Tompkins DM, Dickson G, Hudson PJ (1999) Parasite-mediated competition

between pheasant and grey partridge: a preliminary investigation. Oecologia,

119:378-382

Rezumat
Exemplare de fazan (Phasianus colchicus) și potârniche (Perdix perdix) au fost ținuți
împreună într-un loc cunoscut a fi contaminat cu ouăle nematodei Heterakis gallinarum
pentru a examina ipoteza că acest parazit comun are un impact mai mare asupra
potârnichii decât asupra fazanului. Am detectat o relație negativă între numărul
viermilor și condiția fizică a potârniche, iar această relație lipsea la fazan. Mai mult de
atât, nu a existat o corelare între intensitatea viermilor după perioada de expunere și
masa corporală înainte de infectare a potârniche, deci concluzia este că înrăutățirea
condiției fizice a fost direct cauzată de vierme. În concordanță cu observațiile anterioare
despre H. gallinarum, fecunditatea și supraviețuirea este mai mare la fazani decât la
potârniche, sursa paraziților fiind fazanii crescuți și eliberați. Diferența impactul asupra
stării organismului gazdă, susține ipoteza creșterea numărului de fazani eliberați din
crescătorii crește răspândirea de paraziți, ceea ce a contribuit la declinul populațiilor de
potârniche în Marea Britanie în ultimii 50 de ani.

Tompkins DM, Greenman JV, Robertson PA, Hudson PJ (2000) The role of shared
parasites in the exclusion of wildlife hosts: Heterakis gallinarum in the ring-
necked pheasant and the grey partridge. Journal of Animal Ecology, 69:829-840

Rezumat
1. Un model macroparazit comun cu două gazde a fost parametrizat din rezultatele de
infecție și transmitere, pentru a investiga dacă concurența aparentă dintre fazan
(Phasianus colchicus) și potârniche (Perdix perdix), mediată prin intermediul
nematodului comun Heterakis gallinarum, poate duce sau nu la eradicarea celei din urmă.
2. Atât modelul creat cât și experimentele efectuate arată că cea mai mare parte a infecției
cu H. gallinarum la potârnichi, atunci când acestea apar în aceleași locații ca fazanii, sunt
cauzate de către fazani și nu de potârnichi. Rata de femele de paraziți la fazani fiind 1,23,
iar la potârniche doar 0,0057. Astfel, atunci când fazanul este prezent în model, populația
de potârniche este afectată de parazitul comun, dar atunci când fazanul este absent,
parazitul este pierdut din sistem.
3. Pe baza celor mai bune estimări ale parametrilor disponibili, impactul observat al H.
gallinarum asupra potârnichii, poate provoca excluziunea speciei atunci când fazanul este
prezent în model. Acest lucru susține ipoteza că în Marea Britanie declinul populațional
puternic al potârnichii, observat în ultimii 50 de ani, poate fi parțial determinat de
concurența aparentă cu fazani.
4. Separarea habitatelor între cele două specii gazdă, unde scade rata de transmitere a H.
gallinarum de la fazan la potârniche, poate permite coexistența acestor două specii în
ciuda prezenței paraziților în sistem. Cu toate acestea, anticipăm că excluderea totală a
potârnichii avea loc dacă separarea este mai mica de 43%.

Tompkins DM, Greenman JV, Hudson PJ (2001) Differential impact of a shared

nematode parasite on two gamebird hosts: implications for apparent competition.
Parasitology, 122:187-193.

Rezumat:
Dacă efectele dăunătoare ale paraziților non-specifici sunt mai mari la speciile gazdă
vulnerabile decât la speciile gazdă rezervor, atunci excluderea gazdei vulnerabile prin
concurența aparentă este mai probabilă. Dovezile sugerează că un astfel de mecanism
apare în interacțiunile dintre fazanii (Phasianus colchicus), potârnichea (Perdix perdix) și
parazitul lor comun, Heterakis gallinarum. Modelarea sistemului prezice că impactul
redus al parazitului asupra fazanului comparativ cu impactul asupra potârnichii, are ca
rezultat excluderea de potârnichii din zonele populate de fazani. Întrucât impactul
parazitului este estimat în prezent din activitatea corelațională, au fost efectuate infecții
controlate pentru a compara experimental impactul H. gallinarum asupra celor două
gazde și a verifica relația dintre cauză și efect. În timp ce potârnichile infectate au
manifestat pierdere de greutate, consum redus de alimente și deficiențe cecalice, impactul
parazitului asupra fazanilor infectați a fost redus la deficiențe cecalice.
Impactul parazitului H. gallinarum pe exemplarele de potârniche infectate este în
conformitate cu datele corelaționale anterioare, susținând predicția că o concurență
aparentă mediată de paraziți cu fazanii poate avea ca rezultat dispariția potârnichii. Cu
toate acestea, scăderea observată în activitatea cecală a fazanilor provocați ar putea
implica faptul că H. gallinarum poate avea, de asemenea, un impact asupra fecundității și
supraviețuirii fazanilor în sălbăticie, în special dacă hrana este limitată. Dacă este așa,
scăderea populațională asociată de infectare poate fi suficientă pentru a schimba predicția
modelului de la excluderea potârnichii la coexistența fazanului și a potârnichii.
Oecologia (1999) 119:378±382
D.M. Tompkins á G. Dickson á P.J. Hudson
Parasite-mediated competition between pheasant and grey partridge:
a preliminary investigation
Received: 11 September 1998 / Accepted: 13 February 1999
Abstract Pheasants (Phasianus colchicus) and grey par-
tridges (Perdix perdix) were maintained together on land
known to be contaminated with eggs of the caecal
nematode Heterakis gallinarum to examine the hypoth-
esis that this shared parasite has a greater impact on grey
partridges than on pheasants. Since an inverse rela-
tionship between worm intensity and partridge body
condition was detected, while no such relationship with
pheasant body condition was observed, we were unable
to refute this hypothesis. Furthermore, that there was no
relationship between worm intensity after the exposure
period and partridge body mass prior to the infection
trial implies that infection caused the decrease in
partridge body condition, and not vice versa. Data
consistent with previous observations that H. gallinarum
fecundity and survival is greater in pheasants than in
partridges suggest that the bulk source of nematode in-
fection to wild grey partridges is reared pheasants, and
not the partridges themselves. This, and the di€erential
impact on host body condition, supports the hypothesis
that the spread of parasites from increasing numbers of
released pheasants has contributed to the decline in wild
grey partridge populations in the UK within the past
50 years.
Key words Apparent competition á Heterakis
gallinarum á Nematode á Perdix perdix á Phasianus
colchicus
Introduction
The number of wild grey partridge (Perdix perdix) has
declined dramatically in Europe within the past 50 years
D.M. Tompkins (&) á G. Dickson á P.J. Hudson
Institute of Biological Sciences,
University of Stirling,
Stirling, FK9 4LA, UK
e-mail: dmt1@stir.ac.uk,
Tel: +44-1786-467808, Fax: +44-1786-464994
Ó Springer-Verlag 1999
(Potts 1986). This decline has been linked with changes
in agricultural practices in general (Sotherton 1998) and,
more speci®cally, a decrease in the abundance of inver-
tebrate food for chicks due to herbicide and pesticide
application (Southwood and Cross 1969; Rands 1985;
Potts and Aebischer 1994). Grey partridge abundance,
however, has also decreased in upland regions where
agricultural practices have remained relatively un-
changed and application of herbicides is uncommon.
Thus, additional factors must also be involved in their
decline.
During the period that grey partridge abundance has
declined in the UK, the number of pheasants (Phasianus
colchicus) reared and released on private sporting estates
has increased dramatically (Tapper 1992). This inverse
relationship between the two species highlights the
possibility that adverse interactions with released
pheasants may have contributed to the decline in the
grey partridge population. One mechanism by which this
may have occurred is `apparent' competition via the
shared parasites of the two gamebird species (Wright
et al. 1980; Kimmel 1988; Robertson 1996). When two
host species share the same parasites, the more resistant
host can be a superior competitor by simply harbouring
and transmitting those parasites to the more vulnerable
host (Holt and Lawton 1994; Hudson and Greenman
1998).
Pheasants and grey partridges share a range of gas-
trointestinal nematodes by which apparent competition
may be mediated (Keymer et al. 1962). One of the most
likely candidates is the caecal worm Heterakis gallina-
rum which is by far the most abundant worm infecting
pheasants in the UK (Hillgarth 1990), and which also
regularly infects grey partridges (Clapham 1935).
H. gallinarum is known to cause tissue damage in the
caeca of its hosts (Kanshik and Deorani 1969), and its
infective egg stage can act as a carrier for the pathogenic
protozoan Histomonas meleagridis, the causative agent
of `blackhead' (Ru€ et al. 1970).
In this paper, we examine the hypothesis that the
shared caecal nematode H. gallinarum has a greater im-
 379

pact on grey partridges than on pheasants. Speci®cally,

we test the prediction that partridge body condition and
intensity of infection are inversely related, while no such
relationship occurs for pheasants or, if it does, it is not as
pronounced as for partridges. This approach cannot
prove the above hypothesis, but the absence of an inverse
relationship between worm intensity and grey partridge
body condition would refute the hypothesis and would
preclude the need for any further investigation.

Materials and methods

During July±September 1997, 15 individuals of each host species
were reared from day-old chicks on sterilised concrete to ensure
that no individuals were exposed to nematodes prior to the trial. At
12 weeks of age, up to which no chick mortality had occurred,
three individuals of each species were culled to con®rm that the
birds were free of nematode infection. The remaining birds were
sexed, wing-tagged, and weighed to the nearest 5 g. Three indi-
viduals of each species were then placed into each of four grass pens
(measuring 1.8 ´ 3.6 m) located on the rearing ®eld of a gamebird
estate in Stirlingshire, Scotland. Previous sampling had con®rmed
that the rearing ®eld was heavily contaminated with H. gallinarum
eggs, in which the protozoan H. meleagridis was absent. After
40 days, during which the birds were supplied with water, grit and
food (gamebird maintenance pellets) ad libitum, all birds were
culled and the intensity of H. gallinarum infection and host body
condition measured.
All worms were removed from the gut of each bird by washing
the intestinal and caecal contents through a coarse sieve (1.4 mm)
to remove host tissue, and then a ®ne sieve (0.2 mm) to collect the
worms. Sieving is a standard method for collecting gastrointestinal
worms (Doster and Goater 1997). The trachea of each host was
also examined for nematode parasites. Worms recovered were
identi®ed and counted under ´25 magni®cation of a binocular
microscope. The body length of all H. gallinarum worms recovered
was measured, using an ocular micrometer under ´40 magni®ca-
tion, to the nearest 0.025 mm.
Host body condition was estimated by measuring the pectoralis
muscle mass of each bird to the nearest 0.01 g. Lean wet breast
muscle mass is highly correlated with the total protein content of
gamebirds and, when adjusted for body size, is a good index of
condition (Brittas and MarcstroÈm 1982). Body size was estimated
from the length of the left tarsus of each bird, measured to the nearest
0.1 mm. Adjustments were made separately for each host species by
®tting a least-squares linear regression to the muscle mass and tarsal
length measurements, and adding the residual value generated for
each individual to the muscle mass value for a bird of mean body size,
as predicted by the ®tted equation. This ®nal step provided `real'
values, rather than deviation units, for later illustration.
All analyses were conducted using generalized linear models
(GLMs) with both host sex and pen number included as factors,
thus controlling for host sex and avoiding pseudoreplication
problems. While measurements of worm size and host body con-
dition were analysed using standard GLMs with normal error
distributions (Crawley 1993), parasite intensity was analysed using
a GLM with an explicitly de®ned negative binomial error distri-
bution (Wilson et al. 1996; Wilson and Grenfell 1997). This al-
lowed a valid model to be ®tted to the aggregated parasite intensity
data (see Fig. 1). All analyses were conducted by ®rst ®tting the full
model, and then discarding the non-signi®cant interaction terms.
Results
Although the majority of nematodes recovered from the
experimental birds were indeed the caecal worm
H. gallinarum (see below), the birds were also infected by
Fig. 1 Frequency distribution of Heterakis gallinarum intensity in
(a) pheasants (n = 12 birds) and (b) grey partridges (n = 12
birds), after 40 days exposure to ground contaminated with H. gall-
inarum eggs. 100% of the pheasants were infected with a mean ‹ SD
of 72.17 ‹ 83.05 worms, while 92% of the partridges were infected
with 5.45 ‹ 4.27 worms
two other nematode species. An intestinal worm, Cap-
illaria annulata, was recovered from 58.33% of the
pheasants (with a mean ‹ SD of 4.86 ‹ 5.96 worms
per infected bird) and 83.33% of the partridges (with
3.30 ‹ 2.50 worms per infected bird). A tracheal worm,
Syngamus trachea, was recovered from 41.67% of the
pheasants (with 5.60 ‹ 4.28 worms per infected bird).
After the 40-day exposure period, the pheasants were
infected with more H. gallinarum worms than were the
partridges (Fig. 1; deviance = 23.37, df = 1,17, P <
0.001). While there were no signi®cant di€erences in H.
gallinarum intensity either among pens (devi-
ance = 7.47, df = 3,17, P = 0.06) or between sexes
(deviance = 3.33, df = 1,17, P = 0.07), there was a
signi®cant interaction between host sex and host species
(deviance = 4.81, df = 1,17, P = 0.03) ± parasite in-
tensity di€ered between the sexes in pheasants (100% of
males infected with 85.40 ‹ 85.22 worms versus 100%
of females infected with 6.00 ‹ 1.41 worms), but not in
partridges (100% of males infected with 5.20 ‹ 2.77
worms versus 86% of females infected with 5.67 ‹ 5.50
worms).
H. gallinarum worms recovered from pheasants were
signi®cantly longer than those recovered from partridges
(Fig. 2; F1,17 = 7.79, P = 0.01). There were no di€er-
ences in worm length either among pens (F3,17 = 1.45,
P = 0.26) or between host sexes (F1,17 = 0.12,
P = 0.73).
There was no relationship between log-transformed
H. gallinarum intensity, after the 40-day exposure peri-
od, and either pheasant body mass prior to the infection
380

Fig. 2 Frequency distribution of mean H. gallinarum body length

recovered from (a) pheasants (n = 12 birds) and (b) grey partridges
(n = 11 birds) (one partridge was free of infection). Worms recovered
from pheasants had a mean ‹ SD length of 7.01 ‹ 1.25, while those
recovered from partridges had a mean length of 5.18 ‹ 1.41

trial (Fig. 3a; F1,6 = 0.22, P = 0.66) or pheasant body

condition after the trial (Fig. 3b; F1,6 = 0.33, P =
0.59). However, while log-transformed H. gallinarum
intensity was also unrelated to partridge body mass
prior to the infection trial (Fig. 4a; F1,6 = 0.36,
P = 0.57), it was negatively correlated with partridge
body condition after the trial (Fig. 4b; F1,6 = 6.30,
P = 0.05). No sex di€erences were found in either
pheasant (F1,6 = 1.71, P = 0.24) or partridge
(F1,6 = 0.57, P = 0.48) body mass prior to the infection
trial, or pheasant (F1,6 = 0.06, P = 0.82) or partridge
(F1,6 = 0.87, P = 0.39) relative body condition after
the trial. Likewise, there were no di€erences among pens
for either pheasant (F3,6 = 3.47, P = 0.09) or partridge
(F3,6 = 0.56, P = 0.66) body mass prior to the infection
trial, or pheasant (F3,6 = 0.55, P = 0.67) or partridge
(F3,6 = 2.14, P = 0.20) relative body condition after
the trial.
Discussion
This study investigated the hypothesis that the spread of
parasites from released pheasants may have contributed
to the decline in wild grey partridge populations. Fol-
lowing controlled exposure, we found that infection by
the caecal worm H. gallinarum was negatively correlated
with grey partridge body condition (Fig. 4b), while be-
ing unrelated to pheasant body condition (Fig. 3b). That
there was no relationship between the intensity of
H. gallinarum infection after the 40-day exposure period
Fig. 3 Relationship between log-transformed H. gallinarum intensity
and (a) pheasant body mass prior to the infection trial, and (b) lean
wet breast muscle mass of pheasants, adjusted for body size, after the
trial (n = 12 birds). Muscle mass was adjusted to a mean tarsal length
of 83.6 mm, using residuals from the regression equation M =
4.33T ) 123.97 [where M = breast muscle mass (g) and T = tarsal
length (mm)]
and partridge body mass prior to the infection trial
(Fig. 4a) implies that infection caused the decrease in
body condition, and not vice versa. This di€erential
impact does not allow us to refute the hypothesis that
parasite-mediated competition between pheasants and
grey partridges can adversely a€ect partridge popula-
tions. However, further information concerning parasite
transmission both within and between host species,
parasite survival and fecundity in the two di€erent hosts,
and whether the e€ect on partridge body condition
translates into an e€ect on host survival and fecundity is
required before this hypothesis can be accepted. There is
also some evidence to suggest further complications:

Fig. 4 Relationship between log-transformed H. gallinarum intensity
and (a) grey partridge body mass prior to the infection trial, and
(b) lean wet breast muscle mass of partridges, adjusted for body size,
after the trial (n = 12 birds). Muscle mass was adjusted to a mean
tarsal length of 52.72 mm, using residuals from the regression
equation M = 4.26T ) 126.01 [where M = breast muscle mass (g)
and T = tarsal length (mm)]
H. gallinarum may interact with nutritional status in its
impact on host ®tness (Clapham 1934; R.A.H.Draycott,
personal communication), and the presence of the
protozoon H. meleagridis in H. gallinarum eggs may
exacerbate the di€erential impact on pheasants and
partridges (Lund and Chute 1971, 1972a).
Some information concerning the survival and fe-
cundity of H. gallinarum in pheasants versus grey par-
tridges can be discerned from this limited study. Since
the H. gallinarum worms recovered from the grey par-
tridges after the 40-day exposure period were signi®-
cantly smaller than those recovered from the pheasants
(Fig. 2), and H. gallinarum fecundity is correlated with
worm size (Tompkins and Hudson, in press), the
381
fecundity of worms infecting partridges appears to be
less than that of worms infecting pheasants. This dif-
ference in host suitability is also the most likely expla-
nation for the lower intensity of H. gallinarum infection
in the grey partridge, following the 40-day exposure
period (Fig. 1), than in the pheasant. Indeed, previous
work by Lund and Chute (1972b) has documented both
lower survival and lower fecundity of H. gallinarum in
the grey partridge than in the pheasant. This suggests
that the bulk of nematode infection to wild grey par-
tridges in the UK is sourced from reared pheasants, and
not from the partridges themselves.
The higher intensity of H. gallinarum infection in
male than in female pheasants, as seen in this study, has
also been documented previously (Hillgarth et al. 1990;
Tompkins and Hudson, in press). Hillgarth et al. (1990)
suggested that the higher intensities in males may be due
to the suppression of the immune system in stressed
birds competing for mates. However, since we docu-
mented the same pattern, prior to any breeding in-
volvement, this appears to be unlikely. An alternative
explanation is that the rate of H. gallinarum transmis-
sion to male pheasants may be greater than that to fe-
male pheasants, possibly due to di€erences in foraging
strategy. Either way, these studies imply that male
pheasants are the major source of H. gallinarum infec-
tion.
Acknowledgements We wish to thank Pauline Monteith, Fergus
MacGregor, Florence Troup and The Game Conservancy Trust for
their assistance. The comments of Pete Robertson and two anon-
ymous referees greatly improved the manuscript. This work was
funded by NERC project grant GR3/10647.
References
Brittas R, MarcstroÈm V (1982) Studies in willow grouse Lagopus
lagopus of some possible measures of condition in birds. Ornis
Fenn 59:157±169
Clapham PA (1934) Some observations on the e€ect of dietary
de®ciency on infestation of chickens with the nematode He-
terakis gallinae. J Helminthol 12:123±126
Clapham PA (1935) Some helminth parasites from partridges and
other English birds. J Helminthol 13:139±148
Crawley MJ (1993) GLIM for ecologists. Blackwell, Oxford
Doster GL, Goater CP (1997) Collection and quanti®cation of
avian helminths and protozoa. In: Clayton DH, Moore J (eds)
Host-parasite evolution ± general principles and avian models.
Oxford University Press, Oxford, pp 396±418
Hillgarth N (1990) Parasites and sexual selection in pheasants.
DPhil. thesis, University of Oxford
Hillgarth N, Robertson P, Woodburn M (1990) A preliminary
survey of pheasant parasites in the wild. Game Conservancy
Trust, Fordingbridge
Holt RD, Lawton JH (1994) The ecological consequences of shared
natural enemies. Annu Rev Ecol Syst 25:495±520
Hudson PJ, Greenman J (1998) Competition mediated by parasites:
biological and theoretical progress. Trends Ecol Evol 13:387±
390
Kanshik RK, Deorani VPS (1969) E€ects of experimental infection
with Heterakis gallinarum. J Helminthol 43:69±78
Keymer IF, Rose JH, Beesley WN, Davies SFM (1962) A survey
and review of parasitic diseases of wild and game birds in Great
Britain. Vet Rec 74:887±894
382
Kimmel RO (1988) Potential impacts of ring-necked pheasants on
other gamebirds. In: Hallett DL, Edwards WR, Burger GV
(eds) Pheasants: symptoms of wildlife problems on agricultural
lands. North Central Section of the Wildlife Society, Bloom-
ington, pp 253±265
Lund EE, Chute AM (1971) Histomoniasis in the chukar partridge.
J Wildl Manage 35:307±315
Lund EE, Chute AM (1972a) The ring-necked pheasant (Phasianus
colchicus torquatus) as a host for Heterakis gallinarum and
Histomonas meleagridis. Am Midl Nat 87:1±7
Lund EE, Chute AM (1972b) Reciprocal responses of eight species
of galliform birds and three parasites: Heterakis gallinarum,
Histomonas meleagridis, and Parahistomonas wenrichi. J Para-
sitol 58:940±945
Potts GR (1986) The partridge: pesticides, predation and conser-
vation. Collins, London
Potts GR, Aebischer NJ (1994) Population dynamics of the grey
partridge Perdix perdix 1793±1993: monitoring, modelling and
management. Ibis 137:S29±S37
Rands MRW (1985) Pesticide use on cereals and the survival of
grey partridge chicks: a ®eld experiment. J Appl Ecol 22:49±
54
Robertson PA (1996) Naturalised introduced gamebirds in Britain.
In: Holmes JS, Simons JR (eds) The introduction and natu-
ralisation of birds. HMSO, London, pp 63±69
Ru€ MD, McDougald LR, Hansen MF (1970) Isolation of
Histomonas meleagridis from embryonated eggs of Heterakis
gallinarum. J Protozool 17:10±11
Sotherton NW (1998) Land use changes and the decline of farm-
land wildlife: an appraisal of the set-aside approach. Biol
Conserv 83:259±268
Southwood TRE, Cross DJ (1969) The ecology of the partridge.
III. Breeding success and the abundance of insects in natural
habitats. J Anim Ecol 38:497±509
Tapper S (1992) Game heritage: an ecological review from shooting
and gamekeeping records. Game Conservancy Trust, Fording-
bridge
Tompkins DM, Hudson PJ (in press) Regulation of nematode fe-
cundity in the ring-necked pheasant (Phasianus colchicus): not
just density dependence. Parasitology
Wilson K, Grenfell BT (1997) Generalized linear modelling for
parasitologists. Parasitol Today 13:33±38
Wilson K, Grenfell BT, Shaw DJ (1996) Analysis of aggregated
parasite distributions: a comparison of methods. Funct Ecol
10:592±601
Wright VL, Farris AL, Graham DL, Fielder WR (1980) E€ects of
Heterakis and Histomonas on the survival of juvenile gray
partridge. In: Peterson SR, Nelson L (eds) Proceedings of
Perdix II gray partridge workshop. University of Idaho, Mos-
cow, pp 156±164
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 1
23 when infecting pheasants, but only 0
0057
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 sucient 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%.

Key-words: apparent competition, nematode, parasite-mediated competition, Per-

dix perdix, Phasianus colchicus.
Journal of Animal Ecology (2000) 69, 829±840

Introduction (Holt & Lawton 1994; Abrams & Matsuda 1996;

Indirect interactions between species may play a cri-
tical role in determining the community structure
and dynamics of ecological assemblages (Abrams
et al. 1995; Menge 1997; Schmitz 1998). One form
of such interaction is where two species, which do
not compete for resources, share natural enemies
Correspondence: Dr Daniel M. Tompkins, Institute of
Biological Sciences, University of Stirling, Stirling, FK9
# 2000 British 4LA, UK, dmt1@stir.ac.uk, Tel.: 01786 467812, Fax:
Ecological Society 01786 464994
MuÈller & Godfray 1997; Bonsall & Hassell 1998;
Hudson & Greenman 1998). Under these circum-
stances the density of shared enemies supported by
each species individually will impact on both species
present. Since each of the two species can su€er as a
consequence of the presence of the other species, as
in competitive situations, this type of interaction has
been termed `apparent competition' (Holt 1977).
Apparent competition between two species can lead
to the rapid local extinction of one of the two spe-
cies, with the species that persists being the one that
can tolerate the higher densities of shared enemies
(Holt & Lawton 1993; Bonsall & Hassell 1997).
830 Cases where host exclusion can be attributed to
Apparent the presence of shared parasites are often cited as
competition examples of apparent competition (e.g. Settle & Wil-
mediated via son 1990; Grosholz 1992). However, conclusively
shared parasites demonstrating that host exclusion is due to apparent
competition, as opposed to either direct competition
or other parasite e€ects can be dicult to accom-
plish (as discussed in Hudson & Greenman 1998). A
recent series of controlled experiments, conducted
on laboratory populations of two moth species (Plo-
dia interpunctella and Ephestia kuehiella) and the
parasitoid Venturia canescens, has provided the ®rst
explicit demonstration of apparent competition
mediated via a shared parasitoid (Bonsall & Hassell
1997, 1998). Providing an explicit demonstration is
far harder to accomplish in natural systems, how-
ever, due to the logistical constraints involved. In
many circumstances the controlled experiments
required are unworkable. The majority of ®eld stu-
dies to date have thus been descriptive, often failing
to disentangle parasite e€ects from resource compe-
tition among hosts (e.g. Schall 1992; Schmitz &
Nudds 1994; Hanley, Vollmer & Case 1995).
De®nitive proof that apparent competition
mediated via shared parasites occurs in the ®eld will
require the large scale manipulation of host popula-
tions as employed in other gamebird-parasite studies
(Hudson, Dobson & Newborn 1998; May 1999). It
would be premature to conduct such an experiment
with any natural system, however, without ®rst
demonstrating that model simulations run with the
best available parameter estimates do, indeed, pre-
dict that apparent competitive e€ects are of su-
cient magnitude to be detectable. This is in line with
the view that mathematical modelling is a valuable
precursor to conducting population scale manipula-
tions in the wild, in order to justify the time and
expense involved (Tompkins & Begon 1999). The
aim of this study is to provide such a demonstration
for two gamebirds, the ring-necked pheasant [Pha-
sianus colchicus (L.)] and the grey partridge [Perdix
perdix (L.)], investigating whether the biology of the
shared caecal nematode Heterakis gallinarum
(Schrank) could result in exclusion of the partridge.
H. gallinarum occurs in several species of galliform
birds, transmitted via an actively ingested egg stage
(Lund & Chute 1974).
Numbers of wild grey partridge have declined
dramatically in the UK within the past 50 years
(Tapper 1992). This decline is linked primarily to
the intensi®cation of agriculture and increased pre-
dation pressure (Potts 1986, 1997; Sotherton 1998),
as supported by large scale ®eld experimentation
(Rands 1985; Tapper, Potts & Brockless 1996).
However, recent studies indicate that apparent com-
# 2000 British petition with the ring-necked pheasant may also be
Ecological Society
involved (Wright et al. 1980; Tompkins, Dickson &
Journal of Animal
Ecology, 69, Hudson 1999; Tompkins, Draycott & Hudson
829±840 2000). The experimental exposure of naive birds to
infection suggests that the pheasant acts as a reser-
voir host for H. gallinarum, the negative impact of
which is greater on the partridge (Tompkins et al.
1999, 2000). This is supported by fully controlled
experiments with singly housed birds, which clearly
demonstrate that the parasite is a cause of decreased
body condition in the grey partridge and not vice-
versa (D.M. Tompkins, in preparation). Therefore,
this study will determine whether a two-host shared-
macroparasite model, parameterized from the results
of infection and transmission experiments, predicts
exclusion of the grey partridge due to apparent com-
petition with the ring-necked pheasant.
Methods
THE MODEL EQUATIONS
The model used to describe the two-host shared-
parasite system is illustrated in Fig. 1, and is de®ned
by the following equations (for i,j ˆ 1,2; i 6ˆ j):
dHi =dt ˆ ri Hi …1 ÿ Hi =Ki † ÿ …ai ‡ di †Pi eqn 1a
dPi =dt ˆ fi bi WHi ÿ …mi ‡ bi ‡ ai †Pi
ÿ ai k0i Pi …Pi =Hi † eqn 1b
dW=dt ˆ l1 P1 ‡ l2 P2 ÿ g0 W ÿ b1 WH1
ÿ b2 WH2 eqn 1c
The model explores the dynamics of W, the num-
ber of free-living stages in the common infective
pool, Pi, the adult parasite in the ith host, and Hi,
the host population. The natural exponential growth
of the host population (ri) in equation 1a is o€set by
density dependent host mortality (with Ki being the
carrying capacity) and by the parasite induced
e€ects on host survival (ai) and fecundity (di). The
number of free living stages (equation 1c) increases
through the deposition of worm eggs (li) and
decreases through both natural mortality (g0) and
ingestion of eggs by the host (bi). The number of
parasitic worms (equation 1b) increases with the
ingestion of eggs by hosts (bi), modi®ed by the pro-
portion that survive to become mature worms (fi),
and decreases due to the combined e€ects of worm
mortality (mi), and natural (bi) and infection-induced
(ai) host mortality. The natural host mortality rate
(bi) incorporates density dependence, whereby bi ˆ
bi0 ‡ riHi/Ki. The natural host birth rate is ai, with
the net population growth rate at low population
levels expressed as ri ˆ ai ÿ bi0. The last term in
equation 1b models parasite mortality arising from
parasite-induced host deaths, assuming a negative
binomial distribution of parasites among hosts
(Anderson & May 1978). Parameter ki0 equals 1 ‡ 1/
ki, where ki is the negative binomial parameter, an
831
D. M. Tompkins
et al.

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-
meters is given in Table 1.
In terms of parasite intensity Zi ˆ Pi/Hi (M.
Roberts, personal communication), the equations
become (for i 6ˆ j):
dHi =dt ˆ ri Hi …1 ÿ u1i Hi ÿ u2i Zi †
dZi =dt ˆ fi bi W ÿ si Zi ÿ ei Z2i
dW=dt ˆ l1 H1 Z1 ‡ l2 H2 Z2 ÿ g0 W
ÿ b1 WH1 ÿ b2 WH2
where u1i ˆ K iÿ 1 and u2i ˆ (ai ‡ di)/ri. These coe-
cients scale the host density dependence and parasite
e€ect terms, respectively. The transformed equations
involve two composite parameters: (i) si ˆ (mi ‡ ai ‡
ai), measuring the loss of parasite intensity due to
both adult parasite and infection-induced host mor-
eqn 2a tality, and dilution through host births, and (ii) ei ˆ
ai/ki ÿ di, where di is the parasite-induced reduction
eqn 2b in host fecundity. Parameter ei therefore relates
parasite-induced mortality and the reduction in
fecundity. The relevance and stability of the point
equilibria of model equation 2(a,b,c) have been fully
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

Natural host fecundity a 1
55 1
50 yearÿ1 Brittas et al. (1992);

Tapper et al. 1996
Natural host mortality b 0
65 0
80 yearÿ1 Robertson & Dowell
(1990)
Host carrying capacity K 6 3 home rangeÿ1 R.A.H. Draycott,
personal com
Mortality of parasite eggs g 0
90 0
90 eggÿ1 yearÿ1 Lund (1960)
Ingestion of parasite eggs b 6
70  10ÿ5 5
58  10ÿ5 eggÿ1hostÿ1 yearÿ1 This study
by hosts
Parasite establishment f 0
590 0
065 eggÿ1 This study
Parasite fecundity l 26666 2761 eggs yearÿ1 This study
Parasite mortality m 4
15 4
17 eggs yearÿ1 This study
Aggregation of parasites k 0
30 0
30 Tompkins & Hudson 1999
in hosts
# 2000 British Parasite increase in host a 0
00 ? wormÿ1 yearÿ1 Tompkins et al. 1999
Ecological Society mortality
Journal of Animal Parasite reduction in host d 8
28  10ÿ4 ? wormÿ1 yearÿ1 M. Woodburn,
Ecology, 69, fecundity personal com
829±840
832 this study the relevant results are summarized and
Apparent applied to the pheasant/partridge system. Parameter
competition estimates were obtained from a combination of
mediated via infection and transmission experiments (as detailed
shared parasites below), together with sources in the literature and
unpublished data. Note that the model is con-
structed excluding direct interactions between the
two host species. Any predicted outcome will thus
be due to parasite e€ects alone.
INFECTION EXPERIMENT
Experimental design
The object of the infection experiment was to deter-
mine the establishment success and fecundity of H.
gallinarum worms in both pheasants and partridges,
from which the values for f, m and l could be esti-
mated (see Fig. 1). All of the birds used in the infec-
tion experiment were reared from day-old chicks on
sterilized concrete to ensure that all birds were naõÈ ve
to parasite infection. At 12 weeks of age, ®ve indivi-
duals of each species were culled to con®rm the
absence of parasites and 30 birds (15 male and 15
female) of each species placed into individual cages
with wire mesh ¯oors.
The H. gallinarum eggs used in this study were
from worms collected from pheasants that had
acquired natural infections. Female worms were col-
lected from each bird, maintained for 21 days in
0
5% formalin solution at 21 C to embryonate all
viable eggs, and broken down in saline using a small
electric blender. Embryonated eggs were then
counted in 10 0
1 mL samples, and the volume of
saline adjusted to 100 embryonated eggs per ml.
Infections were carried out on the 21st day of the
embryonation period. Fifteen individuals of each
host species were randomly selected and given a sin-
gle dose of approximately 100 embryonated H. galli-
narum eggs. Nematode eggs, suspended in 1 mL of
saline, were administered orally via a tube into the
birds crop. The remaining 15 birds of each species
were treated as controls and given 1 mL of saline
containing no nematode eggs. An infective dose of
100 eggs was chosen since this was the largest that
could be used, whilst avoiding previously documen-
ted density-dependent in¯uences on H. gallinarum
fecundity (Tompkins & Hudson 1999). The birds
were maintained for 100 days and supplied with
food (gamebird maintenance pellets), water and grit
(medium ¯int grit) ad libitum. Preliminary infection
trials indicated that 100 days was sucient to moni-
tor worm life expectancy (unpublished data).
# 2000 British Estimation of parasite establishment success
Ecological Society
Previous work has shown that once H. gallinarum
Journal of Animal
Ecology, 69, worms reach maturity (at approximately 30 days in
829±840 pheasants), they undergo negligible mortality for at
least the following 20 days (Tompkins & Hudson
1999). Thus, to estimate the rate at which ingested
H. gallinarum eggs survived to become mature para-
sites within each host species, six birds (three of
each sex) from both experimental and control
groups were randomly selected, and culled at 40
days post-infection and their worm burdens deter-
mined. All worms were removed from both caeca of
each bird by sequentially washing the caecal con-
tents through a course sieve (1
4 mm), to remove
host tissue, and a ®ne sieve (0
2 mm), to collect the
worms, using standard techniques (Doster & Goater
1997). Worms were counted under a binocular
microscope.
Estimation of parasite fecundity
To monitor H. gallinarum egg production the num-
ber of H. gallinarum eggs present in the caecal drop-
pings of individual hosts was counted at 5-day
intervals. Half a gram of each sample was suspended
in 10 mL of saturated salt solution and eggs
counted, using McMasters chambers under 100
magni®cation, in ®ve 0
1-mL subsamples. To con-
vert egg counts (expressed as eggs per gram of cae-
cal dropping) into number of eggs expelled per day,
they were multiplied by the total mass of caecal
droppings produced by that host on that day. The
total number of nematode eggs expelled per infected
individual was estimated for each host species by
multiplying the overall mean number of eggs
expelled per day by individuals of that species by
100 days. Each estimate was then converted into the
total number of eggs expelled per mature H. galli-
narum worm infecting that host species, using the
previously determined success rates for parasite
establishment (see above).
TRANSMISSION TRIAL
Experimental design
The aim of the transmission trial was to determine
the rate at which individuals of both host species
ingest H. gallinarum eggs from the environment, and
from this estimate the transmission coecient b
(Fig. 1). Birds were kept for a set period of time in
pens (measuring 1
8  3
6 m), where the density of
worm eggs was known. Prior to the transmission
trial, 13 000 embryonated H. gallinarum eggs
(02000 eggs mÿ2) were distributed evenly on the
ground in three pens; three other pens were left
unmanipulated to control for background levels of
nematode eggs. As with the infection experiment, all
of the birds used in the transmission trial were
reared from day-old chicks on sterilized concrete. At
12 weeks of age, three birds of each species were
placed into each of the six pens, where they were
maintained for the following 50 days. Fifty days was
833 considered sucient time for mature worms to accu-
D. M. Tompkins mulate before either worm mortality or host re-
et al. infection occurred. Birds were supplied with food
(gamebird maintenance pellets), water and grit
(medium ¯int grit) ad libitum. All of the birds were
culled at the end of the transmission trial and indivi-
dual worm burdens determined.
Estimation of parasite transmission rates
To convert worm burdens into transmission rate
estimates, calculations were based on the results
from the infection experiment. First, to estimate the
number of days during which any mature H. galli-
narum worms found in birds at the end of the trans-
mission trial must have actually initially infected the
host, the mean age at maturity for worms in each of
the two host species was subtracted from the 50-day
exposure period. The mean age at maturity for
worms in each host species was estimated as the
mean day post-infection at which worm eggs were
®rst observed in host caecal droppings in the infec-
tion experiment. This is a valid estimate since the
maturation of individuals within a cohort of H. gal-
linarum worms is highly correlated (unpublished
data). Secondly, to estimate the number of H. galli-
narum eggs that would have been ingested by each
individual host, the number of mature worms found
in each exposed host was divided by the mean suc-
cess rate of H. gallinarum establishment in that host
species. The number of mature worms in each host
was estimated as twice the number of mature female
worms, since mature females can be more accurately
distinguished from immature worms (by the pre-
sence of viable eggs) than can mature males, and the
sex ratio of H. gallinarum is 1 : 1 (Tompkins & Hud-
son 1999). Prior to calculating numbers of eggs,
each estimate of mature worms was adjusted to con-
trol for infection from background levels of nema-
tode eggs by subtracting the mean number of
mature worms observed in the control birds of the
appropriate host species from each estimate. A rate
of egg ingestion for each host was then calculated
by dividing the number of eggs ingested by the num-
ber of days during which those eggs could have been
taken up. Note that this approach assumes negligi-
ble egg mortality.
MODEL PREDICTIONS
Since empirical values for apartridge and dpartridge
(parasite impact on wild partridge survival and
fecundity) have not yet been determined (accurate
estimation requires controlled population manipula-
tions), we investigated whether a previously docu-
# 2000 British mented impact of H. gallinarum on grey partridge
Ecological Society
body condition (Tompkins et al. 1999) was of su-
Journal of Animal
Ecology, 69, cient magnitude for host exclusion to be a possibi-
829±840 lity. Calculations were made to estimate the levels of
apartridge and dpartridge in which the observed impact
could theoretically result. These calculations were
based on the intensively studied gamebird-nematode
system, Trichostrongylus tenuis in red grouse, where
parasites increase host mortality (from a non-parasi-
tized rate of 1
05 yearÿ1) by 3  10ÿ4 wormÿ1 yearÿ1
and decrease fecundity (from a non-parasitized rate
of 1
8 yearÿ1) by 5  10ÿ4 wormÿ1 yearÿ1 (Hudson
& Dobson 1997).
Figure 7
4 of Hudson (1986) illustrates how a
sample of `very thin' grouse (having lost 070% of
their breast muscle mass) had average worm bur-
dens of 7800 T. tenuis, a sample of grouse in `poor
condition' (having lost 050% of their breast muscle
mass) had average burdens of 3250 worms and a
sample of grouse in `average to good' condition
(having lost 020% of their breast muscle mass) had
average burdens of only 1850 worms. This approxi-
mates to a linear reduction in host body condition
of 1
12  10ÿ2 wormÿ1. Thus, a parasite-induced
reduction in grouse body condition of 01% equates
to a 02
5% increase in the yearly mortality rate
and a 02
5% decrease in the yearly fecundity rate.
Applying this relationship to the grey partridge
converts the observed reduction in body condition
(Fig. 2) to an increase in partridge mortality of 2
15
 10ÿ2 wormÿ1 yearÿ1 and a decrease in partridge
fecundity of 4
04  10ÿ2 wormÿ1 yearÿ1. The model
was run using these parameter values. However,
since this is only a rough approximation, sensitivity
analyses were conducted to determine the robustness
of any ®nding. Note, this approach does not imply
Fig. 2. Relationship between Heterakis gallinarum intensity
and grey partridge breast muscle mass adjusted for body
size (an index of body condition), obtained from an experi-
mental exposure of naive birds to infection. Muscle mass
was adjusted to a mean tarsal length of 52
7 mm. Fitting a
linear regression to the data illustrates that, on average,
there is a drop of 1
076% in body condition for each H.
gallinarum worm infecting (n ˆ 12 birds). Modi®ed from
Tompkins et al. (1999).
834 similar pathogenicity of H. gallinarum and T. tenuis,
Apparent rather it assumes that the relationship between host
competition body condition and host ®tness is similar for the
mediated via two gamebirds.
shared parasites

SPATIAL SEPARATION

An assumption implicit in the model is that the two

host species sharing the same parasite also share
precisely the same habitat. This condition, however,
will rarely be met for wild systems; it certainly does
not hold for the ring-necked pheasant and the grey
partridge (Cocchi et al. 1990). Since the driving
force behind host exclusion due to apparent compe-
tition mediated via shared parasites is the transmis-
sion of parasites between host species, spatial
separation (when it decreases such transmission)
would allow species to co-exist that would not
otherwise. If the model does, indeed, predict exclu-
sion, the important question is then whether or not
the level of separation between the two host species Fig. 3. Frequency distribution of Heterakis gallinarum
in the wild is sucient to prevent such exclusion intensity in (a) pheasants (n ˆ 6 birds), and (b) grey par-
from actually occurring. As a preliminary investiga- tridges (n ˆ 6 birds), 40 days after being infected with
approximately 100 embryonated H. gallinarum eggs.
tion, parameters of the current model were adjusted
to approximate the e€ect of spatial separation
between the pheasant and the partridge. Since the
basic reproductive number (R0; the number of adult
female parasites derived from each adult female PARASITE FECUNDITY

parasite in a population of uninfected hosts) for H.
gallinarum infecting pheasants is at least 100 that
for the parasite infecting partridges (see Results),
the pheasant is indeed primarily responsible for the
spread of infection. Therefore, an approximation of
spatial separation was modelled by simply reducing
the rate at which the partridges were ingesting the
nematode eggs (i.e. a 50% decline in bpartridge
mimics 50% spatial separation between the two host
species).
Results
Over the course of the infection experiment, six
pheasants and four partridges were euthanased due
to husbandry problems unrelated to parasite infec-
tion. In the remainder, the number of worm eggs
expelled was signi®cantly higher in the caecal drop-
pings of pheasants than in the caecal droppings of
partridges (Fig. 4); infected pheasants expelled a
mean (‹ SE) of 3793 ‹ 3117 eggs dayÿ1, whilst
infected partridges expelled only 43 ‹ 30 eggs dayÿ1
(U ˆ 6, P ˆ 0
02). 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
and 662 in partridges.

PARASITE ESTABLISHMENT
Forty days after being infected, H. gallinarum inten-
sities in pheasants were signi®cantly higher than
those in partridges (Fig. 3). Infected pheasants were
host to a mean (‹ SE) of 59
00 ‹ 14
83 worms,
whilst infected partridges were host to only 6
50 ‹
3
62 worms (Mann±Whitney U ˆ 5, P ˆ 0
04). Thus,
considering that each infected host was given
approximately 100 embryonated H. gallinarum eggs,
0
590 of the eggs given to pheasants survived to
# 2000 British become mature parasites, whilst only 0
065 of the
Ecological Society
eggs given to partridges survived. None of the con-
Journal of Animal
Ecology, 69, trol birds of either host species contained any
829±840 worms.
PARASITE TRANSMISSION
After the transmission trial, H. gallinarum intensity
was signi®cantly higher in the exposed pheasants (U
ˆ 13
5, P ˆ 0
04) and partridges (U ˆ 15, P ˆ 0
05)
than in the control birds (Fig. 5). Controlling for
background infection, the 13 000 worm eggs laid
down in each pen resulted in infections of 151
50
mature worms per exposed pheasant and 7
17
mature worms per exposed partridge. Since the
mean age of maturity for H. gallinarum was esti-
mated as 35 days in pheasants and 42
5 days in par-
tridges (see Fig. 4), only those H. gallinarum eggs
picked up by pheasants in the ®rst 15 days, or by
835
D. M. Tompkins
et al.
Fig. 4. Number of Heterakis gallinarum eggs expelled in
the caecal droppings of (a) pheasants (n ˆ 6 birds), and (b)
grey partridges (n ˆ 8 birds), over the 100 days following
infection with approximately 100 embryonated H. galli-
narum eggs. Mean numbers (‹ SE) are shown. Note the
di€erent y-axis scales.
partridges in the ®rst 7
5 days of the trial, would
have developed to mature worms. Daily rates of
worm ingestion were thus estimated as 17
12 eggs
birdÿ1 for the pheasants, and 14
70 eggs birdÿ1 for
the partridges.
MODEL PARAMETERIZATION
Model parameters, and the sources from which they
were estimated, are listed in Table 1. The experi-
ments detailed in this study were used to quantify
parasite transmission, establishment, fecundity and
mortality.
Instantaneous rates of parasite fecundity in both
host species were obtained by dividing the mean
number of eggs produced by worms in each host
(quanti®ed in the infection experiment) by parasite
longevity in that host species (measured in years).
# 2000 British Assuming that the cessation of egg production in
Ecological Society
infected individuals represented the age at which
Journal of Animal
Ecology, 69, infecting worms died (an assumption supported by
829±840 the fact that no worms were found in hosts when
culled at 100 days post-infection), parasite life expec-
tancy was estimated as a mean of 88 days in phea-
sants and a mean of 87
5 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 6
5 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
6
5 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 8
28 
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.
Draycott, personal communication).
MODEL PREDICTIONS
When solved for the best available parameter esti-
mates, the two-host shared-parasite model predicts
Fig. 5. Heterakis gallinarum burdens in both pheasants and
partridges after being maintained for 50 days in pens on a
grass ®eld. Mean burdens (‹ SE) are shown. Filled points
indicate the birds (12 of each species) which were main-
tained in pens where approximately 13 000 embryonated
H. gallinarum eggs had been distributed evenly on the
ground prior to the transmission trial; open points indicate
the birds (six of each species) maintained in unmanipulated
pens to control for background levels of nematode eggs.
836 exclusion of the grey partridge. In general, in the becomes biologically feasible, when all population
Apparent absence of direct competition, host exclusion densities are above zero. Algebraically, R0i* is found
competition requires that: from the condition Z2* ˆ r2/(a2 ‡ d2), where Z2* is
mediated via the value of Z2 at this co-existence threshold. Since,
shared parasites S0i > 1 eqn 3a by de®nition, the product of S0i and S0j necessarily
where S0i is the `tolerance' index (Greenman & Hud- equals 1, only one of the two hosts can exclude the
son 1998, 1999): other. From the parameter values listed in Table 1,
and impacts of H. gallinarum on partridge fecundity
S0i ˆ …fj Wi0 †=…fi Wj0 † eqn 3b and survival of 4
04  10ÿ2 wormÿ1 yearÿ1 and
2
15  10ÿ2 wormÿ1 yearÿ1 respectively, we ®nd that
(i 6ˆ j), with: S0pheasant ˆ 7
09 and R0*pheasant ˆ 1
12. Since
R0pheasant ˆ 1
23 (see next section) the model pre-
Wi0 ˆ …di =bi †‰ri =…ai di †Š eqn 3c dicts that the partridge will be excluded by the phea-
where: sant, with the pheasant remaining in co-existence
with the parasite.
di ˆ si ‡ ri ei =…ai ‡ di † The closeness in value of R0pheasant and R0*pheasant
suggests that the point in parameter space de®ned
ˆ mi ‡ ai ‡ bi ‡ ri ai ki 0=…ai ‡ di † eqn 3d by the empirically determined parameter values lies
close to the exclusion±co-existence boundary. This
where di > 0. Wi0 denotes the equilibrium value of
proximity to the threshold was studied in more
W when host j ( j 6ˆ i) is absent and density depen-
dence can be ignored. If condition equation 3a detail by carrying out sensitivity analysis on indivi-
holds, host exclusion will occur for: dual parameters. Varying the calculated parameters
dpartridge and apartridge singly (with all other model
R0i > R0i > 1 eqn 4a equation parameters kept ®xed) found a boundary
value of dpartridge ˆ 1
02  10ÿ2 wormÿ1 yearÿ1 for
where: the switch in model outcome from exclusion to co-
existence, whilst there was no boundary intersection
R0i ˆ …fi li =si ÿ 1†…bi Ki †=g0 eqn 4b
for apartridge. Thus, while a 75% lower dpartridge leads
is the basic reproductive number for the parasite to co-existence of the two host species, co-existence
infecting host i and R0i* is the threshold value of cannot be brought about by altering apartridge alone
R0i for which the host co-existence equilibrium ®rst (Fig. 6).

# 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.
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

Parameter Pheasant value Partridge value

Symbol Threshold % Change Threshold % Change

Natural host fecundity a 1
06 ÿ 32% 2
11 ‡ 41%

Natural host mortality b 1
12 ‡ 72% 0
25 ÿ 69%
Ingestion of parasite eggs by hosts b 4
23  10ÿ4 ÿ 84% 3
17  10ÿ5 ÿ 43%
Parasite increase in host mortality a 5
33  10ÿ4 ± ± ±
Parasite reduction in host fecundity d 1
65  10ÿ3 ‡ 99% 1
02  10ÿ2 ÿ 75%

Sensitivity analyses were also conducted on
apheasant, dpheasant, and b, a and b for both host spe-
cies, since these were the other quantities not
directly estimated in this study to which the model
outcome was considered to be highly sensitive.
However, the model outcome of partridge exclusion
was also relatively robust to changes in these values
(see Table 2 for a summary of all sensitivity analyses
conducted).
SPATIAL SEPARATION
When the model was run for each host species alone
with the parasite, the qualitative outcome for the
pheasant was unchanged (remaining in co-existence
with the parasite), while that for the partridge chan-
ged from exclusion of the host to exclusion of the
parasite. The model equilibrium, describing an unin-
fected single host (host i) at its carrying capacity, is
stable against parasite invasion provided R0i < 1. In
the two-host simulations, this equilibrium is not
stable against invasion by the other host if we
assume rj > 0 ( j 6ˆ i). From the parameter values
listed in Table 1 we infer that the pheasant co-exists
in equilibrium with the parasite when the partridge
is absent since R0pheasant ˆ 1
23. The average worm
burden is 235 worms hostÿ1 and the pheasant popu-
lation is 0
94 birds haÿ1. The basic reproductive
number for the parasite infecting the partridge,
when the pheasant is absent, is R0partridge ˆ 0
0057,
i.e. the parasite is excluded. This shift in model out-
come, from partridge exclusion when the pheasant is
present, to parasite exclusion when the pheasant is
absent, demonstrates that the host exclusion pre-
dicted by the two-host shared-parasite model is
indeed due to the transmission of parasites from the
pheasant. These single-host simulations also demon-
strate how this parasite-mediated interaction
between the pheasant and partridge is not strictly
# 2000 British apparent competition, where the presence of either
Ecological Society
host indirectly a€ects the density of the other (Holt
Journal of Animal
Ecology, 69, 1977, 1984), but is an amensal form whereby one
829±840 host (the partridge) su€ers a reduction in density,
while the other (the pheasant) is relatively unaf-
fected. This is because the bulk of H. gallinarum
transmission to the pheasant is intra-speci®c, whilst
the opposite is true for the partridge.
To determine the level of spatial separation
between the two host species at which the model
predicts the inter-speci®c transmission of H. galli-
narum from the pheasant to the partridge is low
enough to allow their co-existence, the model was
ran with bpartridge set at di€ering levels below the
empirically determined value (5
58  10ÿ5 eggÿ1
hostÿ1 yearÿ1). A boundary value of bpartridge ˆ
3
17  10ÿ5 eggÿ1 hostÿ1 yearÿ1 was identi®ed,
below which the partridge was no longer excluded
from the system. This implies that spatial separation
of greater than 43% between the two host species
will allow the grey partridge to co-exist with the
pheasant in the presence of H. gallinarum.
Discussion
Based on the best available parameter estimates, the
macroparasite model discussed in this paper predicts
that apparent competition with the ring-necked
pheasant is sucient to cause exclusion of the grey
partridge. This result provides strong evidence for
the view that apparent competition plays a vital role
in determining the structure of natural communities,
and suggests that a population scale experiment
with pheasants and partridges could provide proof
that apparent competition mediated by shared para-
sites occurs in the wild.
Apparent competition is but one mechanism by
which shared parasites can in¯uence host popula-
tions. However, it is fundamentally di€erent from
all other parasite e€ects in that the driving force
behind host exclusion, when it occurs, is the pre-
sence of alternative host species and not the shared
parasite per se. It is this characteristic which requires
demonstration if the occurrence of apparent compe-
tition is to be proven. This study provides such a
demonstration for the pheasant/partridge system,
con®rming that any detrimental e€ects of the nema-
838 tode H. gallinarum on wild grey partridge popula-
Apparent tions will, indeed, be due to apparent competition
competition with the ring-necked pheasant. Both the model cre-
mediated via ated and the experiments conducted show that the
shared parasites bulk of H. gallinarum infections in partridges, when
they occur in the same locations as pheasants, will
be from the pheasants and not from the partridges
themselves. This is due to the success rate of H. gal-
linarum establishment being nine times greater in
pheasants than in partridges, and the fecundity of
established worms being approximately 10 times
greater in pheasants than in partridges. This results
in predicted R0s of 1
23 for the parasite infecting
pheasants and 0
0057 for the parasite infecting par-
tridges. Since the R0 for H. gallinarum infecting grey
partridges is much less than unity, the parasite can-
not be maintained within partridge populations
without the presence of alternative hosts. 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. This clearly illustrates how the
force of H. gallinarum infection to grey partridges,
in areas where pheasants are also present, will be
from the pheasants and any resulting impact will be
due to apparent competition.
A potential source of error in the calculation of
R0 for the parasite infecting partridges is that the H.
gallinarum eggs used in the infection and transmis-
sion experiments were obtained from worms infect-
ing pheasants. Since adaptations of H. gallinarum to
particular host species have been previously demon-
strated (Lund, Chute & Myers 1970), our calculated
value of R0partridge may be an under-estimate. How-
ever, work by Lund & Chute (1974) has shown that
this is likely not the case. In their trials, where H.
gallinarum eggs for experimental infections were
obtained from a mix of host species, the `reproduc-
tive potential' of the parasite (number of viable eggs
produced per embryonated egg infecting) was 243
times less when infecting grey partridges than when
infecting pheasants. This di€erence is of similar
magnitude to that between the values of R0 calcu-
lated in the present study (216 times less when
infecting grey partridges than when infecting phea-
sants).
The observed impact of H. gallinarum on the grey
partridge appears to be sucient to cause exclusion
when the pheasant is present. However, this out-
come could be incorrect for at least three reasons.
First, it is possible that the values for parasite-
induced increase in partridge mortality (apartridge)
and decrease in partridge fecundity (dpartridge) used
in the model, as estimated from the observed impact
on body condition, are too high. The true values
# 2000 British may not lead to partridge exclusion. However, as
Ecological Society
the sensitivity analysis shows, the predicted outcome
Journal of Animal
Ecology, 69, is relatively robust ± partridge and pheasant co-exis-
829±840 tence cannot be bought about in the model by alter-
ing apartridge alone, whilst a drop in dpartridge of 75%
is required. Secondly, as outlined earlier, even
though the potential for partridge exclusion exists in
this non-spatial model, habitat separation between
the two hosts in the wild may decrease the transmis-
sion of H. gallinarum from pheasants to partridges
suciently for the two species to co-exist in the
parasites presence. Our prediction, based on the
approximation of spatial separation employed in
this study, is that partridge exclusion would still
occur if separation was less than 43%. Further
work, both modelling and experimental, is required
to test this prediction. However, since H. gallinarum
has been recorded from wild grey partridges (Clap-
ham 1935; Keymer et al. 1962), and we have shown
here that the parasite cannot be maintained within a
population of grey partridges alone, it is apparent
that at least some parasite transmission to this spe-
cies does occur from other sources in the wild.
Finally, the model outcome of partridge exclusion
may also be incorrect since our estimation of H. gal-
linarum ®tness when infecting the pheasant may be
too high. This estimate was based on experiments
with naive individuals, while evidence suggests there
may be some acquired resistance to H. gallinarum
infection in the ring-necked pheasant (Lund 1967).
Inaccurate estimation of other parameters is
another possible source of error in model predic-
tions. The greatest error may result from the manner
in which values of f (parasite establishment success)
and b (rate of ingestion of parasite eggs by hosts)
were estimated. This is not surprising, since trans-
mission rates are generally considered the hardest of
epidemiological parameters to quantify (McCallum
& Scott 1994). Experiments documented in Tomp-
kins & Hudson (1999) suggest that density depen-
dence may operate to limit the success of
establishing H. gallinarum worms down to a maxi-
mum of approximately 50 worms per dose. Since
the highest value of b obtained was only approxi-
mately 17 eggs per day, this is unlikely to a€ect the
results of the transmission trial. If slight density
dependence was operating at this level, however, our
point estimates of b would be slight under-estimates
and our model would be predicting partridge exclu-
sion whilst erring on the side of caution. Another
possibility is that our infection experiment, where
infective doses of 100 eggs were used, may be under-
estimating f. However, due to the manner in which
b was estimated, and the manner by which both
parameters are incorporated into the model, erro-
neous estimates of f will not a€ect model output.
What may be causing inaccuracies in model output,
however, is the linear fashion by which we scaled
estimates of b from values obtained when birds were
exposed to known numbers of H. gallinarum eggs
on unrealistically small areas of ground to values
applicable to birds on their natural home ranges.
This scaling will be highly sensitive to any inaccura-
839 cies in the estimates of home range size and will
D. M. Tompkins only give approximations of b, since nematode
et al. infective stages in the wild are not spread evenly
over the habitat, but tend to be localized in `hot-
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-
dicted here.
A further factor which may also increase the pos-
sibility of grey partridge exclusion is the pathogenic
protozoan Histomonas meleagridis. This parasite,
which is the causative agent of `blackhead', can be
transmitted between individuals inside the eggs of
H. gallinarum (Ru€, McDougald & Hansen 1970).
Evidence suggests that while partridges which ingest
H. gallinarum eggs carrying the protozoan are killed
by `blackhead' before the nematode worms mature,
pheasants can survive long enough for next-genera-
tion nematode eggs carrying the protozoan to be
expelled (Lund & Chute 1974; D.M. Tompkins &
P.J. Hudson, unpublished data). Thus, when the
protozoan is present, the deleterious e€ects of H.
gallinarum transmission from pheasants to par-
tridges would most likely be exacerbated. On a more
positive note, however, is the fact that the sensitivity
analyses indicate that an increase in partridge
fecundity of 41% would alter the model outcome
from partridge exclusion to pheasant and partridge
co-existence. Since this increased value is within the
documented range of natural grey partridge fecund-
ity (Tapper et al. 1996), it suggests that management
techniques that increase partridge breeding success
(such as predation control or habitat improvement)
would prevent exclusion due to apparent competi-
tion. A decrease in pheasant fecundity of just ÿ32%
would also shift the model outcome to pheasant and
partridge co-existence.
This study has accomplished its goal, in demon-
strating that model simulations run with best avail-
able parameter estimates predict that apparent
competitive e€ects of sucient magnitude to be
detectable do occur between the ring-necked phea-
sant and the grey partridge. Furthermore, the dele-
terious e€ects of H. gallinarum may be sucient to
cause exclusion of the partridge in areas where a
high degree of spatial overlap with pheasants occurs.
Thus, this parasite may have played a contributary
role in the UK grey partridge decline, and may also
be hampering current e€orts to re-establish and
increase wild partridge populations. However,
experimental manipulations at the population scale
are required before the role of H. gallinarum can be
unequivocally proven.
# 2000 British
Ecological Society Acknowledgements
Journal of Animal
Ecology, 69, We wish to thank Roger Draycott, Pauline Mon-
829±840 teith, Maureen Woodburn, and Rufus Sage for their
assistance. The manuscript was greatly improved by
the comments of both Steve Albon and an anon-
ymous referee. This work was funded by NERC
project grant GR3/10647.
References
Abrams, P. & Matsuda, H. (1996) Positive indirect e€ects
between prey species that share predators. Ecology, 77,
610±616.
Abrams, P., Menge, B.A., Mittelbach, G.G., Spiller, D. &
Yodzis, P. (1995) The role of indirect e€ects in food
webs. Food Webs: Integration of Pattern and Dynamics
(eds G. A. Polis & K. O. Winemiller), pp. 371±395.
Chapman & Hall, New York.
Anderson, R.M. & May, R.M. (1978) Regulation and sta-
bility of host±parasite population interactions: I. Regu-
latory processes. Journal of Animal Ecology, 47, 219±
249.
Bonsall, M.B. & Hassell, M.P. (1997) Apparent competi-
tion structures ecological assemblages. Nature, 388,
371±373.
Bonsall, M.B. & Hassell, M.P. (1998) Population dynamics
of apparent competition in a host-parasitoid assem-
blage. Journal of Animal Ecology, 67, 918±929.
Brittas, R., Marcstrom, V., Kenward, R.E. & Karlbom,
M. (1992) Survival and breeding success of reared and
wild ring-necked pheasants in Sweden. Journal of Wild-
life Management, 56, 368±376.
Clapham, P.A. (1935) Some helminth parasites from par-
tridges and other English birds. Journal of Helminthol-
ogy, 13, 139±148.
Cocchi, R., Matteucci, C., Meriggi, A., Montagna, D.,
Toso, S. & Zacchetti, D. (1990) Habitat use of grey
partridge and pheasant on a reclaimed land in north-
ern Italy. International Union of Game Biologists, 12,
354±356.
Doster, G.L. & Goater, C.P. (1997) Collection and quanti-
®cation of avian helminths and protozoa. Host±Para-
site EvolutionÐGeneral Principles and Avian Models
(eds D. H. Clayton & J. Moore), pp. 396±418. Oxford
University Press, Oxford.
Greenman, J.V. & Hudson, P.J. (1998) Parasite-mediated
and direct competition in a two-host shared macropar-
asite system. Stirling Mathematical Ecology Group,
Working Paper #11.
Greenman, J.V. & Hudson, P.J. (1999) Host exclusion and
coexistence in apparent and direct competition: an
application of bifurcation theory. Theoretical Popula-
tion Biology, 56, 48±64.
Grosholz, E.D. (1992) Interactions of intraspeci®c, inter-
speci®c, and apparent competition with host-pathogen
population dynamics. Ecology, 73, 507±514.
Hanley, K.A., Vollmer, D.M. & Case, T.J. (1995) The dis-
tribution and prevalence of helminths, coccidia and
blood parasites in two competing species of gecko:
implications for apparent competition. Oecologia, 102,
220±229.
Holt, R.D. (1977) Predation, apparent competition, and
the structure of prey communities. Theoretical Popula-
tion Biology, 12, 197±229.
Holt, R.D. (1984) Spatial heterogeneity, indirect interac-
tions and the coexistence of prey species. American
Naturalist, 130, 412±430.
Holt, R.D. & Lawton, J.H. (1993) Apparent competition
and enemy-free space in insect host±parasitoid commu-
nities. American Naturalist, 142, 623±645.
840 Holt, R.D. & Lawton, J.H. (1994) The ecological conse-
Apparent quences of shared natural enemies. Annual Review of
Ecology and Systematics, 25, 495±520.
competition Hudson, P.J. (1986). Red Grouse. The Game Conservancy
mediated via Trust, Fordingbridge.
shared parasites Hudson, P.J. & Dobson, A.P. (1997) Transmission
dynamics and host±parasite interactions of Trichos-
trongylus tenuis in red grouse. (Lagopus lagopus scoti-
cus). Journal of Parasitology, 83, 194±202.
Hudson, P.J., Dobson, A.P. & Newborn, D. (1998) Preven-
tion of population cycles by parasite removal. Science,
282, 2256±2258.
Hudson, P. & Greenman, J. (1998) Competition mediated
by parasites: biological and theoretical progress.
Trends in Ecology and Evolution, 13, 387±390.
Keymer, I.F., Rose, J.H., Beesley, W.N. & Davies, S.F.M.
(1962) A survey and review of parasitic diseases of
wild and game birds in Great Britain. Veterinary
Record, 74, 887±894.
Lund, E.E. (1960) Factors in¯uencing the survival of
Heterakis and Histomonas on soil. Journal of Parasitol-
ogy, 46, 38.
Lund, E.E. (1967) Acquired resistance to experimental
Heterakis infections in chickens and turkeys: e€ect on
the transmission of Histomonas meleagridis. Journal of
Helminthology, 41, 55±62.
Lund, E.E. & Chute, A.M. (1974) The reproductive poten-
tial of Heterakis gallinarum in various species of galli-
form birds: implications for survival of H. gallinarum
and Histomonas meleagridis to recent times. Interna-
tional Journal for Parasitology, 4, 455±461.
Lund, E.E., Chute, A.M. & Myers, S.L. (1970) Perfor-
mance in chickens and turkeys of chicken-adapted
Heterakis gallinarum. Journal of Helminthology, 44,
97±106.
May, R.M. (1999) Crash tests for real. Nature, 398, 371±
372.
McCallum, H. & Scott, M.E. (1994) Quantifying popula-
tion processes. Parasitic and Infectious Diseases (eds
M. E. Scott & G. Smith), pp. 29±45. Academic Press,
San Diego.
Menge, B.A. (1997) Detection of direct versus indirect
e€ects: were experiments long enough? American Nat-
uralist, 149, 801±823.
MuÈller, C.B. & Godfray, H.C.J. (1997) Apparent competi-
tion between two aphid species. Journal of Animal
Ecology, 66, 57±64.
Potts, G.R. (1986) The Partridge: Pesticides, Predation and
Conservation. Collins, London.
Potts, G.R. (1997) Cereal farming, pesticides and grey par-
tridges. Farming and Birds in Europe (eds Pain, D.J. &
Pienkowski, M.W.), pp. 150±177. Academic Press.
London.
Rands, M.R.W. (1985) Pesticide use on cereals and the sur-
vival of grey partridge clutches: a ®eld experiment.
Journal of Applied Ecology, 22, 49±54.
Robertson, P.A. & Dowell, S.D. (1990) The e€ects of hand
rearing on wild gamebird populations. The Future of
Wild Galliformes in the Netherlands (eds J. T. Lumeij
# 2000 British
Ecological Society
Journal of Animal
Ecology, 69,
829±840
& Y. R. Hoogeveen), pp. 158±171. Gegevens Konink-
lijke Bibliotheek, Den Haag.
Ru€, M.D., McDougald, L.R. & Hansen, M.F. (1970) Iso-
lation of Histomonas meleagridis from embryonated
eggs of Heterakis gallinarum. Journal of Protozoology,
17, 10±11.
Saunders, L.M., Tompkins, D.M. & Hudson, P.J. (1999)
Investigating the dynamics of nematode transmission
to the red grouse (Lagopus lagopus scoticus): studies
on the recovery of Trichostrongylus tenuis larvae from
vegetation. Journal of Helminthology, 73, 171±175.
Schall, J.J. (1992) Parasite-mediated competition in Anolis
lizards. Oecologia, 92, 58±64.
Schmitz, O.J. (1998) Direct and indirect e€ects of preda-
tion and predation risk in old±®eld interaction webs.
American Naturalist, 151, 327±342.
Schmitz, O.J. & Nudds, T.D. (1994) Parasite-mediated
competition in deer and moose: how strong is the e€ect
of the meningeal worm on moose? Ecological Applica-
tions, 4, 91±103.
Settle, W.H. & Wilson, L.T. (1990) Invasion by the varia-
gated leafhopper and biotic interactions: parasitism,
competition and apparent competition. Ecology, 71,
1461±1470.
Sotherton, N.W. (1998) Land use changes and the decline
of farmland wildlife: an appraisal of the set-aside
approach. Biological Conservation, 83, 259±268.
Tapper, S. (1992). Game Heritage: an Ecological Review
from Shooting and Gamekeeping Records. Game Con-
servancy Trust, Fordingbridge.
Tapper, S., Potts, G.R. & Brockless, M.H. (1996) The
e€ect of an experimental reduction in predation pres-
sure on the breeding success and population density of
grey partridges Perdix perdix. Journal of Applied Ecol-
ogy, 33, 965±978.
Tompkins, D.M. & Begon, M. (1999) Parasites can regu-
late wildlife populations. Parasitology Today, 15, 311±
313.
Tompkins, D.M., Dickson, G. & Hudson, P.J. (1999) Para-
site-mediated competition between pheasant and grey
partridge: a preliminary investigation. Oecologia, 119,
378±382.
Tompkins, D.M., Draycott, R.A.H. & Hudson, P.J. (2000)
Field evidence for apparent competition mediated via
the shared parasites of two gamebird species. Ecology
Letters, 3, 10±14.
Tompkins, D.M. & Hudson, P.J. (1999) Regulation of
nematode fecundity in the ring-necked pheasant (Pha-
sianus colchicus): not just density dependence. Parasi-
tology, 118, 417±423.
Wright, V.L., Farris, A.L., Graham, D.L. & Fielder, W.R.
(1980) E€ects of Heterakis and Histomonas on the sur-
vival of juvenile gray partridge. Proceedings of Perdix
II Gray Partridge Workshop (eds S. R. Peterson &
L. Nelson), pp. 156±164. University of Idaho, Mos-
cow.
Received 26 May 1999; revision received 14 March 2000
 187

Differential impact of a shared nematode parasite on two

gamebird hosts : implications for apparent competition

D. M. T O M P K I N S "*, J. V. G R E E N M A N # and P. J. H U D S O N "

" Department of Biological Sciences, University of Stirling, Stirling FK9 4LA, UK
# Department of Computing Science and Mathematics, University of Stirling, Stirling FK9 4LA, UK

(Received 25 May 2000 ; revised 27 July 2000 ; accepted 27 July 2000)


If the deleterious effects of non-specific parasites are greater on vulnerable host species than on reservoir host species then
exclusion of the vulnerable host through apparent competition is more likely. Evidence suggests that such a mechanism
occurs in interactions between the ring-necked pheasant (Phasianus colchicus), the grey partridge (Perdix perdix), and their
shared caecal nematode Heterakis gallinarum. Modelling of the system predicts that the reduced parasite impact on the
pheasant compared to the partridge results in the force of infection transmitted from pheasants to partridges being
sufficient to cause partridge exclusion. Since the parasite impacts are currently estimated from correlational work,
controlled infections were conducted to experimentally compare the impact of H. gallinarum on the two hosts and verify
cause and effect. While challenged partridges showed reduced mass gain, decreased food consumption, and impaired
caecal activity, in comparison to controls, the only detectable effect of parasite challenge on the pheasant was impaired
caecal activity. The impact of H. gallinarum on challenged partridges conforms with previous correlational data, supporting
the prediction that parasite-mediated apparent competition with the ring-necked pheasant may result in grey partridge
exclusion. However, the observed decrease in the caecal activity of challenged pheasants could imply that H. gallinarum
may also have an impact on the fecundity and survival of pheasants in the wild, particularly if food is limiting. If this is
the case, the associated decrease in the force of infection to which the partridge is exposed may be sufficient to change the
model prediction from partridge exclusion to pheasant and partridge coexistence.

Key words : Heterakis gallinarum, Perdix perdix, Phasianus colchicus, partridge, pheasant, parasite-mediated competition.

In the majority of cases, however, evidence for such


Non-specific parasites can affect the structure of
animal communities through indirect effects such as
apparent competition, where the presence of one
host species adversely affects another simply through
the increased presence of shared parasites (Holt,
1977 ; Holt & Lawton, 1994), or parasite-mediated
competition, where infection alters the relative
competitive strength of host species (Freeland, 1983 ;
Price et al. 1986). The potential of such interactions
was noted over 50 years ago by Haldane (1949) when
he stated that ‘ A non-specific parasite … is a power-
ful competitive weapon ’. However, although studies
have explicitly demonstrated that such interactions
can affect community structure in the laboratory
(Park, 1948 ; Bonsall & Hassell, 1997), evidence for
effects on natural communities is limited (Hudson &
Greenman, 1998).
There are many instances in which non-specific
parasites are believed to be involved in population
declines of threatened wildlife species (Tompkins &
Wilson, 1998 ; Daszak, Cunningham & Hyatt, 2000).
* Corresponding author : Department of Biological
Sciences, University of Stirling, Stirling FK9 4LA, UK.
Tel : j44 1786 467808. Fax : j44 1786 464994.
E-mail : dmt1!stir.ac.uk
an involvement is based on either descriptive or
correlational work (Hudson & Greenman, 1998).
Specifically, the cause and effect of observed negative
correlations between parasite infection and com-
ponents of host fitness has yet to be ascertained in a
controlled manner that is comparable between the
host species. This is hardly surprising since a
reasonable weight of evidence demonstrating that
parasites are a cause of decreased fitness in any wild
population has only recently been obtained (Gulland,
1995 ; Tompkins & Begon, 1999).
Evidence suggests that apparent competition be-
tween the ring-necked pheasant (Phasianus colchicus
(L.)) and the grey partridge (Perdix perdix (L.)),
mediated via the caecal nematode Heterakis gallin-
arum (Schrank), may have played a role in the
decline of wild grey partridge populations in the UK
over the past 50 years (Tompkins, Dickson &
Hudson, 1999 ; Tompkins, Draycott & Hudson,
2000 a). This hypothesis is supported by a 2-host
shared macroparasite model which predicts partridge
exclusion for the current set of parameter estimates
(Tompkins et al. 2000 b). However, since this
outcome is based only on correlational evidence for
parasite effects (which indicates a greater impact on
the partridge than on the pheasant), work is required

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Parasitology (2001), 122, 187–193. Printed in the United Kingdom " 2001 Cambridge University Press
https://doi.org/10.1017/S0031182001007247
 D. M. Tompkins, J. V. Greenman and P. J. Hudson
to quantify parasite impact on the 2 hosts in a
comparable manner and verify cause and effect.
Such work was carried out here through the use of
controlled infection experiments.
Differential impact is one of the potential causes of
the non-reciprocity that is often observed in enemy-
mediated apparent competition (Chaneton &
Bonsall, 2000). Such asymmetry, however, does not
necessarily increase the likelihood that one of the
competing species will be excluded. For example,
with parasite-mediated apparent competition, ex-
clusion of vulnerable host species is dependent on
the transmission of parasites from ‘ reservoir ’ host
species (Tompkins et al. 2000 a). Hence, if parasite
impact were greater on a reservoir host and lesser on
a vulnerable host, the probability that such exclusion
would actually occur may be reduced through 2
concurrent mechanisms. First, parasite-induced re-
ductions in reservoir population size\density may
decrease the ‘ force of infection ’ to which the
vulnerable host was exposed whilst, second, the
lesser impact on the vulnerable host would mean that
more infection would be required to cause exclusion.
The possibility of exclusion could only be increased
if the opposite were true – a lesser impact on a
reservoir host may increase the force of infection to
which a vulnerable host was exposed whilst a greater
impact on a vulnerable host would mean that less
infection would be required to cause exclusion. This
second scenario describes the role which the dif-
ferential impact of H. gallinarum plays in the
pheasant\partridge system – for example, if parasite
impact on host fecundity was either 99 % higher for
the pheasant or 75 % lower for the partridge the
predicted outcome would switch from partridge
exclusion to host coexistence (Tompkins et al.
2000 b). Thus, verification that the impact of H.
gallinarum is indeed as high on the grey partridge
and as low on the ring-necked pheasant as the
correlational work suggests is essential to this
demonstration of apparent competition.
  
Infection experiment
Heterakis gallinarum effects on host body mass, food
consumption, and caecal activity were directly
quantified for both the ring-necked pheasant and the
grey partridge through the controlled experimental
infection of individually caged birds. Both species
were reared from day-old chicks on sterilized
concrete to ensure that all birds were naive to
parasites. Absence of infection was confirmed at 12
weeks of age through the culling and detailed
examination of 5 individuals of each species.
The H. gallinarum eggs used in this study were
from worms collected from pheasants that had
acquired natural infections on a Scottish gamebird
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https://doi.org/10.1017/S0031182001007247
188
estate where previous sampling had confirmed the
absence of Histomonas gallinarum (a protozoan
parasite that can be transmitted via H. gallinarum
eggs ; Lund & Chute, 1972). Female worms were
maintained for 21 days in 0n5 % formalin solution at
21 mC to embryonate all viable eggs, and broken
down in saline solution using a small electric blender.
Embryonated eggs were then counted in 10i0n1 ml
samples, and the volume of saline adjusted to 100
embryonated eggs\ml.
Infections were carried out on the 21st day of the
embryonation period, when the recipient hosts were
12 weeks of age. Nine individuals of each host
species were randomly selected and given a single
oral dose of approximately 100 embryonated H.
gallinarum eggs, via a tube into the birds crop. This
is a realistic challenge since H. gallinarum burdens in
the low hundreds are common (Tompkins &
Hudson, 1999 ; Draycott et al. 2000). A single
challenge was chosen over a continuous challenge
since hosts are likely to be exposed to ‘ clumps ’ of H.
gallinarum eggs in the wild, due to the highly
aggregated nature of this parasite (Tompkins &
Hudson, 1999 ; Draycott et al. 2000). However, even
if this is not the case, work on other gamebird\
nematode systems indicates that the infection re-
sulting from a single challenge is not significantly
different from that resulting from a continuous
challenge (Shaw & Moss, 1989). Nine other in-
dividuals of each species were treated as controls and
given 1 ml of saline containing no nematode eggs.
All birds were weighed to the nearest 5 g at the
start of the experiment and then maintained in their
individual cages (on wire mesh floors) for the
following 100 days, during which body mass was
monitored at 25-day intervals. Preliminary infection
trials indicated that the approximate life-expectancy
of H. gallinarum worms infecting pheasants is 100
days (unpublished data). Food (gamebird main-
tenance pellets), water and grit were supplied ad
libitum, with the mass of pellets provided being
recorded whenever hoppers were re-filled. The
caecal droppings produced by each bird were
collected at 5-day intervals and weighed to the
nearest 0n1 g. To confirm that experimental birds
were successfully infected, 0n5 g of each sample
collected was suspended in 10 ml of saturated salt
solution and H. gallinarum eggs counted, using
McMasters chambers under 100i magnification, in
5i0n1 ml subsamples. At the end of the study all
birds were culled and their body condition estimated
by measuring the breast muscle mass of each bird to
the nearest 0n01 g and adjusting for host body size
(see Tompkins et al. (1999) for further details).
For each host species, the body mass, food
consumption and caecal activity of control versus
experimentally challenged birds were compared over
the course of the experiment using the repeated
measures analysis of variance module in StatisticaTM
 Differential impact of a shared parasite
B challenged, 100 days earlier, with approximately 100
Fig. 1. Comparison of body mass between control birds
and (A) partridges and (B) pheasants orally challenged
with approximately 100 embryonated Heterakis
gallinarum eggs. Means and standard errors are shown
for 6 control (#) versus 8 experimental ($) partridges,
and 6 control (4 male (#) and 2 female (W)) versus 6
experimental (3 male ($) and 3 female (X)) pheasants.
For the pheasant, body mass was significantly different
between the sexes both at the beginning of the study
(F , l 20n98, P l 0n002) and at 25–100 days post-
")
infection (F , l 33n65, P 0n001).
")
v. 5.5, 1999. Both food consumption and caecal
dropping production were summed over 25-day
intervals for each individual. Host sex was included
as a factor in all analyses, being discarded when non-
significant.

Over the course of the infection experiment, 6
pheasants and 4 partridges were euthanased due to
husbandry problems unrelated to parasite infection.
For the remaining birds, observed parasite effects on
the host were greater in the grey partridge than in the
ring-necked pheasant, even though the level of
established infection appeared to be far lower in
partridges than in pheasants. During the 100 day
trial period, the mean (p..) number of H.
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https://doi.org/10.1017/S0031182001007247
189
Fig. 2. Comparison of body condition between control
birds and both partridges and pheasants orally
embryonated Heterakis gallinarum eggs. Means and
standard errors are shown for 6 control versus 8
experimental partridges, and 6 control versus 6
experimental pheasants.
gallinarum eggs expelled in the caecal droppings of
challenged partridges was only 43p84 eggs\day,
with eggs detected in the droppings of only 2 of the
8 experimental birds, compared to 3793p7636
eggs\day in the droppings of challenged pheasants
(see Tompkins et al. (2000 b) for further details).
Host body mass and condition
While the body mass of control and experimental
partridges was similar at the beginning of the study
(Fig. 1 A ; F , l 0n01, P l 0n91), infection resulted
" "#
in experimental birds being 11 % lighter than control
birds at 25–100 days post-challenge (Fig. 1 A ; F ,
" "#
l 6n12, P l 0n03). No such pattern was observed for
the pheasant, however, where the body mass of
control and experimental birds was similar both at
the beginning of the study (Fig. 1 B ; F , l 0n00, P
" ")
l 0n95) and post-challenge (Fig. 1 B ; F , l 0n00, P
")
l 0n99). The general increase in body mass over the
course of the infection trial reflects the last stages of
growth of the juvenile birds involved. Thus the
parasite reduced the growth rate of partridges but
not of pheasants.
The body condition of control versus experimental
birds at the end of the infection trial was not
significantly different for either the pheasant (Fig.
2 A ; F , l 0n01, P l 0n91) or the partridge (Fig.
" "!
2 A ; F , l 2n30, P l 0n15).
" "#
Host food consumption
A significant effect of infection on partridge food
consumption was detected as an interaction with
days post-challenge (Fig. 3 A). There was no sig-
nificant difference between control and experimental
groups over the full 100 days of the study (F , l
" "#
 D. M. Tompkins, J. V. Greenman and P. J. Hudson
A A
B B
Fig. 3. Comparison of food consumption between
control birds and (A) partridges and (B) pheasants orally
challenged with approximately 100 embryonated
Heterakis gallinarum eggs. Means and standard errors
are shown for 6 control (#) versus 8 experimental ($)
partridges, and 6 control (4 male (#) and 2 female (W))
versus 6 experimental (3 male ($) and 3 female (X))
pheasants. For the pheasant, food consumption over the
course of the study was significantly different between
the sexes (F , l 40n40, P 0n001).
")
1n61, P l 0n23), although control birds consumed
19 % more in the first half of the study while
experimentally challenged birds consumed 9 % more
in the second half of the study (F , l 4n57, P l
$ $'
0n008).
Again there was no detectable effect of infection on
the pheasant (Fig. 3 B) ; food consumption by control
and experimental birds was not significantly different
(F , l 1n20, P l 0n31). The general decrease in food
")
consumption over the course of the infection trial
may reflect the reduced demands associated with a
slow down in growth of the juvenile birds involved.
Host caecal activity
The mass of caecal droppings produced over the
course of the study was significantly lower in
experimentally challenged birds than in controls for
both partridges (F , l 7n74, P l 0n02) and pheasants
" "#
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https://doi.org/10.1017/S0031182001007247
190
Fig. 4. Comparison of caecal dropping production
between control birds and (A) partridges and (B)
pheasants orally challenged with approximately 100
embryonated Heterakis gallinarum eggs. Means and
standard errors are shown for 6 control (#) versus 8
experimental partridges ($), and 6 control (#) versus 6
experimental ($) pheasants.
(F , l 6n64, P l 0n03). On average, challenged
" "!
partridges produced 32 % less caecal droppings than
control partridges (Fig. 4 A) while challenged
pheasants produced 23 % less caecal droppings than
control pheasants (Fig. 4 B).
Impact on the grey partridge
Although the body condition of control and ex-
perimental partridges at the end of the infection trial
was not significantly different (Fig. 2), the body
condition of the 2 partridges for which H. gallinarum
eggs were detected in caecal droppings was signifi-
cantly lower than that of the other 6 experimental
partridges for whom parasite eggs were not detected
(Fig. 5 ; F , l 21n01, P l 0n004). These birds were
"'
also 21 % lighter than the other 6 experimental
partridges at 25–100 days post-challenge (F , l
"'
48n28, P 0n001) and ate 13 % less food (F , l 8n19,
"'
P l 0n03), although there was no significant dif-
ference in the mass of caecal droppings produced
(F , l 1n65, P l 0n25).
"'
 Differential impact of a shared parasite
Fig. 5. Box and whiskers plot comparing the body
condition of those partridges, orally challenged 100 days
earlier with approximately 100 embryonated Heterakis
gallinarum eggs, for which H. gallinarum eggs were
detected in caecal droppings (n l 2) versus those for
which eggs were not detected (n l 6).
The impact of H. gallinarum was thus greater on 2
of the 8 challenged partridges. However, there was
still a deleterious effect of parasite challenge on the
other 6, who were 6 % lighter than control partridges
at 25–100 days post-challenge (F , l 4n89, P l
" "!
0n05), produced 28 % less caecal droppings (F , l
" "!
4n82, P l 0n05), and for whom there was still a
significant effect of treatment on food consumption
detectable as an interaction with days post-challenge
(control birds consumed 10 % more in the first half
of the study, the 6 consumed 6 % more in the second
half of the study ; F , l 3n10, P l 0n04).
$ $!

Previous correlational work has suggested that while
infections of the caecal nematode H. gallinarum have
no detectable effect on ring-necked pheasants their
impact on grey partridges is of a magnitude likely to
cause reductions in host fecundity and survival
(Tompkins et al. 1999, 2000 a). In demonstrating
that H. gallinarum causes a significant reduction in
the weight gain and food consumption of partridges,
but not of pheasants, the controlled experimental
infections conducted in this study show that such a
differential impact is indeed the case. There are,
however, some detectable effects of H. gallinarum on
the pheasant – a significant decrease in caecal drop-
ping production was observed in this study for
challenged individuals of both host species. Since
the avian caecum may play an important role in
nutrient absorption (Clench & Mathias, 1995), such
an effect on caecal activity could reduce pheasant
fecundity and survival in the wild, particularly if
food is limiting (Holmes, 1995 ; Coop & Holmes,
1996). Further work is required to test this hy-
pothesis. Since there is some evidence from parasite
removal experiments that nematodes do reduce
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https://doi.org/10.1017/S0031182001007247
191
pheasant reproductive success in the field, a rela-
tively minor impact of H. gallinarum on pheasant
fecundity was included in the initial parameterization
of the pheasant\partridge\H. gallinarum model
(Tompkins et al. 2000 b). In light of the current
experiment, however, the actual impact may be
greater.
One possible confounding factor in the results
observed here is that, since the H. gallinarum eggs
used for the experimental infections were derived
from naturally infected pheasants, they may have
been adapted to this host and thus had a less
pathogenic effect on pheasants and a greater patho-
genic effect on partridges than they would otherwise.
Indeed, adaptations of H. gallinarum to particular
host species have been demonstrated previously
(Lund, Chute & Myers, 1970). However, since the
basic reproductive rate (Ro ; the number of adult
female parasites derived from each adult female
parasite in a population of uninfected hosts) for H.
gallinarum in the partridge is far below unity
(estimated as 0n006 ; Tompkins et al. 2000 b), most, if
not all, of the parasites infecting partridges in the
wild must be derived from other host species. Since
the pheasant is the main reservoir host of H.
gallinarum (Lund & Chute, 1974 ; Draycott et al.
2000), in which parasite Ro has been estimated as
1n23 (Tompkins et al. 2000 b), H. gallinarum eggs of
pheasant origin are the correct ones to use when
investigating the impact of this parasite on the grey
partridge.
Failure to gain weight, inappetence (reduction in
voluntary food intake), and the disruption of normal
gastrointestinal function, as observed in this study,
are all common clinical consequences of infection by
gastrointestinal nematodes (Holmes, 1987). For
many hosts, these effects are believed to be prin-
cipally caused not by the established adult worms
but rather by the developing larvae (e.g. Sadun,
1950 ; Williams et al. 1983 ; Ovington, 1985 ; Shaw &
Moss, 1990). Since, in the current study, food
consumption of grey partridges was only reduced up
to 50 days post-challenge and increased (possibly in
compensation) thereafter, and by 100 days post-
challenge there was no significant difference in the
body condition of control and challenged partridges,
the same may be true for H. gallinarum infections
(where larvae infecting partridges mature after
approximately 40 days ; Tompkins et al. 2000 b).
Greater deleterious effects of larval as opposed to
adult H. gallinarum would not be surprising since
only the larvae have a tissue stage which can damage
the caecal mucosa and possibly elicit host inflamma-
tory responses (Kaushik & Sharma Deorani, 1969).
Such damage could potentially affect caecal activity,
as was observed.
The lack of a significant difference in the body
condition of control and experimental partridges at
the end of the infection trial was due to a greater level
 D. M. Tompkins, J. V. Greenman and P. J. Hudson
A individuals than on others. However, even though
B
Fig. 6. Exclusion – coexistence boundary curves in the
parasite-induced increase in partridge mortality\
parasite-induced decrease in partridge fecundity cross-
section of parameter space for the pheasant\partridge\
H. gallinarum model detailed by Tompkins et al.
(2000 b) illustrating how the boundary shifts as (A)
the parasite-induced decrease in pheasant fecundity
is increased logarithmically from its estimated
value of 8n28i10V%\worm\year (curve a) to
8n28i10V$\worm\year (curve b), and (B) the parasite-
induced increase in pheasant mortality is increased
linearly from 0n00 (curve a) to 3n00i10V$\worm\year
(curve b). The parameters on both axes are scaled from
0n1 to 10 times their empirical values. Crosses indicate
the predicted outcome at the empirical values. The
outcome shifts from partridge exclusion to host
coexistence when either the decrease in pheasant
fecundity is increased to 1n65i10V$\worm\year, or the
increase in pheasant mortality is increased to
5n33i10V%\worm\year.
of variance in the condition of challenged indi-
viduals. Such an increase is a common effect of
parasite infection on animal populations (Whitlock,
1961), and in this case was caused by the parasite
challenge having greater deleterious effects on some
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https://doi.org/10.1017/S0031182001007247
192
not significant, the magnitude of the overall dif-
ference was equivalent to that recorded in the
previous correlational studies. Since the establish-
ment success of H. gallinarum infecting the grey
partridge is 6n5 % (Tompkins et al. 2000 b), the
effects observed in this study (where individuals
were challenged with approximately 100 H. gallin-
arum eggs each) are related to a mean established
parasite intensity of 6n5 worms. This is equivalent to
a decrease in body condition of 2n0 g breast muscle
mass\worm, which is consistent with the 1n1–2n5
g\worm range seen in the correlational data
(Tompkins et al. 1999 ; Tompkins et al. 2000a).
In verifying that H. gallinarum is a cause of
decreased body condition in gamebirds, and clearly
showing that it does indeed have differential impacts
on the ring-necked pheasant and the grey partridge,
this study has accomplished its goal. The exper-
imental results documented here, however, have
contrasting implications for the prediction that
parasite-mediated apparent competition between the
pheasant and the grey partridge results in partridge
exclusion. Since the impact of H. gallinarum on
challenged partridges was of a magnitude similar to
that previously suggested by the correlational data,
the deleterious effects of this parasite do appear to be
sufficient to cause partridge exclusion. However, the
possibility that H. gallinarum may have an impact on
pheasants that is greater than is currently included in
the 2 host shared-macroparasite model of the system
could mean that the force of infection from pheasants
to partridges in the wild may not be sufficient for
such exclusion to actually occur. The shift in model
outcome from exclusion to host coexistence due to
this effect is illustrated in Fig. 6, demonstrating how
the inter-specific transmission of parasites from
reservoir to vulnerable hosts decreases as the parasite
impact on the reservoir host increases.
We wish to thank Pauline Monteith for her assistance in
the laboratory, and Roger Draycott for comments on the
manuscript. This work was funded by NERC project
grant GR3\10647.

, . .  , . . (1997). Apparent
competition structures ecological assemblages. Nature,
London 388, 371–373.
, . .  , . . (2000). Enemy-
mediated apparent competition : empirical patterns
and the evidence. Oikos 88, 380–394.
, . .  , . . (1995). The avian cecum :
a review. Wilson Bulletin 107, 93–121.
, . .  , . . (1996). Nutrition and
parasite interaction. International Journal for
Parasitology 26, 951–962.
, ., , . .  , . . (2000).
Emerging infectious diseases of wildlife – threats to
biodiversity and human health. Science 287, 443–449.
 Differential impact of a shared parasite
, . . ., , . . ., , . . .
 , . . (2000). Spring survey of the parasite
Heterakis gallinarum in wild-living pheasants in
Britain. Veterinary Record 147, 245–246.
, . . (1983). Parasites and the coexistence of
animal host species. American Naturalist 121,
223–236.
, . . . (1995). Impact of infectious diseases
on wild animal populations, a review. In Ecology of
Infectious Diseases in Natural Populations (ed.
Grenfell, B. T. & Dobson, A. P.). Cambridge
University Press, Cambridge.
, . . . (1949). Disease and evolution. La
Ricercha Scientifica Suppl. 19, 68–76.
, . . (1995). Population regulation : a dynamic
complex of interactions. Wildlife Research 22, 11–19.
, . . (1987). Pathophysiology of parasitic
infections. Parasitology 94, S29–S51.
, . . (1977). Predation, apparent competition, and
the structure of prey communities. Theoretical
Population Biology 12, 197–229.
, . .  , . . (1994). The ecological
consequences of shared natural enemies. Annual
Review of Ecology and Systematics 25, 495–520.
, .  , . (1998). Competition
mediated by parasites : biological and theoretical
progress. Trends in Ecology and Evolution 13, 387–390.
, . .   , . . (1969). Studies
on tissue responses in primary and subsequent
infections with Heterakis gallinae in chickens and on
the process of formation of caecal nodules. Journal of
Helminthology 43, 69–78.
, . .  , . . (1972). Reciprocal responses
of eight species of galliform birds and three parasites :
Heterakis gallinarum, Histomonas meleagridis, and
Parahistomonas wenrichi. Journal of Parasitology 58,
940–945.
, . .  , . . (1974). The reproductive
potential of Heterakis gallinarum in various species of
galliform birds : implications for survival of H.
gallinarum and Histomonas meleagridis to recent times.
International Journal for Parasitology 4, 455–461.
, . ., , . .  , . . (1970).
Performance in chickens and turkeys of chicken-
adapted Heterakis gallinarum. Journal of Helminthology
44, 97–106.
, . . (1985). Dose-dependent relationships
between Nippostrongylus brasiliensis populations and
rat food intake. Parasitology 91, 157–167.
Downloaded from https://www.cambridge.org/core. University of Debrecen, on 03 Jan 2018 at 11:52:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.1017/S0031182001007247
193
, . (1948). Experimental studies of interspecies
competition. I. Competition between populations of
the flour beetles, Tribolium confusum Duval and
Tribolium castaneum Herbst. Ecological Monographs
18, 265–307.
, . ., , ., , ., , . ., ,
. ., , . .  , . (1986). Parasite
mediation in ecological interactions. Annual Review of
Ecology and Systematics 17, 487–505.
, . . (1950). Studies on the pathogenicity in
chickens of single infections of variable size with the
nematode Ascaridia galli. Poultry Science 29, 712–722.
, . .  , . (1989). Factors affecting the
establishment of the caecal threadworm
Trichostrongylus tenuis in the red grouse (Lagopus
lagopus scoticus). Parasitology 99, 259–264.
, . .  , . (1990). Effects of the caecal
nematode Trichostrongylus tenuis on egg-laying by
captive red grouse. Research in Veterinary Science 48,
59–63.
, . .  , . (1999). Parasites regulate
wildlife populations. Parasitology Today 15, 311–313.
, . ., , .  , . . (1999).
Parasite-mediated competition between pheasant and
grey partridge : a preliminary investigation. Oecologia
119, 378–382.
, . ., , . . .  , . .
(2000 a). Field evidence for apparent competition
mediated via the shared parasites of two gamebird
species. Ecology Letters 3, 10–14.
, . .  , . . (1999). Regulation of
nematode fecundity in the ring-necked pheasant
(Phasianus colchicus) : not just density dependence.
Parasitology 118, 417–423.
, . ., , . ., , . . 
, . . (2000 b). The role of shared parasites in
the exclusion of wildlife hosts : Heterakis gallinarum in
the ring-necked pheasant and the grey partridge.
Journal of Animal Ecology 69, 829–840.
, . .  , . (1998). Wildlife disease
ecology : from theory to policy. Trends in Ecology and
Evolution 13, 476–478.
, . . (1961). Parasitology, biometry and
ecology. British Veterinary Journal 117, 337–348.
, . ., , . ., , . .  ,
. . (1983). Experimental and natural infection of
calves with Bunostomum phlebotomum. Veterinary
Parasitology 13, 225–237.