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BIODIVERSITY SERIES / SÉRIES DE BIODIVERSITÉ
The function of biodiversity in the ecology of
vector-borne zoonotic diseases
Richard S. Ostfeld and Felicia Keesing
Abstract: This is a critical evaluation of the influence of species diversity within communities of vertebrates on the
risk of human exposure to vector-borne zoonoses. Vertebrates serve as natural reservoirs of many disease agents (viral,
bacterial, protozoal) that are transmitted to humans by blood-feeding arthropod vectors. We describe the natural history
of the Lyme disease zoonosis to illustrate interactions among pathogens, vectors, vertebrate hosts, and risk to humans.
We then describe how the presence of a diverse assemblage of vertebrates can dilute the impact of the principal reser
-
voir (the white-footed mouse, Peromyscus leucopus) of Lyme disease spirochetes (Borrelia burgdorferi), thereby reduc
-
ing the disease risk to humans. Exploring the logic of what we call the dilution effect reveals four conditions that are
necessary for it to apply generally to vector-borne zoonoses: (1) the feeding habits of the vector are generalized;
(2) the pathogen is acquired by the vector from hosts (as opposed to exclusively transovarial transmission); (3) reser
-
voir competence (the ability of a particular host species to infect a vector) varies among host species; and (4) the most
competent reservoir host tends to be a community dominant, as defined by the proportion of the tick population fed by
that species. When these conditions are met, vertebrate communities with high species diversity will contain a greater
proportion of incompetent reservoir hosts that deflect vector meals away from the most competent reservoirs, thereby
reducing infection prevalence and disease risk. Incorporating the likelihood that the abundance of competent reservoirs
is reduced in more diverse communities, owing to the presence of predators and competitors, reinforces the impact of
the dilution effect on the density of infected vectors. A review of the literature reveals the generality, though not the
universality, of these conditions, which suggests that the effects of diversity on disease risk may be widespread. Issues
in need of further exploration include (i) the relative importance of diversity per se versus fluctuating numbers of par-
ticular species; (ii) the relevance of species richness versus evenness to the dilution effect; (iii) whether the dilution ef-
fect operates at both local and regional scales; and (iv) the shape of empirically determined curves relating diversity to
measures of disease risk. Further studies linking community ecology with epidemiology are warranted. 2078
Résumé : On trouvera ici une évaluation critique de l’influence de la diversité des espèces des communautés de verté
-
brés sur les risques, pour les humains, d’une exposition à des zoonoses transmises par des vecteurs. Les vertébrés sont
les réservoirs naturels de plusieurs vecteurs de maladie (virus, bactéries, protozoaires) transmis aux humains par des ar
-
thropodes hématophages. Nous décrivons ici l’histoire naturelle de la zoonose de la maladie de Lyme pour illustrer les
interactions entre les pathogènes, les vecteurs, les vertébrés hôtes et les risques pour les huma ins. Nous poursuivons
en expliquant comment la présence d’un groupe diversifié de vertébrés peut diluer l’impact du réservoir principal (la
Souris à pattes blanches, Peromyscus leucopus) des spirochètes associés à la maladie de Lyme (Borrelia burgdorferi),
diminuant par le fait même les risques de transmission de la maladie aux humains. La logique qui sous-tend l’effet de
dilution a permis de reconnaître quatre conditions nécessaires pour que cet effet s’applique de façon générale aux zoo
-
noses transmises par des vecteurs : (1) les vecteurs ont des habitudes alimentaires généralistes, (2) le pathogène passe
de l’hôte au vecteur par transmission active (par opposition à la transmission exclusivement trans-ovarienne), (3)
l’aptitude à servir de réservoir varie d’une espèce d’hôte à l’autre et (4) l’espèce hôte la plus apte à servir de réservoir
a tendance à être l’espèce dominante de la communauté, telle que définie par la proportion de la population de tiques
nourrie à même cette espèce. Lorsque ces conditions sont remplies, les communautés de vertébrés très diversifiées
contiennent une plus grande proportion d’hôtes réservoirs inaptes qui font dévier les vecteurs loin des espèces réser
-
voirs plus appropriées, ce qui limite la prévalence des infections et les risques de maladie. En tenant compte de la pro
-
babilité que l’abondance des réservoirs appropriés soit réduite dans les communautés plus diversifiées à cause de la
présence de prédateurs et de compétiteurs, on augmente l’impact de l’effet de dilution sur la densité des vecteurs infec
-
tés. Une revue de la littérature met en lumière la généralité, sinon l’universalité, de ces conditions, ce qui semble
Can. J. Zool. 78: 2061–2078 (2000) © 2000 NRC Canada
2061
Received June 19, 2000. Accepted September 21, 2000.
R.S. Ostfeld.
1
Institute of Ecosystem Studies, Box AB, 65 Sharon Turnpike, Millbrook, NY 12545, U.S.A.
F. Keesing. Department of Biology, Bard College, Annandale, NY 12504, U.S.A.
1
Author to whom all correspondence should be addressed (e-mail: Rostfeld@ecostudies.org).
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indiquer que les effets de la diversité sur les risques de maladie peuvent être répandus. Il faudra explorer davantage les
sujets suivants : (i) l’importance relative de la diversité per se par opposition à la densité fluctuante d’espèces particu
-
lières; (ii) l’influence sur l’effet de dilution de la richesse en espèces par opposition à la régularité; (iii) les limites du
champ d’opération de l’effet de dilution (à l’échelle locale ou à des échelles régionales et (iv) la forme des courbes dé
-
terminées empiriquement et reliant la diversité aux mesures des risques de maladie. D’autres études sur la relation
entre l’écologie des communautés et l’épidémiologie s’imposent.
[Traduit par la Rédaction]
Review / Synthèse
Introduction
The importance of species diversity (the number and relative
abundance of different species within an ecological commu
-
nity) in the performance of ecosystem functions, such as pri
-
mary production and resource extraction, is widely debated.
The primary experimental method used for addressing this
issue is to assemble communities of, for instance, herba
-
ceous plants or protists that differ in the number of species
which are drawn from the pool of possible species (Tilman
et al. 1996; McGrady-Steed et al. 1997; Naeem and Li 1997).
A key issue in this controversy is whether any measured
variation in ecosystem processes among the assembled com
-
munities is due to differences in species richness per se, or
to differences in the specific identity or functional roles of
the species added (Schwartz et al. 2000; Wardle et al. 1999).
Resolving this issue is important for policy and management
actions that would impact biodiversity. If species diversity
per se consistently has an impact on ecosystem processes,
then the loss of species, irrespective of their particular func-
tional roles, would be expected to affect ecosystem services
such as efficient capture of energy from sunlight or filtering
of pollutants. On the other hand, if particular functional groups
or individual species have a disproportionately large effect
on ecosystem functions, the loss of other components of the
ecological community would likely have little impact on
ecosystem services.
Consensus seems to be emerging that greater diversity in
the functional roles of species in experimental communities
leads to greater efficiency in the use of scarce resources and
increases the resilience of the community in the face of
environmental variability (e.g., drought) (Tilman et al. 1996;
Naeem and Li 1997). Similarly, high diversity within an eco
-
logical community may interfere with the ability of competi
-
tively superior species to become numerically dominant (Pimm
1991). Under such conditions, diversity begets diversity (Mayer
and Pimm 1997).
Recent studies suggest that species diversity may also be
important in the ecology of infectious diseases, particularly
vector-borne zoonoses, diseases of humans in which the dis
-
ease agent resides predominantly in a non-human animal
host and is transmitted among hosts (including humans) via
the bite of a vector, typically an arthropod. On one hand,
high species diversity in vertebrate hosts of vectors may play
a beneficial role by impeding dominance by particular spe
-
cies that act as key reservoirs of the pathogen. On the other
hand, high diversity of vertebrate hosts may provide genera
-
list vectors or pathogens with a hedge against local extinc
-
tion that would accompany the extirpation of a primary host,
and therefore may play a role in increasing the disease risk
to humans.
In this paper we address the role of species diversity in
the ecology and epidemiology of vector-borne zoonoses. We
begin by describing the natural history of one of the best
known such diseases, Lyme disease, in order to lay the foun
-
dation for a conceptual model of the role of vertebrate diver
-
sity in disease risk. We then briefly describe conceptual and
mathematical models of the dilution effect in the Lyme dis
-
ease epidemic. Four crucial assumptions of the dilution ef
-
fect are then critically analyzed in light of recent studies of a
variety of vector-borne zoonoses. We end with a general dis
-
cussion of the generality of the dilution effect.
Lyme disease and the dilution effect
Natural history of Lyme disease
Lyme disease was first described in the 1970s, when a
cluster of cases of childhood arthritis in Lyme, Connecticut,
U.S.A., was linked to tick bites and a spirochetal pathogen
subsequently named Borrelia burgdorferi. The discovery of
this spirochetal pathogen and the link to disease symptoms
associated with it led to a flurry of research designed to un-
cover the enzootic cycle both in North America and in Eu-
rope, where similar symptoms had been linked to tick bites.
Within 10 years of the initial description, a basic under-
standing of the natural history of Lyme disease had devel-
oped for foci in both eastern North America and northern
Europe.
Lyme disease is transmitted via the bite of a member of
the Ixodes ricinus complex (Acari: Ixodidae), which includes
Ixodes scapularis in eastern and central North America, Ixodes
pacificus in western North America, Ixodes ricinus in Europe,
and Ixodes persulcatus in Asia (Lane et al. 1991; Barbour
and Fish 1993; Piesman and Gray 1994). Each of these tick
species has a life cycle that includes three active stages,
larva, nymph, and adult, each of which takes a single blood
meal from a single individual before dropping off the host
and either molting to the next stage (in the case of larvae and
nymphs) or reproducing and dying (in the case of adults). Be
-
cause transovarial transmission of B. burgdorferi is highly
inefficient, the vast majority of larval ticks hatch uninfected
with the spirochete and therefore unable to infect their host
during feeding (Piesman et al. 1986; Patrican 1997a). The
larval meal represents an opportunity for the tick to acquire
an infection, which is maintained through all subsequent
molts. Larval ticks in the I. ricinus complex tend to be
highly generalized in their host selection, feeding from a
wide variety of mammalian, avian, and reptilian hosts. The
specific identity of the host of larval ticks is important in the
enzootiology of Lyme disease, because host species vary dra
-
matically in their probability of infecting a feeding larval tick.
In eastern North America, the white-footed mouse (Peromyscus
leucopus) is highly efficient at infecting feeding ticks, and is
considered the principal natural reservoir of Lyme disease
(reviewed by Giardina et al. 2000). Eastern chipmunks (Tamias
striatus) also appear to be competent reservoirs in North
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America (Slajchert et al. 1997; Schmidt and Ostfeld 2000). In
Europe and Asia, voles (Clethrionomys glareolus), mice (e.g.,
Apodemus spp.), introduced gray squirrels (Sciurus caroli
-
nensis), red squirrels (Sciurus vulgaris), and blackbirds (Turdus
merula) are competent reservoirs (Matuschka et al. 1992b,
1994; Humair and Gern 1998; Humair et al. 1998). Other
hosts, such as deer (Odocoileus virginianus and Capreolus
capreolus), lizards (Sceloporus occidentalis and Lacerta vi
-
vipara), and ovenbirds (Seiurus aurocapillus) do not transmit
B. burgdorferi to feeding ticks, and are considered incompe
-
tent reservoirs (Telford et al. 1988; Jaenson and Tälleklint
1992; Magnarelli et al. 1992; Lane and Quistad 1998).
Ticks infected during their larval meal become active about
1 year later, after they molt into infected nymphs capable of
transmitting the pathogen to their hosts. Those not infected
during their larval meal have a second opportunity to acquire
the Lyme disease pathogen during their nymphal meal. Ticks
that become infected during either their larval or their nymphal
meal will molt into an infected adult, which becomes active
between several months and >1 year later. Thus, both nymphs
and adults are capable of transmitting Lyme disease, as well
as perpetuating the enzootic cycle, when they bite a reservoir
host. The synchrony between annual peaks in activity of
nymphs and human cases of Lyme disease suggests that
most cases of Lyme disease result from transmission of the
pathogen by nymphs rather than by adults (Barbour and Fish
1993). Given the small size of nymphs of Ixodes spp. and
their tendency to reach a seasonal activity peak in summer,
when humans are most likely to enter tick habitat, it is not
surprising that the nymphal stage is most dangerous to people.
Two parameters describing the tick population are crucial
in determining the probability of human exposure to Lyme
disease within specific localities that people use domestically
or recreationally. The first is nymphal infection prevalence
(NIP) within the local population, defined as the proportion
of nymphal ticks that are infected with B. burgdorferi. NIP
will determine the probability that a given bite from a nymphal
tick will transmit Lyme disease to the human host. NIP will
be a function of the distribution of larval ticks among verte
-
brate hosts. The larger the proportion of larvae that feed
from highly competent reservoirs, the higher will be the in
-
fection prevalence in the nymphal generation. The second
parameter is the local density of infected nymphs (DIN),
which will strongly influence the probability that a person
will encounter a tick capable of transmitting Lyme disease.
DIN will be a function of both NIP and the local population
density of ticks. The density of nymphs, in turn, will be in
-
fluenced by both the distribution of ticks among vertebrate
hosts, which vary in their ability to support successful feed
-
ing by ticks, and by biotic and abiotic conditions affecting
tick survival and reproduction.
The dilution effect
Recent research has suggested that variation in the diver
-
sity of vertebrate hosts of ticks might influence the risk of
human exposure to Lyme disease as measured by either NIP
or DIN (Ostfeld and Keesing 2000; Schmidt and Ostfeld
2000). This assertion is based on the following observations
about the ecology of Lyme disease in eastern and central
North America. First, the main vector, I. scapularis, shows
little or no transovarial transmission of B. burgdorferi, there
-
fore larval ticks typically hatch free of Lyme disease bac
-
teria. Second, I. scapularis is a generalist vector: larvae and
nymphs feed from dozens of species of vertebrate hosts,
including mammals, birds, and reptiles. Third, I. scapularis
larvae acquire Lyme disease bacteria more efficiently from
white-footed mice than from other hosts. A few other hosts,
such as chipmunks and American robins (Turdus migratorius),
are competent reservoirs, but most hosts show a low proba
-
bility of infecting feeding ticks. Fourth, the white-footed
mouse is one of the most abundant and widespread of all
possible hosts for ticks, being present in both species-rich
and species-poor vertebrate communities. From these obser
-
vations, Ostfeld and Keesing (2000) argued that species-poor
vertebrate communities should be characterized by a high
relative abundance of white-footed mice, and that species-
rich communities should include a higher relative abundance
of non-mouse species that are poorer disease reservoirs. As a
result, high vertebrate diversity should dilute the impact of
white-footed mice on tick infection prevalence and conse
-
quently reduce the risk of human exposure to Lyme disease.
Schmidt and Ostfeld (2000) further analyzed the dilution
effect using both empirical and modeling approaches. First,
they found that at sites in southeastern New York State, eastern
chipmunks are highly competent reservoirs of Lyme disease,
infecting almost 70% of larval ticks that fed to repletion
from them. Chipmunks were only moderately less competent
than white-footed mice, which infected >90% of larval ticks
that fed to repletion. Second, they demonstrated that the in-
fection prevalence of questing nymphal ticks was dramati-
cally lower than would be expected if all larval meals were
taken from either mice or chipmunks. Third, using a simple
mathematical model, they postulated that at their study sites,
about 60% of larval meals must be taken from non-mouse,
non-chipmunk hosts, in order to account for the observed in-
fection prevalence of questing nymphs (38%). They inter-
preted this result as demonstrating the dilution effect at the
scale of local vertebrate assemblages. The presence of a
diverse assemblage of relatively inefficient reservoir hosts
reduces NIP.
However, Schmidt and Ostfeld (2000) noted that species
diversity in a community can be measured as the number of
species (species richness), the relative abundance of the vari
-
ous species (species evenness), or a combination of richness
and evenness, as represented by diversity indices such as the
Shannon Index (Magurran 1988). These metrics of diversity
have different implications for disease risk. Adding species
to a species-poor community without changing the absolute
abundance of the dominant species in the community may
provide the tick population with more feeding opportunities
than it would have in the absence of the added hosts. If
the added species are incompetent reservoirs, the additional
diversity would decrease NIP, but the added feeding oppor
-
tunities might simultaneously increase the total density of
nymphs. To investigate the net effects of variation in species
richness and evenness on disease risk, Schmidt and Ostfeld
(2000) used computer simulation modeling to assess the ef
-
fects of both host species richness and evenness on the den
-
sity of infected nymphs.
Schmidt and Ostfeld (2000) assembled simulated vertebrate
communities by adding between 6 and 12 species drawn ran
-
domly from a pool of potential community members to an
© 2000 NRC Canada
Review / Synthèse 2063
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© 2000 NRC Canada
2064 Can. J. Zool. Vol. 78, 2000
initial community consisting of white-footed mice and east
-
ern chipmunks. These species were assumed to have several
attributes. First, each species was assumed to have a low to
moderate fixed reservoir competence (also termed infectivity
or reservoir capacity), which is the ability of a particular
host species to infect a vector; this was assigned randomly
from a uniform distribution between 0 and 0.20. This as
-
sumption was based on characteristics of host communities
in eastern North America (reviewed by Giardina et al. 2000)
in which most hosts are weakly capable of infecting feeding
ticks. Holding reservoir competence at a fixed level for each
species was a simplifying factor that we explore further below.
Second, each species was assumed to have relative dominance
in the community, which is the product of its characteristic
population size and average tick burden. This assumption al
-
lowed us to represent species that exhibit covariation in pop
-
ulation density and average tick burden. For example, for
some larger-bodied species (e.g., raccoons, Procyon lotor),
population densities are likely to be relatively low but the
tick burden per individual is likely to be high (Fish and
Dowler 1989). Third, each species was assigned an interac
-
tion coefficient with white-footed mice (mean = 0.90, SD =
0.15), so each added species modified the relative domi
-
nance of mice. Although any given species could have either
a net antagonistic or net mutualistic effect on mice, we as-
sumed that an antagonistic effect is more likely, therefore
the mean interaction coefficient was <1.0. The effect of these
simulated species can be either a direct reduction in mouse
abundance (e.g., predation, competition) or a siphoning of
tick meals away from mice. Finally, to reflect the observa-
tion (see below) that numerically dominant members of host
communities are often, but perhaps not always, the most
competent reservoirs, we allowed the correlation between
host dominance and reservoir competence to vary. Running
the simulations with both high and low correlations between
host dominance and reservoir competence allowed us to assess
outcomes when dominance and competence are not linked.
The model showed that the effect of species richness on
disease risk is contingent on the community composition of
hosts. When neither interaction coefficients among hosts nor
correlations between community dominance and reservoir
competence were incorporated, increasing species richness
had a positive effect on DIN simply by providing more feed
-
ing opportunities for ticks. However, when we allowed addi
-
tional hosts to have a net negative impact on the abundance
of, or tick burdens on, highly competent reservoirs, increas
-
ing species richness dramatically decreased DIN and there
-
fore disease risk (Schmidt and Ostfeld 2000).
Unlocking reservoir competence
Often, reservoir competence is determined using xeno
-
diagnosis, a process in which uninfected vectors are fed on
hosts that have been either artificially (via injection) or natu
-
rally (via vector) infected with the pathogen. The reservoir
competence of field-caught hosts can be measured by de
-
termining the infection prevalence of previously uninfected
vectors that are known to have parasitized the host. When
the infection status of the host is known, field determinations
of reservoir competence can provide an ecologically realistic
estimation of the probability that a particular host species
will infect a vector in nature. Laboratory measurements of
reservoir competence, on the other hand, typically assess the
maximum value for hosts that have recently been infected.
Because the actual reservoir competence of an individual
host tends to decline with time following inoculation with
the pathogen (Levin et al. 1995; Shih et al. 1995; Lindsay et al.
1997; Markowski et al. 1998), these maximum values may
not accurately represent reservoir competence under natural
conditions. The reservoir competence of particular species
can be characterized by three different parameters: (1) a
maximum value achieved shortly after inoculation; (2) a char
-
acteristic rate of decay with time since inoculation; and (3) a
characteristic probability that repeated inoculations will re
-
turn competence values to the maximum (E.M. Schauber
and R.S. Ostfeld, in preparation). The wide variation in esti
-
mates of the reservoir competence of particular host species
(see below) may be due to failure to incorporate these three
parameters when determining competence. By specifying val
-
ues for these parameters, the reservoir competence of a host
over the course of a season of varying vector activity, or its
effective reservoir competence, can be estimated (E.M.
Schauber and R.S. Ostfeld, in preparation). Effective reser
-
voir competence is useful in assessing the net effects of par
-
ticular species on the infection prevalence of vectors.
Models of E.M. Schauber and R.S. Ostfeld (in prepara-
tion) suggest that species diversity in host communities can
influence disease risk via an additional pathway: reducing
the effective reservoir competence of each host. Imagine a
host community that is dominated by a species with a high
maximum reservoir competence, such as one with many white-
footed mice and few alternative hosts. Because the popula-
tion of larval ticks will feed predominantly on this compe-
tent reservoir, many will become infected and molt the next
year into infected nymphs. As a result of high NIP, inocula-
tion rates of both the highly competent and the less compe-
tent reservoirs will tend to be rapid, pushing the effective
reservoir competence of all hosts toward their maxima. High
effective reservoir competence will reinforce high NIP, re
-
sulting in a positive feedback loop. Now, imagine another
host-species-rich community with low maximum reservoir
competence. The same initial population of larval ticks will
have a lower average probability of feeding on a competent
reservoir, and fewer will molt the next year into infected
nymphs. As a result of the lower NIP, inoculation rates of all
hosts will be low, and larvae will be more likely to feed after
reservoir competence has decayed, resulting in low effective
reservoir competence and a positive feedback loop toward
low NIP. The model suggests that high diversity in the verte
-
brate community may reduce disease risk not only by dilut
-
ing the effects of the most competent reservoirs, but also by
reducing the reservoir competence of hosts. As we indicate
below, evaluating the veracity of this model requires further
research into the various parameters that influence effective
reservoir competence.
Generality of the dilution effect in vector-
borne zoonoses
Although Lyme disease is the most common vector-borne
disease in parts of North America and Europe (Centers for
Disease Control and Prevention 2000; Smith et al. 1998),
many other vector-borne zoonoses plague humans through
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out the world. Often these diseases are debilitating and even
lethal. It is therefore useful to assess the degree to which the
dilution effect may apply to diseases other than Lyme dis
-
ease. Four attributes are necessary for the dilution effect to
operate in a disease system: a generalist vector, a significant
role for oral (as opposed to transovarial) acquisition of the
pathogen by vectors, variation in reservoir competence among
hosts, and a positive correlation between reservoir compe
-
tence and numerical dominance of hosts in the community.
We describe these four attributes below and then explore
their likely occurrence for vector-borne zoonoses in general.
A generalist vector
Arthropod parasites vary widely in their degree of special
-
ization on hosts. For instance, for a vector-borne zoonosis to
exist, the vector must at least parasitize both a non-human
animal and a human. For zoonoses in which vectors are ex
-
treme specialists, i.e., parasitize one or a few host species,
diversity in the host community will be relatively unimpor
-
tant in determining vector abundance and infection preva
-
lence because most hosts will be irrelevant to the enzootic
cycle. Only in those cases in which variation in host diver
-
sity represents a change in feeding opportunities for the
vector will the dilution effect apply.
Oral acquisition of the pathogen
Some pathogens are transmitted across vector generations
via transovarial passage from mother to offspring. For these
zoonoses, vectors are often infected when they hatch, which
liberates them from immediate reliance on a blood meal
from a host for pathogen acquisition. Only in those cases in
which a significant proportion of pathogen acquisition by
vectors is from host meals will the dilution effect apply.
Variation in reservoir competence among hosts
If the probability of transmitting the disease agent to a
feeding vector is similar for all hosts, then variation in host
diversity is unlikely to influence the infection prevalence of
vectors because a meal from each host species will have a
similar probability of transmitting the pathogen. Only when
different host species vary in their reservoir competence will
changes in the composition of the host community influence
the disease risk.
A positive correlation between reservoir competence
and numerical dominance in the community
If the most competent reservoirs of a pathogen tend to be
rare members of their communities, they will probably be
absent from species-poor communities and present only in
species-rich communities (Davies et al. 2000). In such cases,
the disease risk will be higher in more diverse communities,
which is the opposite of the dilution effect. Only in situa
-
tions in which high species richness is accompanied by the
inclusion of species with low average reservoir competence
will the dilution effect apply.
Exploration of the necessary attributes
A generalist vector
Although comprehensive assessments of the degree to which
zoonotic vector species are selective of hosts are rare, it ap
-
pears that extreme specialists are few. For instance, some
species of mosquitoes feed largely on birds and others largely
on mammals, but most or all of these mosquitoes feed on at
least several species within each vertebrate class (Tempelis
1975). The widespread use of domestic chickens and live
-
stock as sentinels to detect mosquito-borne diseases such as
malaria, dengue fever, and various mosquito-borne encepha
-
litis viruses capitalizes on the tendency for vector mosqui
-
toes to feed on both human and non-human hosts. Indeed,
zooprophylaxis, which is related to the dilution effect, con
-
sists of using domestic animals as alternative hosts that may
deflect host-seeking mosquitoes from human hosts (Hess and
Hayes 1970). However, whereas the dilution effect is con
-
cerned with the impact of diversity of native host communi
-
ties on both abundance and infection prevalence of vectors,
zooprophylaxis is concerned with the role of domestic ani
-
mals in vector use of human hosts.
Ixodid ticks appear to vary greatly in their degree of host
generalization, from species such as Ixodes neotomae, which
attacks relatively few mammalian hosts, and not humans, to
I. scapularis and I. ricinus, which parasitize at least several
dozen host species in three vertebrate classes (Lane et al.
1991; Matuschka et al. 1992b; Kurtenbach et al. 1995; Kollars
et al. 1999). Tick vectors of the Crimean–Congo hemor
-
rhagic fever (CCHF) virus (genera Hyalomma, Rhipicephalus,
and Amblyomma) infest numerous species of wild and do-
mestic ungulates, rodents, and ground-dwelling birds (Camicas
et al. 1990; Zeller et al. 1994). Rhipicephalus sanguineus,a
tick vector of tick typhus, Rocky Mountain spotted fever, Q-
fever, Lyme disease, tularemia, and CCHF is known to para-
sitize domestic dogs, livestock, wild carnivores, ungulates,
and other mammals (Walker et al. 2000). Similarly, in the
Neotropics, several syntopic species of sand fly (genus
Lutzonyia) vectors of zoonotic cutaneous leishmaniasis (ZCL)
vary dramatically in their host specificity, but few take more
than 50% of their blood meals from any single host species
(Christensen and de Vasquez 1982). Old World sand fly (ge
-
nus Phlebotomus) vectors of ZCL are known to be attracted
to and feed on several species of native rodents and rabbits,
as well as domestic stock and pets (Schlein et al. 1984;
Johnson et al. 1993; Githure et al. 1996). Triatomine bug
vectors of Chaga’s disease feed on a wide variety of mam
-
malian and avian hosts. Zeledón et al. (1973) reported a sin
-
gle adult Triatoma dimidiata as having fed on six species of
hosts belonging to five mammalian orders. A population of
mosquitoes (Aedes albopictus) from Missouri, U.S.A., fed
from at least nine species of mammals and members of four
orders of birds (Savage et al. 1993). Tsetse fly (Glossina
spp.) vectors of African trypanosomiasis are known to feed
on dozens of species of both wild and domestic mammals
(reviewed by Milligan and Baker 1988). We conclude that
host generalization by disease vectors appears to be wide
-
spread. However, we hasten to add that, with few exceptions,
the absolute degree of host generalization by arthropod vec
-
tors, as represented by the distribution of blood meals among
hosts, is poorly understood.
Oral versus transovarial transmission of pathogens
Many pathogens have multiple routes of transmission to
vectors, including transovarial, venereal, and oral. For some
vector-borne zoonoses, especially mosquito-borne viral dis
-
eases (Table 1), transovarial transmission is relatively effi
-
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cient, leading to moderate or high infection prevalences in
newly hatched larvae produced by infected mothers. For other
vector-borne zoonoses, including many viral, bacterial, and
protozoal diseases, transovarial transmission is highly ineffi
-
cient or nonexistent, leading to low to zero infection pre
-
valences in F
1
generations produced by infected mothers
(Table 1).
When transovarial or venereal transmission is the main
route of pathogen transmission, infection prevalence of vectors
may be largely independent of the source of blood meals,
therefore the dilution effect is less likely to be a strong de
-
terminant of disease risk. Nevertheless, even for zoonoses
with efficient transovarial transmission, efficiency (defined
as the percentage of infected offspring produced by infected
mothers, sometimes called filial transmission) rarely exceeds
80%, and is often <50%. Infection prevalence in the F
2
gen
-
eration often declines dramatically from that in the F
1
gener
-
ation. If transovarial transmission were the only means of
pathogen acquisition, infection prevalence of vectors would de
-
cline exponentially with succeeding generations, leading to
the virtual loss of the pathogen in relatively few generations.
Therefore, even for zoonoses with significant vertical trans
-
mission, the distribution of blood meals among hosts is likely
to influence the infection prevalence of vectors, and there-
fore disease risk (e.g., Turell and LeDuc 1983). Further stud-
ies are warranted to compare the infection prevalence ex-
pected if transmission is exclusively transovarial with the
actual infection prevalence of vectors. This difference, the
effective degree of oral transmission, should be correlated
with the potential for the dilution effect to influence disease
risk.
Variation in reservoir competence among hosts
The reservoir competence (or infectivity) of hosts is typi-
cally assessed by means of one of three methods. First, the
proportion of vectors acquiring an infection from a blood
meal is determined using xenodiagnosis, as described above.
Second, hosts are sampled to determine whether they pos
-
sess circulating antibodies to specific pathogens, under the
assumption that demonstrated recent or current exposure to a
pathogen reflects a host’s state of infectivity to vectors. Third,
hosts are sampled for the presence of the pathogen in the
bloodstream or other tissues, under the same assumption as
for antibody tests. The latter two methods by themselves
are often unreliable because the presence of either particular
antibodies or pathogens may not accurately reflect the prob
-
ability of transmission from host to vector. For example, cir
-
culating levels of B. burgdorferi-specific immunoglobulins
in three species of wild rodents were found to be negatively
correlated with spirochete infectivity to ticks (Kurtenbach et
al. 1994). Similarly, in the case of visceral leishmaniasis,
both culture methods and polymerase chain reaction tech
-
niques demonstrated the presence of Leishmania chagasi in
individual opossums (Didelphis marsupialis) that were not
infective, as determined by xenodiagnosis (Travi et al. 1998).
Whether the presence of pathogens or antibodies specific to
those pathogens in hosts is correlated with infectivity to vectors
is rarely examined for vector-borne zoonoses (cf. Reithinger
and Davies 1999).
For nearly all vector-borne zoonoses of which we are
aware, reservoir competence appears to vary substantially
among hosts (Table 2). However, accurate determination of
reservoir competence in specific disease foci is problematic
for several reasons. First, intraspecific variation in reservoir
competence appears to be commonplace (Table 2) but the
causes of this variation are typically unknown. Second, the
burden of vectors on hosts can influence reservoir competence,
but the presence of heavy vector burdens in some cases in
-
creases, but in other cases decreases, reservoir competence
(Kurtenbach et al. 1995). Third, reservoir competence is likely
to be determined by a combination of characteristics that are
intrinsic to the host (e.g., immune response to the pathogen)
and extrinsic to the host (e.g., the relative abundance of
other hosts in the community and the abundance of vectors).
Fourth, some hosts that are incompetent reservoirs may never
-
theless infect vectors when they are simultaneously parasit
-
ized by infected and uninfected vectors (Ogden et al. 1997;
Patrican 1997b). In such cases, pathogens are transmitted
from vector to vector without being maintained or amplified
in the host (Stafford et al. 1995; Randolph 1998). Further
studies to assess the mechanisms behind both inter- and
intra-specific variation in infectivity are warranted. Such stud
-
ies would facilitate accurate determination of whether host
species have modal values of reservoir competence, and if
so, whether modal values vary substantially among species.
A positive correlation between reservoir competence and
numerical dominance in the community
Few data exist to allow this condition to be explored. Al-
though many studies of vector-borne zoonoses involve as-
sessment of the reservoir competence of various hosts, few
simultaneously assess the relative abundance of each host
species, or average parasite burdens on those hosts. Searches
for reservoir hosts of zoonotic pathogens typically focus ex-
clusively on the most abundant host species. In fact, if a host
species is not both abundant and highly infective to vectors,
it is usually ignored, under the assumption that only species
having both characteristics can be important epidemiologically.
In marked contrast, the dilution effect argues that, because
of their potential to divert meals away from highly infective
hosts, both less common species and those with low infectivity
are likely to be more important than was previously recog
-
nized.
In many endemic foci of Lyme disease in North America,
the white-footed mouse is both the most competent reservoir
and the numerically dominant member of the community of
tick hosts (Mather et al. 1989; Ostfeld 1997; Lindsay et al.
1999; Ostfeld and Keesing 2000). In Lyme disease foci in
Europe and Asia, the bank vole (Clethrionomys glareolus)
tends to be the numerically dominant tick host; in some
studies it has been found to be also the most competent res
-
ervoir (Tälleklint et al. 1993; Matuschka et al. 1994), whereas
others have found higher reservoir competence in syntopic
mice (genus Apodemus) (Matuschka et al. 1992a; Humair et
al. 1993). It is noteworthy that some European studies of
Lyme borreliosis have shown positive correlations between
average tick burden on hosts and reservoir competence of
those hosts (Matuschka et al. 1992a, 1992b, 1994; Ogden
et al. 1997). This finding is consistent with the model of
Schmidt and Ostfeld (2000), which defines host community
dominance in terms of the number of tick meals supplied by
a given host species, rather than host density per se.
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Disease Vector References
Vertical transmission <5%
California group encephalitis virus (LaCrosse virus) Aedes albopictus Tesh and Gubler 1975
Culex fatigans Tesh and Gubler 1975
Chikungunya virus Aedes aegypti Jupp et al. 1981; Mourya 1987
Aedes albopictus Zytoon et al. 1993; Mourya 1987
Aedes furcifer Jupp et al. 1981
Crimean–Congo hemorrhagic fever virus Amblyomma hebraeum Sheperd et al. 1991
Boophilus decoloratus Sheperd et al. 1991
Hyalomma dromedarii Logan et al. 1990
Hyalomma impeltatum Logan et al. 1990
Hyalomma marginatum Sheperd et al. 1991
Hyalomma truncatum Logan et al. 1989, 1990; Sheperd et al. 1991
Rhipicephalus appendiculatis Logan et al. 1989, 1990; Sheperd et al. 1991
Rhipicephalus evertsi Sheperd et al. 1991
Dengue fever virus Aedes aegypti Lee et al. 1997
Aedes albopictus Lee et al. 1997
Eastern equine encephalitis virus Culiseta melanura Morris and Srihongse 1978
Granulocytic ehrlichiosis Ixodes pacificus Ogden et al. 1998b
Ixodes ricinus Ogden et al. 1998b
Ixodes scapularis Ogden et al. 1998b
Human granulocytic ehrlichiosis Ixodes scapularis Levin et al. 1999
Lyme disease Ixodes pacificus Schoeler and Lane 1993
Ixodes ricinus Zhioua et al. 1994
Ixodes scapularis Patrican 1997a, 1997b; Levin et al. 1999
Murine typhus Xenopsylla cheopis Farhang-Azad et al. 1985
Murray Valley encephalitis Aedes aegypti Kay and Carley 1980
Rift Valley fever Aedes juppi Gargan et al. 1988
St. Louis encephalitis Culex pipiens Francy et al. 1981
Vesicular stomatitis Aedes albopictus Tesh and Gubler 1975
Culex fatigans Tesh and Gubler 1975
Lutzonyia longipalpus Tesh et al. 1987
Vertical transmission >5%
California group encephalitis virus Aedes dorsalis Turell et al. 1982
Aedes melanimon Turell et al. 1982
Keystone strain Aedes atlanticus LeDuc et al. 1975
LaCrosse virus Aedes atropalpus Freier and Beier 1984
Aedes triseriatus Woodring et al. 1998; Schopen et al. 1990;
Patrican and DeFoliart 1987
Culiseta inornata Schopen et al. 1990
Snowshoe hare virus Aedes triseriatus Schopen et al. 1990
Culiseta inornata Schopen et al. 1990
Crimean–Congo hemorrhagic fever virus Hyalomma marginatum Zeller et al. 1994
Hyalomma truncatum Wilson et al. 1991; Gonzalez et al. 1992
Jamestown Canyon virus Aedes provocans Boromisa and Grayson 1990
Aedes stimulans Boromisa and Grimstad 1986
Japanese encephalitis virus Aedes alcasidi Rosen et al. 1989
Aedes vexans Rosen et al. 1989
Armigeres flavus Rosen et al. 1989
Armigeres subalbatus Rosen et al. 1989
Culex pipiens Rosen et al. 1989
Culex quinquefasciatus Rosen et al. 1989
Culex tritaeniorhynchus Rosen et al. 1989
Powassan virus Ixodes scapularis Costero and Grayson 1996
Rift Valley fever Aedes lineatopennis Linthicum et al. 1985
Rio Grande virus Lutzonyia anthophora Endris et al. 1983
Note: Vertical transmission includes the percentages of progeny infected from known infected females and from all females.
Table 1. Selected zoonotic diseases for which vertical (i.e., transovarial or filial) transmission of the pathogen is highly inefficient
(<5%) or more efficient (>5%).
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Host
Common name Scientific name Method RC Source Location
Lyme disease
Old World field mouse Apodemus agrarius XW 58 Matuschka et al. 1992a Germany
Yellow-necked mouse Apodemus flavicollis XW 8 Humair et al. 1993 Switzerland
XW 27 Matuschka et al. 1994 Germany
XW 25 Matuschka et al. 1992a Germany
Wood mouse Apodemus sylvaticus XW 21 Humair et al. 1993 Switzerland
XW 0 Matuschka et al. 1994 Germany
XW 46 Gern et al. 1993 Switzerland
Short-tailed shrew Blarina brevicauda XW 37 Telford et al. 1990 Mass., U.S.A.
XW 37 Mather 1993 Mass., U.S.A.
Veery Catharus fuscescens XW 21 Magnarelli et al. 1992 Conn., U.S.A.
XW 43 Rand et al. 1998 Maine, U.S.A.
Bank vole Clethrionomys glareolus XW 15 Humair et al. 1993 Switzerland
XW 72 Matuschka et al. 1994 Germany
XW 39 Matuschka et al. 1992a Germany
Gray catbird Dumetella carolinensis XW 7 Anderson and Magnarelli 1984 Conn., U.S.A.
XW 3 Magnarelli et al. 1992 Conn., U.S.A.
XW 0 Mather 1993 Mass., U.S.A.
XW 10 Anderson et al. 1985 Conn., U.S.A.
Common yellowthroat Geothlypis trichas XW 17 Anderson and Magnarelli 1984 Conn., U.S.A.
XW 2 Magnarelli et al. 1992 Conn., U.S.A.
XW 24 Rand et al. 1998 Maine, U.S.A.
Worm-eating warbler Helmitheros vermivorus XW 7 Magnarelli et al. 1992 Conn., U.S.A.
Wood thrush Hylocichla mustelina XW 0 Magnarelli et al. 1992 Conn., U.S.A.
Edible dormouse Glis glis XW 95 Matuschka et al. 1994 Germany
Sand lizard Lacerta agilis XW 0 Matuschka et al. 1992a Germany
Swamp sparrow Melospiza georgiana XW 19 Anderson and Magnarelli 1984 Conn., U.S.A.
Song sparrow Melospiza melodia XW 12 Rand et al. 1998 Maine, U.S.A.
Field vole Microtus agrestis XW 0* Matuschka et al. 1994 Germany
Meadow vole Microtus pennsylvanicus XW 62 Markowski et al. 1998 R.I., U.S.A.
XW 6 Mather 1993 Mass., U.S.A.
XW 1 Mather 1993 Mass., U.S.A.
White-tailed deer Odocoileus virginianus XW 0 Mather 1993 Mass., U.S.A.
XW 1 Mather 1993 Mass., U.S.A.
XW 1 Telford et al. 1988 Mass., U.S.A.
Rice rat Oryzomys palustris XIV 76 Levin et al. 1995 Ga., U.S.A
White-footed mouse Peromyscus leucopus XIS 22 Lindsay et al. 1997 Canada
XW 25 Anderson and Magnarelli 1984 Conn., U.S.A.
XW 40 Fish and Daniels 1990 N.Y., U.S.A.
XW 46 Mather et al. 1989 Mass., U.S.A.
XW 46 Mather 1993 Mass., U.S.A.
XW 81 Mather 1993 Mass., U.S.A.
XW 76 Mather 1993 Mass., U.S.A.
XW 77 Mather 1993 R.I., U.S.A.
XW 88 Mather et al. 1989 Mass., U.S.A.
XW 83 Mather et al. 1989 Mass., U.S.A.
XW 35 Rand et al. 1998 Maine, U.S.A.
XW 91 Giardina et al. 2000 N.Y., U.S.A.
Deer mouse Peromyscus maniculatus XIV 33* Peavey and Lane 1995 Calif., U.S.A.
Pheasant Phasianus colchicus XIV 23 Kurtenbach et al. 1998 U.K.
XIS 5 Kurtenbach et al. 1998 U.K.
Eastern towhee Pipilo erythrophthalmus XW 0 Rand et al. 1998 Maine, U.S.A.
Raccoon Procyon lotor XW 0 Mather 1993 Mass., U.S.A.
Norway rat Rattus norvegicus XIV 78* Matuschka et al. 1997 Germany
Black rat Rattus rattus XIV 90* Matuschka et al. 1997 Germany
Ovenbird Seiurus aurocapillus XW 1 Magnarelli et al. 1992 Conn., U.S.A.
Table 2. Variation both within and among host species in reservoir competence (RC) for selected diseases.
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Host
Common name Scientific name Method RC Source Location
Common shrew Sorex araneus XW 10 Humair et al. 1993 Switzerland
Eastern chipmunk Tamias striatus XW 20 Mather 1993 Mass., U.S.A.
XW 20 Mather et al. 1989 Mass., U.S.A.
XW 61 Giardina et al. 2000 N.Y., U.S.A.
House wren Troglodytes aedon XW 9 Magnarelli et al. 1992 Conn., U.S.A.
Carolina wren Troglodytes carolinensis XW 16 Magnarelli et al. 1992 Conn., U.S.A.
Robin Turdus migratorius XW 0 Magnarelli et al. 1992 Conn., U.S.A.
XW 17 Rand et al. 1998 Maine, U.S.A.
Red fox Vulpes vulpes XW 13* Mather 1993 Mass., U.S.A.
Hooded warbler Wilsonia citrina XW 9 Magnarelli et al. 1992 Conn., U.S.A.
Visceral leishmaniasis
Dog Canis familiaris XWI 29 Sherlock 1996 Brazil
Opossum Didelphis marsupialis XWI 14* Sherlock 1996 Brazil
XIS 2* Travi et al. 1998 Colombia?
Human Homo sapiens XWI 15 Sherlock 1996 Brazil
Cutaneous leishmaniasis
Spiny mouse Acomys russatus PD 0 Schlein et al. 1984 Israel
Spiny mouse Acomys subspinosus PD 0 Githure et al. 1996 Kenya
Four-toed jerboa Allactaga euphratica PD 0 Saliba et al. 1994 Jordan
Grass rat Arvicanthis niloticus PD 1 Githure et al. 1996 Kenya
Cheesman’s gerbil Gerbillus cheesmani PD 0 El Sibae et al. 1993 Saudi Arabia
Wagner’s gerbil Gerbillus dasyurus PD 0 Schlein et al. 1984 Israel
Baluchistan gerbil Gerbillus nanus PD 0 Schlein et al. 1984 Israel
Greater gerbil Gerbillus pyramidum PD 0 Schlein et al. 1984 Israel
Long-eared desert hedgehog Hemiechinus auritus PD 0* Yaghoobi-Ershadi et al. 1996 Iran
Asiatic porcupine Hystrix indica PD 0* Schlein et al. 1984 Israel
Lacertid lizard Latastia longicauda PD 40 Githure et al. 1996 Kenya
Multimammate mouse Mastomys natalensis PD 1 Githure et al. 1996 Kenya
Jird Meriones crassus PD 0 Saliba et al. 1994 Jordan
PD 7 El Sibae et al. 1993 Saudi Arabia
PD 10 Schlein et al. 1984 Israel
Libyan jird Meriones libycus PD 18 Yaghoobi-Ershadi and Javidian 1996 Iran
PD 25 Yaghoobi-Ershadi et al. 1996 Iran
PD 0 Saliba et al. 1994 Jordan
PD 5 El Sibae et al. 1993 Saudi Arabia
House mouse Mus musculus PD 0* Schlein et al. 1984 Israel
Rock hyrax Procavia capensis PD 0* Schlein et al. 1984 Israel
Fat sand jird Psammomys obesus PD 23 Saliba et al. 1994 Jordan
Norway rat Rattus norvegicus PD 0* El Sibae et al. 1993 Saudi Arabia
Black rat Rattus rattus PD 0* El Sibae et al. 1993 Saudi Arabia
PD 0* Schlein et al. 1984 Israel
Great gerbil Rhombomys opimus PD 54 Yaghoobi-Ershadi and Javidian 1996 Iran
PD 32 Yaghoobi-Ershadi et al. 1996 Iran
Large naked-soled gerbil Tatera robusta PD 13 Githure et al. 1996 Kenya
Monitor lizard Varanus sp. PD 67* Githure et al. 1996 Kenya
Sand fox Vulpes ruppelli PD 0* Schlein et al. 1984 Israel
Chaga’s disease
Three-toed sloth Bradypus variegatus PD 0 Travi et al. 1994 Colombia
Dog Canis familiaris XW 41 Gürtler et al. 1993 Argentina
Two-toed sloth Choloepus hoffmani PD 0* Travi et al. 1994 Colombia
Silky anteater Cyclopes didactylus PD 0* Travi et al. 1994 Colombia
Nine-banded armadillo Dasypus novemcinctus PD 100* Travi et al. 1994 Colombia
Opossum Didelphis marsupialis PD 72 Travi et al. 1994 Colombia
Cat Felis cattus XW 28 Gürtler et al. 1993 Argentina
Table 2 (continued).
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For ZCL in Jordan, Saliba et al. (1994) found that the
fat sand rat or jird, Psammomys obesus, was both the most
abundant rodent and the most competent reservoir for
Leishmania spp. Analyzing ZCL in Iran, Yaghoobi-Ershadi
et al. (1996) found that the numerically dominant species
and most competent reservoir at one site was the Libyan jird
(Meriones libycus), but at another site was the great gerbil
(Rhombomys opimus). At a Saudi Arabian site where Meriones
crassus was captured more frequently than were Meriones
libycus or three other co-occurring rodents, M. crassus was
the most competent reservoir for ZCL (El Sibae at al. 1993).
We conclude that although the evidence for a link between
abundance and reservoir competence of hosts is suggestive
for a few zoonoses, data are insufficient for a thorough eval-
uation of this condition more generally. We expect patho-
gens that are transmitted by generalist vectors to have had
opportunities to interact, and possibly to coevolve, with mul-
tiple host species across many ecological communities. Un-
der such conditions, we expect that selection might favor
pathogen genotypes that are able to exploit the dominant
members of ecological communities, which would provide
them with the most stable “habitats” promoting persistence.
We also urge that more attention be paid to host species that
are poor or incompetent reservoirs for zoonotic agents, and
to rarer members of vertebrate communities. Such species
may provide vector populations with abundant opportunities
to feed but little opportunity for infection.
General discussion
According to the dilution-effect model, increasing the di
-
versity of the community of hosts of vectors will lead to a
greater proportion of blood meals being taken from rarer,
less competent reservoirs, resulting in lower infection preva
-
lence in the vector population (Ostfeld and Keesing 2000;
Schmidt and Ostfeld 2000). The suppressive effects of high
diversity on disease risk will be reinforced when species
added to the host community either diminish the population
density of the primary reservoir host, e.g., via predation or
competition, or reduce the absolute vector burden on the res
-
ervoir host, e.g., by diverting vector meals away from the
reservoir host to incompetent reservoirs (Schmidt and Ostfeld
2000). Moreover, the presence of alternative host species
with low reservoir competence may, by reducing encounter
rates between infected vectors and hosts, reduce the effective
reservoir competence of other host species (E.M. Schauber
and R.S. Ostfeld, in preparation). Although the dilution-effect
model was developed for Lyme disease, it may apply, in
principle, to many other vector-borne zoonoses. The four at
-
tributes necessary for the dilution effect to operate seem to
apply broadly (Table 3), but data are insufficient for a rigor
-
ous analysis of its general applicability.
Case studies?
Two recent studies of non-Lyme vector-borne zoonoses
suggest the operation of the dilution effect. In a study of
Chaga’s disease in Colombia, Travi et al. (1994) determined
that the opossum Didelphis marsupialis is the principal res-
ervoir host for the protozoal agent Trypanosoma cruzi. They
found that Chaga’s disease occurs in human settlements in
tropical dry forest but not in tropical wet forest, despite the
presence of both opossums and triatomine vectors in both ar-
eas. Travi et al. (1994) attributed the lower disease risk in
wet forest to the higher abundance of alternative, eutherian
hosts for triatomines, which may have reduced the infection
prevalence of vectors and therefore contact between infected
insects and humans. Similarly, Ogden et al. (1998a) com-
pared the infection prevalence of granulocytic Ehrlichia spp.
in ticks (I. ricinus) at two U.K. study sites that differed dra
-
matically in the diversity of vertebrate hosts. At an upland
site with abundant reservoir-competent sheep but a low di
-
versity of alternative hosts, tick infection prevalence, and
consequently disease risk for humans, was high. In contrast,
at a woodland site with abundant populations of rodents,
pheasants (Phasianus colchicus), and roe deer (Capreolus
capreolus), which are inefficient reservoirs of granulocytic
Ehrlichia spp., the infection prevalence of nymphal and adult
ticks was significantly lower.
Prospects for the future
Several key questions require resolution if the importance
and generality of the dilution effect are to be determined.
(1) To what extent is the infection prevalence of vectors de
-
termined by diversity within the entire community of
vertebrate hosts, by diversity of particular components
of the host community, or simply by population fluctua
-
tions of the most competent host(s), e.g., mice in the
case of Lyme disease?
If disease risk were related solely to the population abun
-
dance of a single reservoir host, then the dilution effect
would not operate. On the other hand, overall diversity (e.g.,
the Shannon index) within a community of hosts will decrease
whenever the most abundant species increases in absolute
© 2000 NRC Canada
2070 Can. J. Zool. Vol. 78, 2000
Host
Common name Scientific name Method RC Source Location
Brown “four-eyed” opossum Philander opossum PD 0 Travi et al. 1994 Colombia
Kinkajou Potos flavus PD 50* Travi et al. 1994 Colombia
Spiny rat Proechimys semispinosus PD 1 Travi et al. 1994 Columbia
Black rat Rattus rattus PD 6 Travi et al. 1994 Colombia
Climbing rat Tylomys mirae PD 13 Travi et al. 1994 Colombia
Note: Reservoir competence is defined as the percentage of vectors that acquire an infection during a blood meal taken from a host. It is estimated
using a variety of techniques, including xenodiagnosis of wild-caught hosts of unknown infection status (XW), wild-caught hosts known to be infected
(XWI), captive hosts infected by syringe (XIS), and captive hosts infected by vector (XIV) and by direct detection of pathogens (PD). An asterisk denotes
a study in which <10 hosts of a particular species were tested.
Table 2 (concluded).
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abundance, if the remaining species remain at constant density.
Therefore, we expect the dynamics of particular, common
hosts to covary with community diversity. Experimental stud
-
ies that separately manipulate absolute or relative abundance
of particular species and community diversity per se will fa
-
cilitate obtaining an answer to this question. In addition, multi
-
ple regression models in which abundances of single host
species and diversity metrics for the entire community are
used as independent variables should prove useful.
(2) Which metrics of species diversity will perform best as
predictors of vector infection prevalence?
Species diversity can be estimated using metrics such as spe
-
cies richness (number of species) or diversity indices, which
incorporate species richness and evenness (proportional rep
-
resentation of each species). Which metric seems most ap
-
propriate will vary according to specific features of models
linking diversity to disease risk. In a model in which ticks
passively encounter hosts in proportion to host abundance,
diversity indices that incorporate evenness would seem most
appropriate, because evenness, not richness, would capture
the probability of encounter between a passive, nonselective
vector and each species of host. In a model in which vectors
are selective of hosts, or in which host species interact (via
predation or competition), species richness would seem more
appropriate for capturing the impacts of the addition or dele-
tion of particular species.
(3) Does the dilution effect occur only at the scale of local
ecological communities, or is it important in explaining
patterns of vector infection prevalence at large geographic
scales?
Schmidt and Ostfeld (2000) demonstrated that the presence
of inefficient vertebrate reservoirs reduces tick infection prev-
alence within local ecological communities, supporting the
dilution effect model locally for Lyme disease. Ostfeld and
Keesing (2000) provided evidence that the dilution effect may
operate for Lyme disease at the scale of the eastern United
States. Further studies of both local-scale and regional-scale
interactions between host diversity and disease risk are
warranted.
(4) At broad spatial scales, can vertebrate diversity be pre
-
dicted from the degree of habitat destruction or alter
-
ation in the region?
Claims that habitat destruction and alteration affect disease
transmission are frequent but rarely demonstrated. For some
diseases, such as yellow fever, dengue fever, and African
trypanosomiasis, disturbance of natural habitats appears to
alter the behavior of vectors so that encounter rates between
vectors and humans are elevated (Walsh et al. 1993; Moly
-
neux 1997). The dilution effect suggests an alternative mecha
-
nism by which habitat alteration can influence disease risk.
Habitat destruction and the fragmentation of landscapes into
small isolated units are known to cause reduction or elimina
-
tion of some vertebrate species (Nupp and Swihart 1996,
1998; Rosenblatt et al. 1999) and therefore of diversity. Of
-
ten, the species most sensitive to such habitat destruction are
large species that occupy high trophic levels, such as raptors
and carnivorous mammals. Loss of these species, which are
rarely found to be competent reservoirs for vector-borne
zoonoses (for an exception see Reithinger and Davies 1999),
may increase disease risk both via reduction in feeding
opportunities from these incompetent hosts and via the loss
of a regulatory effect of such predators on typically more
reservoir-competent rodents.
(5) Are the curves relating diversity to disease risk linear or
curvilinear?
If disease risk, as measured by vector infection prevalence or
density of infected vectors, decreases more or less linearly
with increasing vertebrate diversity, a critical implication would
be that any loss of diversity will result in a measurable in
-
crease in disease risk. On the other hand, analyses of Lyme
disease by Ostfeld and Keesing (2000) and Schmidt and
Ostfeld (2000) suggest that the association between diversity
and disease risk is better described by a saturating function,
so changes in diversity have a strong effect only on species-
poor communities. Similar, saturating curves describing the
relationship between diversity and ecosystem function appear
to be commonplace (McGrady-Steed et al. 1997; Schwartz
et al. 2000). In such cases, the system may be more resilient
to the loss of diversity; highly diverse vertebrate communi
-
ties should be affected only modestly, if at all, by modest
losses in diversity, whereas already depauperate communities
should be affected dramatically.
Disease systems inconsistent with the dilution effect should
be sought. One likely exception to the beneficial impact of
host diversity on disease risk is the plague epizootic, in
which the pathogen (Yersinia pestis) is transmitted from non-
human mammal reservoirs to humans by several species of
fleas. Unlike most zoonotic pathogens, Y. pestis is highly
pathogenic to virtually all hosts, often causing mortality in
ca. 99% of infected individuals across a wide range of spe-
cies (Gage et al. 1995; Anderson and Williams 1997; Cully
et al. 1997). As a result of high mortality rates, plague tends
to occur as a rapidly developing epizootic that decimates
host populations and then goes locally extinct (Barnes 1993;
Anderson and Williams 1997). In this case, low diversity in
the host community appears to facilitate rapid extinction of
the plague epizootic, whereas more diverse mammal com
-
munities provide the pathogen with refugia from rapid local
extinction, maintaining its potential to infect people (R.
Parmenter, personal communication).
It is important to note that our arguments concerning the
role of diversity in disease risk are limited to diversity within
communities of vertebrate hosts and reservoirs. The effects
of variation in diversity within other components of zoonotic
disease systems are worthy of exploration in their own right.
For example, for both cutaneous and visceral leishmaniases,
a diverse assemblage of sand fly species and parasites (Leish
-
mania spp.) are involved, but the effects of vector and patho
-
gen diversity are poorly understood. Clearly, disease risk to
humans will typically be higher in geographic areas that
contain a greater diversity of pathogens and vectors, such as
the tropics, than in regions with fewer infectious agents,
which include the boreal zone.
Finally, it is worth exploring whether directly transmitted
zoonoses, in addition to vector-borne diseases, also are subject
to the dilution effect. Rodents are the reservoirs for numer
-
ous bacterial and viral diseases of humans that are transmit
-
ted by direct contact or inhalation of aerosols containing
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pathogens from urine and feces. Horizontal transmission of
these pathogens within rodent populations is associated with
intraspecific contact (Mills and Childs 1998). High diversity
within vertebrate communities may reduce rates of intra
-
specific contact either by direct reduction of population density
of primary reservoirs or by facilitating interspecific contact
at the expense of intraspecific contact.
To explore whether the dilution effect holds promise for
understanding geographic patterns in directly transmitted
rodent-borne zoonoses, we analyzed data from Kosoy et al.
© 2000 NRC Canada
2072 Can. J. Zool. Vol. 78, 2000
Disease Pathogen Vector
Viral diseases
LaCrosse virus Bunyavirus Aedes sp., Culex sp. (mosquitoes)
Rift Valley fever Bunyavirus Aedes sp., Culex sp. (mosquitoes)
Oropouche Bunyavirus Culex quinquifasciatus (mosquito), Culicoides sp. (midge)
Crimean–Congo hemorrhagic fever Bunyavirus Hyalomma sp., Rhipicephalus sp., Amblyomma sp. (ticks)
St. Louis encephalitis Flavivirus Culex sp. (mosquito)
Yellow fever Flavivirus Aedes sp., Haemogogus sp. (mosquitoes)
West Nile virus Flavivirus Culex sp. (mosquito)
Japanese encephalitis Flavivirus Culex sp., Aedes sp. (mosquitoes)
Murray Valley encephalitis Flavivirus Culex annulirostris, Aedes aegypti (mosquitoes)
Kyasanur forest disease Flavivirus Haemaphysalis sp. (tick)
Tick-borne encephalitis
c
Flavivirus Ixodes spp. and other ticks
Omsk hemorrhagic fever Flavivirus Dermacentor pictus (tick)
Equine encephalitis
Western Togavirus Culex tarsalis (mosquitoes)
Eastern Togavirus Coquillettidiea perturbans, Aedes sp., Culiseta sp.
(mosquitoes)
Venezuelan Togavirus Psorophora ferox, Culex sp., Aedes sp. (mosquitoes)
Ross River virus Togavirus Aedes sp., Cules sp. (mosquitoes)
Chikungunya virus Togavirus Aedes sp. (mosquitoes)
Sinbis virus Togavirus Culex sp. (mosquito)
Colorado tick fever Reovirus Dermacentor andersoni (tick)
Bacterial diseases
Murine typhus Rickettsia typhi Xenopsylla cheopis, Leptopsylla segnis (flies)
Rickettsial pox Rickettsia akari Liponyssoides sanguineus (mite)
Human epidemic typhus Rickettsia prowazeki Pediculus humanus (louse)
Scrub typhus Rickettsia tsutsugamushi Leptotrombidium mite
Rocky Mountain spotted fever Rickettsia rickettsia Dermacentor sp., Amblyomma sp., Rhipicephalus sp. (ticks)
Tick typhus Rickettsia sibirica Various ticks
Boutonneuse fever Rickettsia conorii Various ticks
Human ehrlichiosis Ehrlichia sp. Ixodes scapularis, Amblyomma sp. (tick)
Plague Yersinia pestis Xenopsylla sp. (flea), Amblyomma sp. (tick)
Q-fever Coxiella burnetii Various ticks
Tularemia Francisella tularensis Various ticks
Relapsing fever Borrelia hermsii Ornithodoros hermsi (tick)
Lyme disease Borrelia burgdorferi Ixodes sp. (tick)
Protozoal diseases
Human babesiosis Babesia microti Ixodes scapularis (tick)
Leishmaniasis
Visceral Leishmania spp. Phlebotomus spp. (sand flies)
Lutzonyia spp. (sand flies)
Cutaneous Leishmania spp. Phlebotomus spp. (sand flies)
Chaga’s disease Trypanosoma cruzi Rhodnius prolixus, Triatoma sp. (hemipterans)
Sleeping sickness Trypanosoma brucei Glossina spp. (flies)
Note: Pathogens and vectors are identified to genus when multiple species of a genus are involved as pathogen or vector.
a
The main vertebrate taxa from which the vector acquires the pathogen during blood meals. Because data are often incomplete or lacking, the list of taxa is
not exhaustive.
b
The main vertebrate taxa that are parasitized by the vector but that play at most a minor role as a disease reservoir.
c
Includes Louping III, Powassan virus, Russian spring–summer encephalitis.
Table 3. Pathogens, vectors, and reservoir species for key vector-borne diseases of humans.
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(1997) and Mills et al. (1998) on Bartonella spp., a bacterial
zoonosis, and the hantavirus pulmonary syndrome (HPS),
respectively. In both cases we regressed the infection preva
-
lence within entire rodent communities, as a surrogate for
disease risk to humans, against the species diversity (Shan
-
non index (base 10)) within those communities. Consistent
with expectations from the dilution effect, the overall prev
-
alence of infection with Bartonella spp. was significantly
lower in more diverse rodent assemblages (Fig. 1a). We
observed a similar pattern for HPS, although the regression
© 2000 NRC Canada
Review / Synthèse 2073
Principal reservoir hosts(s)
a
Tangential host(s),
including humans
b
References
Chipmunks, rabbits, tree squirrels Mammals (?) Johnson 1990; Woodring et al. 1996
Cattle and domestic stock Small mammals Monath 1988; Holbrook 1996
Monkeys, sloths Primates, birds, rodents Monath 1988; Holbrook 1996; Pinheiro et al. 1981
Lagomorphs, rodents Mammals, birds Monath 1988; Hoogstraal 1979; Piesman and Gage 1996
Passerines Mammals Johnson 1990; Woodring et al. 1996; Monath 1988
Monkeys Humans Woodring et al. 1996; Monath 1988, 1990; Nasci and
Miller 1996
Pigeons, crows Mammals, birds Monath 1988; Nasci and Miller 1996; Tesh 1990
Aquatic birds, pigs Water buffalo Nasci and Miller 1996; Kettle 1995; Igarashi 1994
Horses, dogs, chickens Mammals (?) Monath 1988; Kettle 1995; Doherty 1977
Rodents, shrews Monkeys, cattle Hoogstraal 1981; Kettle 1995
Insectivores, rodents, deer, grouse, songbirds Mammals, birds Hoogstraal 1981; Hayes and Wallis 1977
Muskrat, water voles Other rodents (?) Hoogstraal 1981; Kettle 1995
Passerines Mammals, horses Monath 1988; Hayes and Wallis 1977
Passerines Primates, rodents, horses,
pheasants
Monath 1988; Kettle 1995; Scott and Weaver 1989
Rodents, horses Mammals (?) Kettle 1995
Cattles, horses, kangaroos, wallabies Mammals (?) Kettle 1995; Monath 1991
Monkeys Primates (?) Nasci and Miller 1996; Kettle 1995; Monath 1991
Songbirds Mammals (?) Monath 1988, 1991; Kettle 1995
Sciurid rodents Rodents Piesman and Gage 1996; Kettle 1995
Rats Rodents Azad 1990
Mice, voles Rodents Kettle 1995; Rehacik 1979
Flying squirrels, humans Rodents (?) Piesman and Gage 1996
Rats Rodents, birds, insectivores Piesman and Gage 1996; Kettle 1995
Rodents Mammals, birds Piesman and Gage 1996; Hoogstraal 1967
Rodents Mammals, birds Hoogstraal 1967
Rodents, lagomorphs Mammals, birds Kettle 1995; Hoogstraal 1967
Rodents Mammals, birds, reptiles Desvignes and Fish 1997; Telford et al. 1996
Rodents, lagomorphs Mammals Thomas 1996; Twigg 1978
Wild and domestic ungulates, marsupials Mammals (?) Kettle 1995
Rodents, lagomorphs Mammals, birds Kettle 1995
Sciurid rodents Mammals, birds (?) Piesman and Gage 1996; Kettle 1995
Rodents Mammals, birds, reptiles Piesman and Gage 1996; Ostfeld 1997
Rodents Mammals, birds Piesman and Gage 1996
Rats, canids, badger Mammals (?) Kettle 1995; Tesh and Guzman 1996; Arias and Naiff 1981
Edentates, opossums
Rodents, hyraxes Rodents, ungulates Kettle 1995; Tesh and Guzman 1996
Rodents, armadillos, dogs Mammals, birds, reptiles Kettle 1995; Marquardt 1996
Bovids Mammals, reptiles Kettle 1995; Marquardt 1996; Molyneux 1980
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was not statistically significant (Fig. 1b). For Bartonella spp.,
an exponential decay curve fit the data better (r
2
= 0.50)
than did a linear regression (r
2
= 0.32), which suggests a sat
-
urating effect of increasing reservoir diversity on disease
risk.
Conclusions
A crucial task for scientists is to determine the ecological
consequences of the erosion of biodiversity. Some of these
consequences involve changes in the ways in which ecologi
-
cal systems capture and use resources (including pollutants),
respond to disturbances, such as drought, and resist inva
-
sions by exotic species (Schwartz et al. 2000; Levine 2000).
Some experimental and comparative studies reveal utilitarian
functions of biodiversity that are important in attaining such
desirable goals as pest or weed control, filtration of pollut
-
ants, and sustained resource extraction (e.g., Tilman et al.
1996; Daily et al. 1997). We have highlighted an additional
utilitarian benefit of biodiversity: protection of human health.
High diversity within communities of vertebrates that serve
as hosts for vectors or reservoirs for zoonotic diseases may
dilute the power of disease transmission to humans. Using
both empirical and theoretical evidence we have demon
-
strated the existence of the dilution effect for Lyme disease
in North America (Ostfeld and Keesing 2000; Schmidt and
Ostfeld 2000; E.M. Schauber and R.S. Ostfeld, in prepara
-
tion). However, many crucial aspects of the interactions be
-
tween biodiversity and zoonotic diseases remain to be
explored. Our approach in this paper has been to dissect the
logic of the dilution-effect argument and determine the fea
-
tures of disease systems that are required for the dilution ef
-
fect to operate. Our exploration of the degree to which these
features exist across the various vector-borne zoonoses sug
-
gests that the dilution effect may apply broadly. However,
such a conclusion is not definitive. Although many features
of these diseases are well understood by biomedical research
-
ers, in most cases knowledge of the key ecological variables
is incomplete or lacking. In part, the absence of relevant in
-
formation seems to result from a schism between the ways
in which epidemiologists, vector biologists, and ecologists
view infectious diseases (Rogers 1988). For instance, little ef
-
fort has been devoted to determining comprehensively the
distribution of vector meals on all members of the host com
-
munity, or assessing for these hosts the probability, under
natural conditions, that they will infect the vector. We con-
clude that the perspectives of, and expertise gained from, the
science of ecology have much to contribute to the epidemi-
ology of infectious diseases.
Acknowledgements
We are grateful to Sue Norkeliunas and Cathy Gorham for
excellent library assistance. Ken Schmidt and Eric Schauber
contributed to the development of some of the ideas and
model results reviewed herein. R.W. Ashford provided a help
-
ful review. Our research on the ecology of Lyme disease is
supported by the National Science Foundation (DEB 9615414
and DEB 9807115), the National Institutes of Health (R01
AI40076), and the Nathan Cummings Foundation. This is a
contribution to the program of the Institute of Ecosystem
Studies, Millbrook, N.Y.
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