. Ecol. 55,85-92
IO Potts, C. R.. Tapper,
S. C. and Hudson.
P
I
(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
I
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
reviews
7986
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
-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)
I
Anim. Ecol. 55,85-92
IO Potts, C. R.. Tapper,
S. C. and Hudson.
P
I
(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
I
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