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Journal of Animal
Ecology 2000,
The role of shared parasites in the exclusion of wildlife
69, 829±840 hosts: Heterakis gallinarum in the ring-necked pheasant
and the grey partridge
D. M. TOMPKINS*, J. V. GREENMAN{, P. A. ROBERTSON{ and
P. J. HUDSON*
*Institute of Biological Sciences, University of Stirling, Stirling, FK9 4LA; {Department of Computing Science
and Mathematics, University of Stirling, Stirling, FK9 4LA; and {Central Science Laboratory, Sand Hutton,
York, YO41 1LZ, UK
Summary
1. A two-host shared-macroparasite model was parameterized from the results of
infection and transmission experiments, to investigate whether apparent competi-
tion between the ring-necked pheasant (Phasianus colchicus) and the grey partridge
(Perdix perdix), mediated via the shared nematode Heterakis gallinarum, could the-
oretically cause partridge exclusion.
2. Both the model created and the experiments conducted show that the bulk of H.
gallinarum infection to partridges, when they occur in the same locations as phea-
sants, will be from the pheasants and not from the partridges themselves. This is
due to R0 for the parasite being 123 when infecting pheasants, but only 00057
when infecting partridges. Thus, when the pheasant is present in the model the par-
tridge population is impacted by the shared parasite but, when the pheasant is
absent, the parasite is lost from the system.
3. Based on best available parameter estimates, the observed impact of H. galli-
narum on the grey partridge may be sucient to cause exclusion when the pheasant
is present in the model. This supports the hypothesis that the UK grey partridge
decline observed over the past 50 years may be partly due to apparent competition
with pheasants.
4. Habitat separation between the two host species, where it decreases the rate of
H. gallinarum transmission from the pheasant to the partridge, may allow them to
co-exist in the ®eld in the presence of the parasite. We predict, however, that grey
partridge exclusion would still occur if separation was less than 43%.
Fig. 1. Flow diagram of the basic two-host/shared-parasite model, where W denotes the number of parasite eggs in a com-
mon infective pool while, for the ith host, Pi denotes the adult parasite and Hi the host populations. See Table 1 for para-
meter de®nitions and estimates.
inverse measure of aggregation. A full list of para- where u1i K iÿ 1 and u2i (ai di)/ri. These coe-
meters is given in Table 1. cients scale the host density dependence and parasite
In terms of parasite intensity Zi Pi/Hi (M. eect terms, respectively. The transformed equations
Roberts, personal communication), the equations involve two composite parameters: (i) si (mi ai
become (for i 6 j): ai), measuring the loss of parasite intensity due to
both adult parasite and infection-induced host mor-
dHi =dt ri Hi
1 ÿ u1i Hi ÿ u2i Zi eqn 2a tality, and dilution through host births, and (ii) ei
ai/ki ÿ di, where di is the parasite-induced reduction
dZi =dt fi bi W ÿ si Zi ÿ ei Z2i eqn 2b in host fecundity. Parameter ei therefore relates
parasite-induced mortality and the reduction in
dW=dt l1 H1 Z1 l2 H2 Z2 ÿ g0 W fecundity. The relevance and stability of the point
equilibria of model equation 2(a,b,c) have been fully
ÿ b1 WH1 ÿ b2 WH2 eqn 2c discussed elsewhere (Greenman & Hudson 1999). In
Table 1. Parameter de®nitions and estimates used in the mathematical model. Empirical values for apartridge and dpartridge
have not yet been determined.
Pheasant Partridge
Parameter Symbol value value Units Source
MODEL PREDICTIONS
SPATIAL SEPARATION
parasite in a population of uninfected hosts) for H. Over the course of the infection experiment, six
gallinarum infecting pheasants is at least 100 that pheasants and four partridges were euthanased due
for the parasite infecting partridges (see Results), to husbandry problems unrelated to parasite infec-
the pheasant is indeed primarily responsible for the tion. In the remainder, the number of worm eggs
spread of infection. Therefore, an approximation of expelled was signi®cantly higher in the caecal drop-
spatial separation was modelled by simply reducing pings of pheasants than in the caecal droppings of
the rate at which the partridges were ingesting the partridges (Fig. 4); infected pheasants expelled a
nematode eggs (i.e. a 50% decline in bpartridge mean ( SE) of 3793 3117 eggs dayÿ1, whilst
mimics 50% spatial separation between the two host infected partridges expelled only 43 30 eggs dayÿ1
species). (U 6, P 002). Since no worm eggs were detected
in the caecal droppings of any of the control birds,
the average total egg production by each mature H.
gallinarum worm was estimated as 6429 in pheasants
Results and 662 in partridges.
PARASITE ESTABLISHMENT
PARASITE TRANSMISSION
Forty days after being infected, H. gallinarum inten-
sities in pheasants were signi®cantly higher than After the transmission trial, H. gallinarum intensity
those in partridges (Fig. 3). Infected pheasants were was signi®cantly higher in the exposed pheasants (U
host to a mean ( SE) of 5900 1483 worms, 135, P 004) and partridges (U 15, P 005)
whilst infected partridges were host to only 650 than in the control birds (Fig. 5). Controlling for
362 worms (Mann±Whitney U 5, P 004). Thus, background infection, the 13 000 worm eggs laid
considering that each infected host was given down in each pen resulted in infections of 15150
approximately 100 embryonated H. gallinarum eggs, mature worms per exposed pheasant and 717
0590 of the eggs given to pheasants survived to mature worms per exposed partridge. Since the
# 2000 British become mature parasites, whilst only 0065 of the mean age of maturity for H. gallinarum was esti-
Ecological Society
eggs given to partridges survived. None of the con- mated as 35 days in pheasants and 425 days in par-
Journal of Animal
Ecology, 69, trol birds of either host species contained any tridges (see Fig. 4), only those H. gallinarum eggs
829±840 worms. picked up by pheasants in the ®rst 15 days, or by
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835 culled at 100 days post-infection), parasite life expec-
D. M. Tompkins tancy was estimated as a mean of 88 days in phea-
et al. sants and a mean of 875 days in partridges (see Fig.
4).
The values obtained for H. gallinarum transmis-
sion were converted into instantaneous rates per
parasite egg by taking into account the number of
eggs to which experimental birds were exposed in
the transmission trial (13 000 per pen), adjusting for
uptake during the trial. Since the birds were main-
tained in 65 m2 pens during the transmission trial,
when they would normally occur on home ranges of
approximately 5 ha (50 000 m2; R. A. H. Draycott,
personal communication), each transmission rate
was adjusted to a realistic level by multiplying by
65 and dividing by 50 000.
Although captive work has failed to demonstrate
an impact of H. gallinarum on pheasant body condi-
tion (Tompkins et al. 1999), parasite removal experi-
ments indicate that there is an impact on their
reproductive success in the ®eld, possibly due to an
interaction with host nutrition (M. Woodburn, per-
sonal communication). A value for H. gallinarum
induced reduction in pheasant fecundity, of 828
10ÿ4 wormÿ1 yearsÿ1, was estimated from these
experiments. Host carrying capacities for wild popu-
lations were estimated from ®eld observations as six
pheasants, and three partridges, per 5 ha (R. A. H.
Fig. 4. Number of Heterakis gallinarum eggs expelled in Draycott, personal communication).
the caecal droppings of (a) pheasants (n 6 birds), and (b)
grey partridges (n 8 birds), over the 100 days following
infection with approximately 100 embryonated H. galli- MODEL PREDICTIONS
narum eggs. Mean numbers ( SE) are shown. Note the
dierent y-axis scales.
When solved for the best available parameter esti-
mates, the two-host shared-parasite model predicts
MODEL PARAMETERIZATION
# 2000 British
Ecological Society Fig. 6. Exclusion±co-existence boundary curve in the apartridge, dpartridge cross-section of parameter space for the two-host/
Journal of Animal shared parasite model. The parameters on both axes are scaled from one tenth to 10 times their empirical values. `1' denotes
Ecology, 69, co-existence of the two host species, `0' denotes exclusion of the grey partridge. The number in bold text indicates the pre-
829±840 dicted outcome at the empirically determined values.
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837 Table 2. Threshold values (and percentage change from estimated value) for the change in predicted model outcome, from
partridge exclusion to pheasant and partridge co-existence, for those parameters not directly estimated in this study to
D. M. Tompkins
which the model outcome was considered to be highly sensitive. In all cases, values were determined with all other model
et al. equation parameters kept ®xed at their estimated levels. Percentage change cannot be calculated for either apheasant or
apartridge since the estimated value of apheasant is 0, and there is no threshold value for apartridge
Sensitivity analyses were also conducted on while the other (the pheasant) is relatively unaf-
apheasant, dpheasant, and b, a and b for both host spe- fected. This is because the bulk of H. gallinarum
cies, since these were the other quantities not transmission to the pheasant is intra-speci®c, whilst
directly estimated in this study to which the model the opposite is true for the partridge.
outcome was considered to be highly sensitive. To determine the level of spatial separation
However, the model outcome of partridge exclusion between the two host species at which the model
was also relatively robust to changes in these values predicts the inter-speci®c transmission of H. galli-
(see Table 2 for a summary of all sensitivity analyses narum from the pheasant to the partridge is low
conducted). enough to allow their co-existence, the model was
ran with bpartridge set at diering levels below the
empirically determined value (558 10ÿ5 eggÿ1
SPATIAL SEPARATION hostÿ1 yearÿ1). A boundary value of bpartridge
When the model was run for each host species alone 317 10ÿ5 eggÿ1 hostÿ1 yearÿ1 was identi®ed,
with the parasite, the qualitative outcome for the below which the partridge was no longer excluded
pheasant was unchanged (remaining in co-existence from the system. This implies that spatial separation
with the parasite), while that for the partridge chan- of greater than 43% between the two host species
ged from exclusion of the host to exclusion of the will allow the grey partridge to co-exist with the
parasite. The model equilibrium, describing an unin- pheasant in the presence of H. gallinarum.
fected single host (host i) at its carrying capacity, is
stable against parasite invasion provided R0i < 1. In
Discussion
the two-host simulations, this equilibrium is not
stable against invasion by the other host if we Based on the best available parameter estimates, the
assume rj > 0 ( j 6 i). From the parameter values macroparasite model discussed in this paper predicts
listed in Table 1 we infer that the pheasant co-exists that apparent competition with the ring-necked
in equilibrium with the parasite when the partridge pheasant is sucient to cause exclusion of the grey
is absent since R0pheasant 123. The average worm partridge. This result provides strong evidence for
burden is 235 worms hostÿ1 and the pheasant popu- the view that apparent competition plays a vital role
lation is 094 birds haÿ1. The basic reproductive in determining the structure of natural communities,
number for the parasite infecting the partridge, and suggests that a population scale experiment
when the pheasant is absent, is R0partridge 00057, with pheasants and partridges could provide proof
i.e. the parasite is excluded. This shift in model out- that apparent competition mediated by shared para-
come, from partridge exclusion when the pheasant is sites occurs in the wild.
present, to parasite exclusion when the pheasant is Apparent competition is but one mechanism by
absent, demonstrates that the host exclusion pre- which shared parasites can in¯uence host popula-
dicted by the two-host shared-parasite model is tions. However, it is fundamentally dierent from
indeed due to the transmission of parasites from the all other parasite eects in that the driving force
pheasant. These single-host simulations also demon- behind host exclusion, when it occurs, is the pre-
strate how this parasite-mediated interaction sence of alternative host species and not the shared
between the pheasant and partridge is not strictly parasite per se. It is this characteristic which requires
# 2000 British apparent competition, where the presence of either demonstration if the occurrence of apparent compe-
Ecological Society
host indirectly aects the density of the other (Holt tition is to be proven. This study provides such a
Journal of Animal
Ecology, 69, 1977, 1984), but is an amensal form whereby one demonstration for the pheasant/partridge system,
829±840 host (the partridge) suers a reduction in density, con®rming that any detrimental eects of the nema-
13652656, 2000, 5, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1046/j.1365-2656.2000.00439.x by Cochrane Peru, Wiley Online Library on [28/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
838 tode H. gallinarum on wild grey partridge popula- ing apartridge alone, whilst a drop in dpartridge of 75%
Apparent tions will, indeed, be due to apparent competition is required. Secondly, as outlined earlier, even
competition with the ring-necked pheasant. Both the model cre- though the potential for partridge exclusion exists in
mediated via ated and the experiments conducted show that the this non-spatial model, habitat separation between
shared parasites bulk of H. gallinarum infections in partridges, when the two hosts in the wild may decrease the transmis-
they occur in the same locations as pheasants, will sion of H. gallinarum from pheasants to partridges
be from the pheasants and not from the partridges suciently for the two species to co-exist in the
themselves. This is due to the success rate of H. gal- parasites presence. Our prediction, based on the
linarum establishment being nine times greater in approximation of spatial separation employed in
pheasants than in partridges, and the fecundity of this study, is that partridge exclusion would still
established worms being approximately 10 times occur if separation was less than 43%. Further
greater in pheasants than in partridges. This results work, both modelling and experimental, is required
in predicted R0s of 123 for the parasite infecting to test this prediction. However, since H. gallinarum
pheasants and 00057 for the parasite infecting par- has been recorded from wild grey partridges (Clap-
tridges. Since the R0 for H. gallinarum infecting grey ham 1935; Keymer et al. 1962), and we have shown
partridges is much less than unity, the parasite can- here that the parasite cannot be maintained within a
not be maintained within partridge populations population of grey partridges alone, it is apparent
without the presence of alternative hosts. Thus, that at least some parasite transmission to this spe-
when the pheasant is present in the model the par- cies does occur from other sources in the wild.
tridge population is impacted by the shared parasite, Finally, the model outcome of partridge exclusion
but when the pheasant is absent, the parasite is lost may also be incorrect since our estimation of H. gal-
from the system. This clearly illustrates how the linarum ®tness when infecting the pheasant may be
force of H. gallinarum infection to grey partridges, too high. This estimate was based on experiments
in areas where pheasants are also present, will be with naive individuals, while evidence suggests there
from the pheasants and any resulting impact will be may be some acquired resistance to H. gallinarum
due to apparent competition. infection in the ring-necked pheasant (Lund 1967).
A potential source of error in the calculation of Inaccurate estimation of other parameters is
R0 for the parasite infecting partridges is that the H. another possible source of error in model predic-
gallinarum eggs used in the infection and transmis- tions. The greatest error may result from the manner
sion experiments were obtained from worms infect- in which values of f (parasite establishment success)
ing pheasants. Since adaptations of H. gallinarum to and b (rate of ingestion of parasite eggs by hosts)
particular host species have been previously demon- were estimated. This is not surprising, since trans-
strated (Lund, Chute & Myers 1970), our calculated mission rates are generally considered the hardest of
value of R0partridge may be an under-estimate. How- epidemiological parameters to quantify (McCallum
ever, work by Lund & Chute (1974) has shown that & Scott 1994). Experiments documented in Tomp-
this is likely not the case. In their trials, where H. kins & Hudson (1999) suggest that density depen-
gallinarum eggs for experimental infections were dence may operate to limit the success of
obtained from a mix of host species, the `reproduc- establishing H. gallinarum worms down to a maxi-
tive potential' of the parasite (number of viable eggs mum of approximately 50 worms per dose. Since
produced per embryonated egg infecting) was 243 the highest value of b obtained was only approxi-
times less when infecting grey partridges than when mately 17 eggs per day, this is unlikely to aect the
infecting pheasants. This dierence is of similar results of the transmission trial. If slight density
magnitude to that between the values of R0 calcu- dependence was operating at this level, however, our
lated in the present study (216 times less when point estimates of b would be slight under-estimates
infecting grey partridges than when infecting phea- and our model would be predicting partridge exclu-
sants). sion whilst erring on the side of caution. Another
The observed impact of H. gallinarum on the grey possibility is that our infection experiment, where
partridge appears to be sucient to cause exclusion infective doses of 100 eggs were used, may be under-
when the pheasant is present. However, this out- estimating f. However, due to the manner in which
come could be incorrect for at least three reasons. b was estimated, and the manner by which both
First, it is possible that the values for parasite- parameters are incorporated into the model, erro-
induced increase in partridge mortality (apartridge) neous estimates of f will not aect model output.
and decrease in partridge fecundity (dpartridge) used What may be causing inaccuracies in model output,
in the model, as estimated from the observed impact however, is the linear fashion by which we scaled
on body condition, are too high. The true values estimates of b from values obtained when birds were
# 2000 British may not lead to partridge exclusion. However, as exposed to known numbers of H. gallinarum eggs
Ecological Society
the sensitivity analysis shows, the predicted outcome on unrealistically small areas of ground to values
Journal of Animal
Ecology, 69, is relatively robust ± partridge and pheasant co-exis- applicable to birds on their natural home ranges.
829±840 tence cannot be bought about in the model by alter- This scaling will be highly sensitive to any inaccura-
13652656, 2000, 5, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1046/j.1365-2656.2000.00439.x by Cochrane Peru, Wiley Online Library on [28/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
839 cies in the estimates of home range size and will assistance. The manuscript was greatly improved by
D. M. Tompkins only give approximations of b, since nematode the comments of both Steve Albon and an anon-
et al. infective stages in the wild are not spread evenly ymous referee. This work was funded by NERC
over the habitat, but tend to be localized in `hot- project grant GR3/10647.
spot' areas of high use (Saunders, Tompkins & Hud-
son 1999). This uneven spread will increase rates of
H. gallinarum transmission, making partridge exclu-
sion more likely to occur in the wild than is pre-
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# 2000 British
Ecological Society
Journal of Animal
Ecology, 69,
829±840