D. M. Tompkins

Ectoparasite Virulence is Linked to Mode of Transmission

Theory suggests that the evolution of parasite virulence is linked to the dynamics of parasite transmission. All else being equal, parasites transmitted vertically from parents to offspring should be less virulent than parasites capable of horizontal transmission to unrelated hosts. This is because the fitness of vertically transmitted parasites is tightly linked to the reproductive success of the host, whereas the fitness of horizontally transmitted parasites is relatively independent of host reproduction. The virulence-transmission relation has seldom been tested because of difficulties inherent in comparing virulences of different parasite-host systems. We compared the virulence of lice and mites infesting a single group of captive rock doves (Columba livia). Lice, which were vertically transmitted, had no detectable effect on host fitness, whereas horizontally transmitted mites drove host reproductive success to zero. These results, in conjunction with a survey of the literature, support the hypothesis that ectoparasite virulence is linked to the mode of transmission.

Reciprocal Natural Selection on Host‐Parasite Phenotypes

Coevolution is evolution in one species in response to selection imposed by a second species, followed by evolution in the second species in response to reciprocal selection imposed by the first species. Although reciprocal selection is a prerequisite of coevolution, it has seldom been documented in natural populations. We examined the feasibility of reciprocal selection in a simple host‐parasite system consisting of feral pigeons (Columba livia) and their Ischnoceran feather lice (Phthiraptera: Insecta). We tested for a selective effect of parasites on hosts with experimentally altered defenses and for a selective effect of host defense on a component of parasite escape. Previous work indicates that pigeons control lice through efficient preening, while lice escape from preening using complex avoidance behavior. Our results show that feral pigeons with impaired preening, owing to slight bill deformities, have higher louse loads than pigeons with normal bills. We use a controlled experiment to show that high louse loads reduce the survival of pigeons, suggesting that lice select for efficient preening and against bill deformities. In a reciprocal experiment, we demonstrate that preening with a normal bill selects for small body size in lice, which may facilitate their escape from preening. The results of this study verify a crucial element of coevolutionary theory by identifying likely targets of reciprocal phenotypic selection between host and parasite.

Comparative effects of mites and lice on the reproductive success of rock doves (Columba livia)

We report experimental data comparing the effects of Mesostigmatid mites and Ischnoceran lice on the reproductive performance of a single group of captive rock doves (Columba livia). Several components of host reproductive success were compared for the two groups, including number of eggs laid, hatching success, nestling growth rates, fledging success, post-fledging body mass and survival. Adult body mass and survival were also compared. There was a dramatic difference in the effects of the mites and lice. The former drove host reproductive success to zero, mainly by agitating adults and causing them to incubate eggs less faithfully. Nestling growth rates and post-fledging survival were also significantly reduced by mites. Lice showed no effect on reproductive success whatsoever, even though the feather damage they cause is known to have energetic consequences (Booth, Clayton & Block, 1993). Neither parasite had a significant effect on adult birds. Although Ischnocera are found on most species of birds, our results for lice constitute the first experimental test of the impact of Ischnocera on avian reproductive success (preliminary report by Clayton & Tompkins, 1994). We discuss reasons for the different effects of mites and lice, including the relationship of horizontal (mites) and vertical (lice) transmission to the evolution of virulence.

The role of shared parasites in the exclusion of wildlife hosts: Heterakis gallinarum in the ring‐necked pheasant and the grey partridge

1. A two-host shared-macroparasite model was parameterized from the results of infection and transmission experiments, to investigate whether apparent competition between the ring-necked pheasant (Phasianus colchicus) and the grey partridge (Perdix perdix), mediated via the shared nematode Heterakis gallinarum, could theoretically 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 pheasants, 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 partridge 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. gallinarum on the grey partridge may be sufficient 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 field in the presence of the parasite. We predict, however, that grey partridge exclusion would still occur if separation was less than 43%.

Regulation of nematode fecundity in the ring-necked pheasant (Phasianus colchicus): not just density dependence.

Patterns of nematode fecundity were investigated for infections of the caecal worm Heterakis gallinarum in the ring-necked pheasant (Phasianus colchicus). Worm length was a good predictor of parasite fecundity. After controlling for worm length no other factors, including parasite intensity, were related to worm fecundity. Density dependence in worm size was detected in natural infections at parasite intensities above a threshold of 96 worms (worm size decreased with increasing parasite intensity). However, below this threshold, worm size actually decreased with decreasing parasite intensity (inverse density dependence). The interaction between density dependence and inverse density dependence in regulating the development and subsequent fecundity of H. gallinarum worms in ring-necked pheasants was demonstrated in an infection experiment. Density dependence was observed in the stunted growth of worms in heavily infected hosts, relative to worms in lightly infected hosts. Inverse density dependence in worm size was the common pattern across hosts by the end of the experiment, when parasite intensities were below the density dependence threshold. This is the first study to document both density dependence and inverse density dependence in parasite fecundity in the same host-helminth system.

Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus)

Understanding the factors controlling the distribution of parasites within their host population is fundamental to the wider understanding of parasite epidemiology and ecology. To explore changes in parasite aggregation, Taylors power law was used to examine the distributions of five gut helminths of the wild rabbit. Aggregation was found to be a dynamic process that varied with year, season, host sex, age class, and myxomatosis. Yearly and seasonal changes are thought, in the main, to be the result of variations in weather conditions acting upon infectious stages (or intermediate hosts). Evidence in support of this was the comparatively low degree of fluctuation in the aggregation of the pinworm, Passalurus ambiguus, as the infectious stage of this parasite is likely to be less susceptible to environmental variation. Host age had a marked effect on the level of aggregation of all parasites, but this effect varied between parasite species. P. ambiguus, Trichostrongylus retortaeformis and Cittotaenia denticulata aggregation were lower in adult than juvenile rabbits whilst Graphidium strigosum and Mosgovoyia pectinata aggregation tended to increase with age. Host immunity is thought to be responsible for these differences. Differences in aggregation for different parasites were also seen when the rabbit population was split into males and females. Myxomatosis had a marked effect on helminth distribution with substantially less aggregation in rabbits showing clinical signs of the disease.

Effect of vertically transmitted ectoparasites on the reproductive success of Swifts (Apus apus)

1. Parasites that are transmitted vertically from parent hosts to offspring are expected to be relatively benign, because their fitness depends on successful host reproduction. The effects of two species of vertically transmitted ectoparasite on the reproductive success of swifts (Apus apus L.) were tested. Populations of the Chewing Louse, Dennyus hirundinis (L.) (Phthiraptera: Menoponidae), and the Flightless Louse Fly, Crataerina pallida (Latreille) (Diptera: Hippoboscidae), were experimentally manipulated, effectively converting the natural aggregated frequency distribution of each species into a bimodal distribution of high and low loads. 2. Neither parasite had any effect on nestling growth or fledging success, even though parasite loads were boosted above natural levels and host environmental conditions were poor during part of the study, thus increasing the chances of detecting an effect of the parasites. 3. In contrast to parasite load, year, brood size and hatch date were all significantly related to components of nestling growth. Year and brood size were also significantly related to fledging success. 4. These results are consistent with theoretical models suggesting that vertically transmitted parasites evolve reduced virulence because they depend on host reproduction for dispersal to new hosts.

Stochasticity Accelerates Nematode Egg Development

Day-degrees models of nematode development assume that temperature stochasticity has no effect on the development rate of infective stages as long as the mean temperature is held constant. This assumption was tested in this study. Unembryonated Heterakis gallinarum eggs were subjected to nocturnal and diurnal daily temperature cycles at 12 and 17 C, respectively, and embryonation was compared with eggs subjected to similar stochastic daily cycles, in which random normal variations in the temperature were added to the 2 temperatures. The prediction that there is no effect of stochasticity was refuted. Embryonation of eggs subjected to variable daily cycles occurred significantly earlier than that of eggs subjected to deterministic daily cycles, suggesting that stochastic variation in temperature accelerated embryonation even though mean temperatures were the same. These findings show that the development time of H. gallinarum eggs is decreased by stochastic variation in temperature, which may have important implications for the effects of climate change on parasite availability.

The role of oxygen availability in the embryonation of Heterakis gallinarum eggs.

The importance of oxygen availability in the embryonation of the infective egg stages of the gastrointestinal nematode parasite Heterakis gallinarum was studied in the laboratory. Unembryonated H. gallinarum eggs were kept under either aerobic conditions by gassing with oxygen, or anaerobic conditions by gassing with the inert gas nitrogen, under a range of constant temperatures. Oxygenated eggs embryonated at a rate influenced by temperature. Conversely, eggs treated with nitrogen showed no embryonation although when these eggs were transferred from nitrogen to oxygen gas after 60 days of treatment, embryonation occurred. This demonstrated that oxygen is an essential requirement for H. gallinarum egg development, although undeveloped eggs remain viable, even after 60 days in low oxygen conditions. The effects of climate on the biology of free-living stages studied under constant laboratory conditions cannot be applied directly to the field where climatic factors exhibit daily cycles. The effect of fluctuating temperature on development was investigated by including an additional temperature group in which H. gallinarum eggs were kept under daily temperature cycles between 12 and 22 degrees C. Cycles caused eggs to develop significantly earlier than those in the constant mean cycle temperature, 17 degrees C, but significantly slower than those in constant 22 degrees C suggesting that daily temperature cycles had an accelerating effect on H. gallinarum egg embryonation but did not accelerate to the higher temperature. These results suggest that daily fluctuations in temperature influence development of the free-living stages and so development cannot be accurately predicted on the basis of constant temperature culture.

The dynamics of nematode transmission in the red grouse (Lagopus lagopus scoticus) : studies on the recovery of Trichostrongylus tenuis larvae from vegetation

Attempts to recover the infective third-stage larvae of Trichostrongylus tenuis from heather (Calluna vulgaris) vegetation in the field are rarely successful because the larvae may be: (i) concealed within heather leaflets; (ii) concentrated in dew droplets which are lost from the plants upon sampling; or (iii) simply highly aggregated in the field. Heather plants were exposed to T. tenuis larvae in the laboratory and kept under suitable conditions for larval migration. Few larvae were found in dew droplets or concealed within heather leaflets; most larvae were recovered from the plant surface. This suggests that the low larval recovery from vegetation in the field simply reflects a highly aggregated distribution of few larvae. In a second experiment, the efficiency with which infective larvae migrate up the structurally complex heather plants was compared with migration up two control plant species with simpler structures: a monocotyledon, wheat, and a dicotyledon, hebe. After constant exposure, significantly more larvae were recovered from heather than from either of the control plants. This implies that the structural complexity of heather causes no problems for the infective larvae.