Density-dependence in parasite transmission dynamics

The transmission of vector-borne parasites is complex, yet to a large extent this complexity can be unravelled through the insights gained from simple mathematical models of the transmission system. The principle is simple because the key question is merely "what is the rate of increase in numbers of hosts affected?" Clearly, if this rate of increase is greater than unity then the infection can spread, while if it is less than unity it will decline. Ronald Ross in 1911 was the first to formulate this idea for malarial(1) and malaria transmission has since attracted most attention from modellers of parasitic diseases(2-4). But although it is implicitly recognized that nothing- not even parasitic transmission - can increase indefinitely, the importance of some degree of density-dependence in regulating the system tends to be neglected (see Box 1). In this article, Klaus Dietz explores some classical ideas of modelling parasitic disease transmission, emphasizing not only the importance of density dependence but also the importance of knowing exactly where such effects operate in the system.     

Host densities as determinants of abundance in parasite communities

Several epidemiological models predict a positive relationship between host population density and abundance of directly transmitted macroparasites. Here, we generalize these, and test the prediction by a comparative study. We used data on communities of gastrointestinal strongylid nematodes from 19 mammalian species, representing examination of 6670 individual hosts. We studied both the average abundance of all strongylid nematodes within a host species, and the two components of abundance, prevalence and intensity. The effects of host body weight, diet, fecundity and age at maturity and parasite body size were controlled for directly, and the phylogenetically independent contrast method was used to control for confounding factors more generally. Host population density and average parasite abundance were strongly positively correlated within mammalian taxa, and across all species when the effects of host body weight were controlled for. Controlling for other variables did not change this. Even when looking at single parasite species occurring in several host species, abundance was highest in the host species with the highest population density. Prevalence and intensity showed similar patterns. These patterns provide the first macroecological evidence consistent with the prediction that transmission rates depend on host population density in natural parasite communities.     

Pollutant-induced effects on immunological and physiological interactions in aquatic host-trematode systems: implications for parasite transmission

Under conditions of pollution both host and parasite are susceptible to the pathogenic effects of toxicants, which in turn may result in detrimental changes to their immunological and physiological processes. Digenetic trematodes, which encompass species of both medical and economic importance, possess complex life cycles and are common parasites of both vertebrates and molluscs. The combined stress induced by pollution and parasitism influences the physiology of the host which can have implications not only on host survival but also on the functional biology of resident parasite populations. The present paper reviews the effects of pollutants on the immunology and physiology in both vertebrate and molluscan host-trematode systems and the implications for parasite transmission.     

Immune responses and parasite transmission in blood-feeding insects

The detailed model of insect immunity being built for Drosophila, allied to mass sequencing programs for blood-feeding insects, has led to advances in our understanding of the interaction between pathogens and insect vectors. An outline of insect immunity is given here based on the Drosophila studies, which is used as a framework to discuss recent work on Plasmodium-mosquito and Trypanosoma-tsetse interactions.     

Bottom–up regulation of parasite population densities in freshwater ecosystems

Theory predicts the bottom–up coupling of resource and consumer densities, and epidemiological models make the same prediction for host–parasite interactions. Empirical evidence that spatial variation in local host density drives parasite population density remains scarce, however. We test the coupling of consumer (parasite) and resource (host) populations using data from 310 populations of metazoan parasites infecting invertebrates and fish in New Zealand lakes, spanning a range of transmission modes. Both parasite density (no. parasites per m²) and intensity of infection (no. parasites per infected hosts) were quantified for each parasite population, and related to host density, spatial variability in host density and transmission mode (egg ingestion, contact transmission or trophic transmission). The results show that dense and temporally stable host populations are exploited by denser and more stable parasite populations. For parasites with multi‐host cycles, density of the ‘source’ host did not matter: only density of the current host affected parasite density at a given life stage. For contact‐transmitted parasites, intensity of infection decreased with increasing host density. Our results support the strong bottom–up coupling of consumer and resource densities, but also suggest that intraspecific competition among parasites may be weaker when hosts are abundant: high host density promotes greater parasite population density, but also reduces the number of conspecific parasites per individual host.     

The role of salivary vasodilators in bloodfeeding and parasite transmission

In this paper, Donald Champagne reviews the salivary vasodilators, points to effects of similar compounds that may be shared by the insect substances, and discusses the potential significance of these effects with regard to parasite transmission.     

Gut microbiota and parasite transmission by insect vectors

In the gut of some insect vectors, parasites ingested with the bloodmeal decrease in number before coming into contact with host tissues. Many factors could be responsible for this reduction in parasite number but the potentially important role of the large communities of naturally occurring microorganisms that exist alongside the newly ingested parasites in the vector midgut has been largely overlooked. Some previous reports exist of the inhibition of parasite development by vector gut microbiota and of the killing of Trypanosoma cruzi and Plasmodium spp. by prodigiosin produced by bacteria. Based on this evidence, we believe that the microbiota present in the midgut of vector insects could have important roles as determinants of parasite survival and development in insect vector hosts and, therefore, contribute to the modulation of vector competence for many important diseases.     

Constraints on parasite fecundity and transmission in an insect-STD system

Parasites that are sexually transmitted (causing sexually transmitted diseases, or STDs) can have important effects on host population dynamics, but we know almost nothing for such parasites about constraints on fecundity and transmission. In this study, we have examined the effect of two potentially important constraints in one of the few empirically well-studied animal-STD systems, the ladybird, Adalia bipunctata , and its sexually transmitted mite, Coccipolipus hippodamiae . Using a factorial design, we manipulated: (i) within-host competition, by varying infection intensity; and (ii) host condition, by introducing dietary stress. Infection with C . hippodamiae significantly reduced ladybird survival whether or not diet was restricted, and restricting diet led to reduced survival regardless of infection status. Increased infection intensity and reduced host condition (dietary stress) both independently constrained per capita rates of parasite egg production and the development of infective larvae. Furthermore, when host condition was compromised, significantly fewer larvae were transmitted per adult mite during copulation. The effect of infection intensity on per mite transmission was more complex: there was no significant effect when hosts were fed normally, but when the ladybirds were nutritionally stressed higher infection intensity was associated with a slight increase in the numbers that were transmitted (despite the fact that mite fecundity was reduced under these conditions). These results indicate that host condition and within-host competition may both play an important role in shaping the epidemiology of the A . bipunctata – C . hippodamiae system, by influencing the parasite's basic reproductive ratio (R₀) and the rate of epidemic spread. Our data also extend general insights into STD ecology, by highlighting the importance of constraints on disease dynamics that are likely to be widespread.     

Sex-specific differences in shoaling affect parasite transmission in guppies

Background

Individuals have to trade-off the costs and benefits of group membership during shoaling behaviour. Shoaling can increase the risk of parasite transmission, but this cost has rarely been quantified experimentally. Guppies (Poecilia reticulata) are a model system for behavioural studies, and they are commonly infected by gyrodactylid parasites, notorious fish pathogens that are directly transmitted between guppy hosts.

Methodology/Principal Findings

Parasite transmission in single sex shoals of male and female guppies were observed using an experimental infection of Gyrodactylus turnbulli. Parasite transmission was affected by sex-specific differences in host behaviour, and significantly more parasites were transmitted when fish had more frequent and more prolonged contact with each other. Females shoaled significantly more than males and had a four times higher risk to contract an infection.

Conclusions/Significance

Intersexual differences in host behaviours such as shoaling are driven by differences in natural and sexual selection experienced by both sexes. Here we show that the potential benefits of an increased shoaling tendency are traded off against increased risks of contracting an infectious parasite in a group-living species.     

Different transmission strategies of a parasite in male and female hosts

We investigated whether a parasite with two routes of transmission responds to the different transmission opportunities offered by male and female hosts by using different transmission strategies in the two sexes. The parasite Ascogregarina culicis, which infects the mosquito Aedes aegypti, can be transmitted as its host’s pupa transforms into an adult or when a female lays its eggs. As the latter transmission route is missing in males, we expected, and found, that the parasite releases a greater proportion of its infectious forms during emergence when it is within a male than when it infects a female. The transmission route, which influences the parasite’s dispersal and the evolution of its virulence, was also affected by the dose of infection and the parasite’s previous transmission route. Our results emphasize the complexity underlying the development of parasites and show their ability to tune their strategy to their environment.     

Low parasite infestations in high densities: The paradox of woodpigeons in urban areas

The type of habitat occupied by avian populations has a marked effect on the parasitises they host. The growth of cities and urban areas in recent decades has favoured some species of birds adapted to these types of habitats – urban exploiters – although the effects of urbanisation on the parasitism of wildlife are not always well known. This study compares the ectoparasites characteristic of two differentiated populations of woodpigeons, one located in a predominantly urban environment and the other in a rural one. Most of the species found were chewing lice, with Columbicola claviformis and Campanulotes bidentatus being dominant. Despite the higher density of the urban population, woodpigeon individuals were characterised by a lower abundance of chewing lice, as well as the presence of ectoparasites typical of feral pigeons such as Hohorstiella lata and the hippoboscids fly, Pseudolynchia canariensis. Similarly, birds with lower weights showed a higher parasitic load, which became more noticeable in urban woodpigeons. The lower ectoparasite load of urban hosts represents a health advantage compared with rural populations, which could be one of the causes of greater growth and reproductive success in urban populations of woodpigeons.     

Changes in parasite transmission stage excretion after pheasant release

The production of parasite transmission stages was investigated in the faeces of 77 farm-bred ring-necked pheasants (Phasianus colchicus). Coccidian oocysts (Eimeria sp.), and nematode eggs (Heterakis sp., and Capillaria-like eggs) were recovered before and after release but all birds were treated prior to release. Treatment with fenbendazole significantly reduced the abundance of transmission-stage excretion for all parasites, and reduced the prevalence in the case of Eimeria sp. and Heterakis sp. Nonetheless, a significant increase in the excretion abundance for all parasites and in the prevalence of Eimeria sp. and Heterakis sp. was found after release. Eggs of Ascaridia sp. were found only after releasing, suggesting infection ocurred in the wild. A negative relationship was found between the pheasant body condition and Heterakis excretion abundance and a higher abundance of Capillaria sp. eggs in female birds. No significant relationship was found between parasite excretion abundance and pheasant survival. Despite this, results suggest that an increase in the excretion of parasite transmission stages follows the release of captive pheasants into the wild. This can in part explain restocking failures, but also means that autochtonous free-living birds may become exposed to new and potentially harmful pathogens. To avoid these risks it is proposed that improved prophylactic measures should be taken.     

Robust estimation of parasite component community richness.

The performance of 2 nonparametric estimators of species richness, the bootstrap (S(B)) and kth-order jackknife (S(Jk)), are compared using simulated parasite communities. The parameters of the simulation match those of an earlier comparison that favored S(B) as an estimator but did not include S(Jk). S(Jk) is the least biased of the 2 estimators. Whereas the bias of S(B) is significantly affected by true species richness and the proportion of rare species, the bias of S(Jk) is relatively insensitive to changes in these parameters, and is, therefore, recommended as a robust estimator of species richness.