Applying an aggregative dispersive dichotomy (ADD) model to parasitic infections in host populations

An aggregative dispersive dichotomy (ADD) model is presented to describe the distribution of parasites in host populations. The ADD model is a mathematical construct which provides two complementary measures extracted from a reformulated negative binomial (NBD) and an inequality model, which combine to capture observed patterns of a parasitic infection. The dispersion element is modelled using the NBD with the threshold set at a parasite level above zero. By applying binomial dichotomy, the host community is divided into two sub-populations, one including hosts harbouring parasites up to the threshold and the other with parasites above the threshold level. The k parameter, derived from the NBD, provides a cumulative probability. However, k is relatively insensitive to variations in the degree of aggregation, a known feature of the NBD model. The aggregation of parasites above the threshold in the host sub-population is evaluated by using an inequality model which is indexed by a scale-free parameter delta(delta >/= 1) and provides an accurate measure of parasite aggregation. Applications of this model are made from field and simulated data in wood mouse populations infected with the trichostrongylid nematode Heligmosomoides polygyrus from a woodland site in Surrey.     

Host manipulation by Ligula intestinalis: a cause or consequence of parasite aggregation?

Previous investigations suggest that the infection of the cyprinid roach, Rutilus rutilus, with the larval plerocercoid forms of the cestode, Ligula intestinalis, creates behavioural and morphological changes in the fish host, potentially of adaptive significance to the parasite in promoting transmission to definitive avian hosts. Here we consider whether these behavioural changes are important in shaping the distribution of parasite individuals across the fish population. An examination of field data illustrates that fish infected with a single parasite were more scarce than expected under the negative binomial distribution, and in many months were more scarce than burdens of two, three or more, leading to a bimodal distribution of worm counts (peaks at 0 and >1). This scarcity of single-larval worm infections could be accounted for a priori by a predominance of multiple infection. However, experimental infections of roach gave no evidence for the establishment of multiple worms, even when the host was challenged with multiple intermediate crustacean hosts, each multiply infected. A second hypothesis assumes that host manipulation following an initial single infection leads to an increased probability of subsequent infection (thus creating a contagious distribution). If manipulated fish are more likely to encounter infected first-intermediate hosts (through microhabitat change, increased ingestion, or both), then host manipulation could act as a powerful cause of aggregation. A number of scenarios based on contagious distribution models of aggregation are explored, contrasted with alternative compound Poisson models, and compared with the empirical data on L. intestinalis aggregation in their roach intermediate hosts. Our results indicate that parasite-induced host manipulation in this system can function simultaneously as both a consequence and a cause of parasite aggregation. This mutual interaction between host manipulation and parasite aggregation points to a set of ecological interactions that are easily missed in most experimental studies of either phenomenon.     

Aggregation patterns of helminth populations in the introduced fish, Liza haematocheilus (Teleostei: Mugilidae): disentangling host–parasite relationships

A number of hypotheses exist to explain aggregated distributions, but they have seldom been used to investigate differences in parasite spatial distribution between native and introduced hosts. We applied two aggregation models, the negative binomial distribution and Taylor’s power law, to study the aggregation patterns of helminth populations from Liza haematocheilus across its native (Sea of Japan) and introduced (Sea of Azov) distribution ranges. In accordance with the enemy release hypothesis, we predicted that parasite populations in the introduced host range would be less aggregated than in the native host area, because aggregation is tightly constrained by abundance. Contrary to our expectation, aggregation of parasite populations was higher in the introduced host range. However, the analyses suggested that the effect of host introduction on parasite aggregation depends on whether parasite species, or higher level taxonomic groups, were acquired in or carried into the new area. The revealed similarity in the aggregation parameters of co-introduced monogeneans can be attributed to the repeatability and identity of the host–parasite systems. In contrast, the degree of aggregation differed markedly between regions for higher level taxa, which are represented by the native parasites in the Sea of Japan versus the acquired species in the Sea of Azov. We propose that the host species plays a crucial role in regulating infra-population sizes of acquired parasites due to the high rate of host-induced mortality. A large part of the introduced host population may remain uninfected due to their resistance to native naïve parasites. The core concept of our study is that the comparative analysis of aggregation patterns of parasites in communities and populations, and macroecological relationships, can provide a useful tool to reveal cryptic relationships in host–parasite systems of invasive hosts and their parasites.     

The characteristics of the ixodid tick-vertebrate animal parasitic system]

The parasitic system ixodid tick (parasite)--vertebrate animal (host) is relatively stable in space and time. Equilibrium state in the system is maintained at the low levels of the hosts' infection and moderate intensity of their immunity. Parasite sensitizes the host's organism at the stage of feeding on antigens of its saliva and the host develops different degrees of resistance preventing the subsequent individuals of ticks from normal feeding. Antitick immunity is species specific. Its intensity is defined by the species belonging of the parasite and host, intensity and intervals between infections, availability of "anti-immune mechanisms" in tick and by many other factors, which are realized at the feeding stage. Regulation of the number of ticks, depending on their abundance in the host's population, is attained due to the oversparse, close to negative binomial distribution on hosts. This mechanism functions on the principle of feedback, so that at the excessive number of the parasite some individuals in the host's population, which are especially subjected to infection, do not cope with parasitic burden and die. However, ticks, which failed to finish their feeding and represent a disproportionately great part of the whole parasite's population, die together with them and the parasitic system quickly restores its stability. In anthropocoenoses and ecosystems at different stages of anthropogenic transformation mutual regulation mechanisms of the parasite and host number break down. As a consequence, extremely high rises in the number of ticks and epizootics of agricultural animals associated with them can occur.     

青海湖裸鲤寄生对盲囊线虫的种群生态研究

对盲囊线虫的三期幼虫寄生在青海湖裸鲁的体腔,以扁平的透明薄囊包被,附于肠壁和肠系膜间,其种群平均密度随突主体长的增加呈指数形式增加,寄生虫种群在突主种群中呈聚集分布,且其聚集强度随寄生虫的种群平均密度增加而增加。这种分布形式与其第一中间突主锯缘真剑水蚤在青海湖中分布的不均匀性和鱼类宿主在生长过程中的食性分化有关。具体机制无法用数学模式描述,感染率的显著增加引起分布的聚集强度降低。     

Mediterranean Diplodus annularis (Teleostei: Sparidae) and its brain parasite: unforeseen outcome

Patterns of parasite load and aggregation of the bird trematode Cardiocephaloides longicollis in its main intermediate host in the Mediterranean, the annular sea bream, Diplodus annularis, were studied in a large sample collected off Valencia (Spain) and are discussed within the context of the parasite induced host mortality hypothesis. The metacercariae were located within large composite cysts of host origin in the ventricles of the optic lobes of the cerebrum. A weak immunological response was detected in older fish, which was significantly associated with the total parasite load. Although the mean abundance of C. longicollis showed a tendency to increase with host size, the infection levels were generally homogeneous with a noticeable plateauing in the intermediate size classes. The distribution of the metacercariae was aggregated and agreed with the negative binomial distribution. There was a marked decline in parasite aggregation in the largest size-class, suggesting parasite-induced host mortality in the oldest fish possibly due to predation by large non-host fish predators. On the other hand, levelling off of abundance and decrease in heterogeneity of parasite distribution within the intermediate age cohort could indicate that these sizes are being rapidly and/or constantly removed from the host population due to by-catch fishing. The overall high infection levels and the continuous recruitment across age cohorts provides evidence that an enhanced parasite transmission is taking place in the Gulf of Valencia due to increased spatial overlap of the hosts involved in the life cycle. We suggest a human-induced facilitation of the digenean life cycle due to the fact that gulls in the area feed extensively on discards, thus indicating the possibility of an unforeseen effect of fishing practices in a marine littoral system.     

On the interpretation of host-parasite ecology: Heligmosomoides polygyrus (Nematoda) in wild wood mouse (Apodemus sylvaticus) populations

This paper describes epidemiological and seasonal patterns in the interaction between wood mice, Apodemus sylvaticus and Heligmosomoides polygyrus. Data used in the analysis were collected by C. S. Elton and co-workers at Bagley Wood, Oxfordshire in the late 1920s. Heligmosomoides polygyrus was by far the most common helminth parasite with 70% of all wood mice infected and average intensity around 12 worms per mouse. Male and female mice were shown to harbour similar parasite burdens. Parasite numbers per host were highly overdispersed and were well described by the negative binomial distribution. There was little evidence for convexity in age (= weight)-intensity curves, either within or across sexes.
Host and parasite numbers showed predictable seasonal patterns, with mouse populations at their largest at the end of the breeding season, in August and September, and parasite populations at their largest in the late spring, around May. Results are discussed in relation to the ecology of H. polygyrus in wood and laboratory mice, and tentative comparison is made with human helminth infection. The interpretation of epidemiological patterns in these data was problematic. Of particular importance was the statistical distribution of parasites within the host population, and possible differences between mouse sexes in relation to growth, survival and trapping. Such difficulties are relevant to a range of similar field data.     

Indirect evidence of density‐dependent population regulation in Aponomma hydrosauri (Acari: Ixodidae), an ectoparasite of reptiles

Abstract The extent to which density‐dependent processes regulate natural populations is the subject of an ongoing debate. We contribute evidence to this debate showing that density‐dependent processes influence the population dynamics of the ectoparasite Aponomma hydrosauri (Acari: Ixodidae), a tick species that infests reptiles in Australia. The first piece of evidence comes from an unusually long‐term dataset on the distribution of ticks among individual hosts. If density‐dependent processes are influencing either host mortality or vital rates of the parasite population, and those distributions can be approximated with negative binomial distributions, then general host–parasite models predict that the aggregation coefficient of the parasite distribution will increase with the average intensity of infections. We fit negative binomial distributions to the frequency distributions of ticks on hosts, and find that the estimated aggregation coefficient k increases with increasing average tick density. This pattern indirectly implies that one or more vital rates of the tick population must be changing with increasing tick density, because mortality rates of the tick's main host, the sleepy lizard, Tiliqua rugosa, are unaffected by changes in tick burdens. Our second piece of evidence is a re‐analysis of experimental data on the attachment success of individual ticks to lizard hosts using generalized linear modelling. The probability of successful engorgement decreases with increasing numbers of ticks attached to a host. This is direct evidence of a density‐dependent process that could lead to an increase in the aggregation coefficient of tick distributions described earlier. The population‐scale increase in the aggregation coefficient is indirect evidence of a density‐dependent process or processes sufficiently strong to produce a population‐wide pattern, and thus also likely to influence population regulation. The direct observation of a density‐dependent process is evidence of at least part of the responsible mechanism.     

Does the negative binomial distribution add up?

The negative binomial distribution (NBD) is widely used to describe the distribution of parasitic helminths in a number of host individuals and has proved a useful, though possibly overused, empirical and theoretical device. It is therefore important that the limits to the applicability of the NBD be clearly defined. In this paper, Alan Grafen and Mark Woolhouse consider applications of the NBD in situations where either the host or parasite population can be divided into subpopulations of different types (eg. by age, sex or genotype), and they describe the relationships between the frequency distributions relevant to the different subpopulations and those relevant to the total population.     

Modelling parasite aggregation: disentangling statistical and ecological approaches

The overdispersion in macroparasite infection intensity among host populations is commonly simulated using a constant negative binomial aggregation parameter. We describe an alternative to utilising the negative binomial approach and demonstrate important disparities in intervention efficacy projections that can come about from opting for pattern-fitting models that are not process-explicit. We present model output in the context of the epidemiology and control of soil-transmitted helminths due to the significant public health burden imposed by these parasites, but our methods are applicable to other infections with demonstrable aggregation in parasite numbers among hosts.     

Generalized linear modelling for parasitologists

Typically, the distribution of macroparasites over their host population is highly aggregated and empirically best described by the negative binomial distribution. For parasitologists, this poses a statistical provlem, which is often tackled by log-transforming the parasite data prior to analysis by parametric tests. Here, Ken Wilson and Bryan Grenfell show that this method is particularly prone to type I errors, and highlight a much more powerful and flexible alternative: generalized linear modelling.     

Evolution of virulence in a heterogeneous host population

Abstract.— There is a large body of theoretical studies that investigate factors that affect the evolution of virulence, that is parasite-induced host mortality. In these studies the host population is assumed to be genetically homogeneous. However, many parasites have a broad range of host types they infect, and trade-offs between the parasite virulence in different host types may exist. The aim of this paper is to study the effect of host heterogeneity on the evolution of parasite virulence. By analyzing a simple model that describes the replication of different parasite strains in a population of two different host types, we determine the optimal level of virulence in both host types and find the conditions under which strains that specialize in one host type dominate the parasite population. Furthermore, we show that intrahost evolution of the parasite during an infection may lead to stable polymorphisms and could introduce evolutionary branching in the parasite population.     

Population biology of Camallanus oxycephalus Ward and Magath, 1916 (Nematoda: Camallanidae) in white bass in western Lake Erie.

The distribution and abundance of the nematode Camallanus oxycephalus infecting white bass, Morone chrysops, in western Lake Erie was studied for over 2 years. Infection was generally more frequent and of higher intensity in large fish. The frequency distributions of nematode abundance in all segments of the fish population followed the negative binomial distribution. The data show seasonal cycles in population structure, site selection, intensity of infection, maturation, and reproduction. Infection occurs during July and August with a resulting peak in population density; during late summer and autumn, mortality, probably density-dependent, reduces the population by 30 to 60%; surviving worms are eliminated at 1 year of age. Growth and development of female worms is arrested from November to April, then proceeds at a rapid rate until the worms release their larvae and die. This growth pattern is probably related to temperature but may also involve host hormone cycles. The dispersal period of the nematode coincides with the annual maximum density of the intermediate host, a cyclopoid copepod,and is interpreted as an adaptation which increases the probability of successful transmission. Because the number of larvae produced by each female worm is a function of body volume, natural selection has favored rapid spring growth and attainment of large body size relative to the male worm. Both seasonal timing in the life cycle and the number of larvae produced are important factors in determining the abundance of this and perhaps other parasites. Evidence is presented suggesting that fluctuations of environmental parameters may disrupt the timing of transmission and alter the distribution and abundance of the parasite. It is hypothesized that the magnitude of such changes in parasite abundance may be related to the complexity of the host-parasite system.     

Plasmodium spp.: dispersion of malarial oocyst populations in anopheline and culicine mosquitoes

The numbers of malarial oocysts developing in individual, like mosquitoes fed concurrently on a single vertebrate malarial host were found to be distributed according to the negative binomial distribution in 169 experiments utilizing 6 species of Plasmodium, 6 species of mosquitoes and 3 species of vertebrate hosts. Dispersion constants ranged upward to 8.0, and mean clump sizes ranged upward to 298.4. The dispersion constant was demonstrated to be contingent on the species, strain and identity of the mosquito, the parasite and the vertebrate host; on the genetic state of the mosquito; and on the state of the infection in the vertebrate host. It was concluded that the concentration of oocyst production in particular mosquitoes was produced by varying levels and combinations of numerous factors associated with the parasite, the mosquito and the vertebrate host and that the pattern of oocyst distribution favors parasite survival and the maintenance of malaria in the field.     

COMPARATIVE POPULATION GENETIC STRUCTURE OF A PARASITE (FASCIOLOIDES MAGNA) AND ITS DEFINITIVE HOST

The population genetic structure of the American liver fluke, Fascioloides magna, and its definitive host the white-tailed deer, Odocoileus virginianus, was examined in South Carolina. Flukes were significantly more common in deer from river-swamp habitat than upland areas and prevalence increased with host age. The distribution of flukes among deer occurred as a negative binomial with the mean dispersion parameter, k, equal to 0.17 and the range from 0.10 to 1.11 within local areas. Significant spatial genetic differentiation was observed for flukes and deer. Patterns of genetic distance in flukes were not concordant with those of the definitive host nor were they related to geographic distance between sample locations. Spatial genetic differentiation among flukes reflected the tendency for individual hosts to harbor multiple individuals from a limited number of parasite clones. The large population size of the parasite and movements of the definitive host tend to counteract factors that lead to spatial differentiation.     

Invasion and persistence of plant parasites in a spatially structured host population

Spatial structure is of central importance in the dynamics of plant-parasite interactions and is imposed by the growth habit and distribution of host plants and by parasite dispersal which is frequently restricted. To investigate the effects of spatial heterogeneity on the dynamics of plant parasites we introduce a simple model for epidemic development within a spatially structured host population. Here the host population is subdivided into a number of patches which are linked to allow for transmission from one patch to another with the connections defining the spatial structure of the host population. Three key parameters are identified that play a critical role in the ability of the parasite to invade and persist within the host population: the within-patch parasite basic reproductive number which characterises the infection dynamics at the local spatial scale; and the neighbourhood of interaction which describes which patches interact with which and the strength of coupling between patches within the neighbourhood which together characterise the spread of the parasite over larger spatial scales. Using both deterministic and stochastic formulations of the model, we investigate how the thresholds and probabilities of invasion and persistence are affected by these parameters, by demographic stochasticity and by differences in the initial level of infection.     

Epidemiological study of the intestinal helminths of wild boar (Sus scrofa) and mouflon (Ovis gmelini musimon) in central Italy

Since 1995 the population of wild ungulates increased significantly in the "Parco provinciale dei Monti Livornesi" (Livorno, Tuscany, Central Italy). We studied the intestinal macroparasites of two hosts, the wild boar (Sus scrofa) and the mouflon (Ovis gmelini musimon). In the case of wild boars we found a dominant parasite species, Globocephalus urosubulatus. For this parasite the frequency distribution of the number of parasites per host agrees with a negative binomial distribution. There is not a significant correlation between the age of the animals and the parasitosis. Furthermore the mean parasite burden of male and female wild boars does not differ significantly. In the case of mouflons we found a dominant parasite species Nematodirus filicollis with Trichuris ovis as codominant species.     

Interspecific competition among macroparasites in a density-dependent host population

 We analyze the dynamics of a community of macroparasite species that share the same host. Our work extends an earlier framework for a host species that would grow exponentially in the absence of parasitism, to one where an uninfected host population is regulated by factors other than parasites. The model consists of one differential equation for each parasite species and a single density-dependent nonlinear equation for the host. We assume that each parasite species has a negative binomial distribution within the host and there is zero covariance between the species (exploitation competition). New threshold conditions on model parameters for the coexistence and competitive exclusion of parasite species are derived via invadibility and stability analysis of corresponding equilibria. The main finding is that the community of parasite species coexisting at the stable equilibrium is obtained by ranking the species according t! o th e minimum host density H ^* above which a parasite species can grow when rare: the lower H ^* , the higher the competitive ability. We also show that ranking according to the basic reproduction number Q ₀ does not in general coincide with ranking according to H ^* . The second result is that the type of interaction between host and parasites is crucial in determining the competitive success of a parasite species, because frequency-dependent transmission of free-living stages enhances the invading ability of a parasite species while density-dependent transmission makes a parasite very sensitive to other competing species. Finally, we show that density dependence in the host population entails a simplification of the portrait of possible outcomes with respect to previous studies, because all the cases resulting in the exponential growth of host and parasite populations are eliminated.. Received: 24 June 1996 / Revised version: 28 April 1998     

Population biology of two helminth parasites of flatfishes from the Atlantic coast of Morocco

On the Atlantic Moroccan coast, two species of pleuronectiform fish coexist, wedge sole ( Citharus linguatula ) a temperate species, and spotted flounder ( Dicohgoglossa cuneata ) a tropical one. These two species are the definitive host for Bothriocephalus andresi and Acanthocephaloïdes propinquus , respectively. A negative binomial fits the dispersion of B. andresi in the population of C. linguatula . The fish become parasitized between their first and third year, while still immature, with the highest abundances in the third year. After the fish become ichthyopagous, the level of infection drops drastically. We postulate that copepods are the sole source of infection. The presence of B. andresi in both Atlantic and Mediterranean populations of C. linguatula shows that the parasite follows the host during its migration along the Mediterranean coasts.
The prevalence of A. propinquus remains above 50% as a consequence of the large numbers of amphipods included in the diet of D. cuneata , regardless of the age of the fish or the season. The amphipods, Phtisica marina and Pariambus typicus are an important food and represent potential intermediate hosts for A. propinquus . The population dynamics of A. propinquus on the Atlantic Moroccan coasts are similar to those observed in parasite populations of Gobius niger in the Gulf of Lion (French Mediterranean). The observation of B. andresi and A. propinquus in both Moroccan Atlantic and Mediterranean fishes highlights the problem of the evolution of these parasite populations during the colonization of the Mediterranean by the hosts.     

大型多钩槽绦虫在黄鳝体内寄生的研究

解剖检查了５００尾黄鳝。统计表明：黄鳝感染大型多钩槽绦虫的感染率为７．６％,感染强度是２．７,黄鳝感染此种绦虫为一个随机过程。大型钩槽绦虫在宿主种群中的分布符合负二项分布图式,其负二项分布参数ｋ＝０．０３４５,ｐ＝５．９０７８,长度在５ｃｍ以上的绦虫对宿主的正常生长有影响。