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The Role of Shared Parasites in the Exclusion of Wildlife Hosts: Heterakis Gallinarum in the Ring-Necked Pheasant and the Grey P

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The Role of Shared Parasites in the Exclusion of Wildlife Hosts: Heterakis Gallinarum in the Ring-Necked Pheasant and the Grey P Journal of Animal The role of shared parasites in the exclusion of wildlife Ecology 2000, 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 1Á23 when infecting pheasants, but only 0Á0057 when infecting partridges. Thus, when the pheasant is present in the model the par- tridge population is impacted by the shared parasite but, when the pheasant is absent, the parasite is lost from the system. 3. Based on best available parameter estimates, the observed impact of H. galli- narum on the grey partridge may be sucient to cause exclusion when the pheasant is present in the model. This supports the hypothesis that the UK grey partridge decline observed over the past 50 years may be partly due to apparent competition with pheasants. 4. Habitat separation between the two host species, where it decreases the rate of H. gallinarum transmission from the pheasant to the partridge, may allow them to co-exist in the ®eld in the presence of the parasite. We predict, however, that grey partridge exclusion would still occur if separation was less than 43%. 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; MuÈ ller & Godfray 1997; Bonsall & Hassell 1998; Indirect interactions between species may play a cri- Hudson & Greenman 1998). Under these circum- tical role in determining the community structure stances the density of shared enemies supported by and dynamics of ecological assemblages (Abrams each species individually will impact on both species et al. 1995; Menge 1997; Schmitz 1998). One form present. Since each of the two species can suer as a of such interaction is where two species, which do consequence of the presence of the other species, as not compete for resources, share natural enemies 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- Correspondence: Dr Daniel M. Tompkins, Institute of cies, with the species that persists being the one that Biological Sciences, University of Stirling, Stirling, FK9 # 2000 British 4LA, UK, [email protected], Tel.: 01786 467812, Fax: can tolerate the higher densities of shared enemies Ecological Society 01786 464994 (Holt & Lawton 1993; Bonsall & Hassell 1997). 830 Cases where host exclusion can be attributed to infection suggests that the pheasant acts as a reser- Apparent the presence of shared parasites are often cited as voir host for H. gallinarum, the negative impact of competition examples of apparent competition (e.g. Settle & Wil- which is greater on the partridge (Tompkins et al. mediated via son 1990; Grosholz 1992). However, conclusively 1999, 2000). This is supported by fully controlled shared parasites demonstrating that host exclusion is due to apparent experiments with singly housed birds, which clearly competition, as opposed to either direct competition demonstrate that the parasite is a cause of decreased or other parasite eects can be dicult to accom- body condition in the grey partridge and not vice- plish (as discussed in Hudson & Greenman 1998). A versa (D.M. Tompkins, in preparation). Therefore, recent series of controlled experiments, conducted this study will determine whether a two-host shared- on laboratory populations of two moth species (Plo- macroparasite model, parameterized from the results dia interpunctella and Ephestia kuehiella) and the of infection and transmission experiments, predicts parasitoid Venturia canescens, has provided the ®rst exclusion of the grey partridge due to apparent com- explicit demonstration of apparent competition petition with the ring-necked pheasant. mediated via a shared parasitoid (Bonsall & Hassell 1997, 1998). Providing an explicit demonstration is far harder to accomplish in natural systems, how- Methods ever, due to the logistical constraints involved. In T H E M O D E L E Q U A T I O N S many circumstances the controlled experiments required are unworkable. The majority of ®eld stu- The model used to describe the two-host shared- dies to date have thus been descriptive, often failing parasite system is illustrated in Fig. 1, and is de®ned to disentangle parasite eects from resource compe- by the following equations (for i,j 1,2; i 6 j): tition among hosts (e.g. Schall 1992; Schmitz & Nudds 1994; Hanley, Vollmer & Case 1995). dHi=dt riHi 1 Hi=Ki ai diPi eqn 1a De®nitive proof that apparent competition mediated via shared parasites occurs in the ®eld will dPi=dt fibiWHi mi bi aiPi require the large scale manipulation of host popula- 0 tions as employed in other gamebird-parasite studies aikiPi Pi=Hi eqn 1b (Hudson, Dobson & Newborn 1998; May 1999). It would be premature to conduct such an experiment dW=dt l1P1 l2P2 g W b WH1 with any natural system, however, without ®rst 0 1 demonstrating that model simulations run with the b2WH2 eqn 1c best available parameter estimates do, indeed, pre- dict that apparent competitive eects are of su- The model explores the dynamics of W, the num- cient magnitude to be detectable. This is in line with ber of free-living stages in the common infective th the view that mathematical modelling is a valuable pool, Pi, the adult parasite in the i host, and Hi, precursor to conducting population scale manipula- the host population. The natural exponential growth tions in the wild, in order to justify the time and of the host population (ri) in equation 1a is oset by expense involved (Tompkins & Begon 1999). The density dependent host mortality (with Ki being the aim of this study is to provide such a demonstration carrying capacity) and by the parasite induced for two gamebirds, the ring-necked pheasant [Pha- eects on host survival (ai) and fecundity (di). The sianus colchicus (L.)] and the grey partridge [Perdix number of free living stages (equation 1c) increases perdix (L.)], investigating whether the biology of the through the deposition of worm eggs (li) and shared caecal nematode Heterakis gallinarum decreases through both natural mortality (g0) and (Schrank) could result in exclusion of the partridge. ingestion of eggs by the host (bi). The number of H. gallinarum occurs in several species of galliform parasitic worms (equation 1b) increases with the birds, transmitted via an actively ingested egg stage ingestion of eggs by hosts (bi), modi®ed by the pro- (Lund & Chute 1974). portion that survive to become mature worms (fi), Numbers of wild grey partridge have declined and decreases due to the combined eects of worm dramatically in the UK within the past 50 years mortality (mi), and natural (bi) and infection-induced (Tapper 1992). This decline is linked primarily to (ai) host mortality. The natural host mortality rate the intensi®cation of agriculture and increased pre- (bi) incorporates density dependence, whereby bi dation pressure (Potts 1986, 1997; Sotherton 1998), bi0 riHi/Ki. The natural host birth rate is ai, with as supported by large scale ®eld experimentation the net population growth rate at low population (Rands 1985; Tapper, Potts & Brockless 1996). levels expressed as ri ai bi0. The last term in However, recent studies indicate that apparent com- equation 1b models parasite mortality arising from # 2000 British petition with the ring-necked pheasant may also be parasite-induced host deaths, assuming a negative Ecological Society involved (Wright et al. 1980; Tompkins, Dickson & binomial distribution of parasites among hosts Journal of Animal 0 Ecology, 69, Hudson 1999; Tompkins, Draycott & Hudson (Anderson & May 1978). Parameter ki equals 1 1/ 829±840 2000). The experimental exposure of naive birds to 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. 1 inverse measure of aggregation. A full list of para- where u1i K i and u2i (ai di)/ri. These coe- meters is given in Table 1. cients scale the host density dependence and parasite In terms of parasite intensity Zi Pi/Hi (M. eect terms, respectively. The transformed equations Roberts, personal communication), the equations involve two composite parameters: (i) si (mi ai become (for i 6 j): ai), measuring the loss of parasite intensity due to both adult parasite and infection-induced host mor- dHi=dt riHi 1 u1iHi u2iZi eqn 2a tality, and dilution through host births, and (ii) ei ai/ki di, where di is the parasite-induced reduction 2 dZi=dt fibiW siZi eiZi eqn 2b in host fecundity. Parameter ei therefore relates parasite-induced mortality and the reduction in fecundity.
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