Heterakis gallinarum is found worldwide in areas where galliform birds live. Kaufmann, Heterakis gallinarum is a parasite found in the cecum of numerous galliform birds including chickens, turkeys, and pheasants. The eggs of H.
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Metrics details. Density related effects, both inverse density- and density-dependent, contribute to regulating population dynamics of parasites. We investigated whether density related effects are directly controlling lifetime fecundity of Heterakis gallinarum.
Daily total numbers of H. The birds were necropsied 8 wk p. Density related effects on cumulative egg excretion CEE , lifetime fecundity and worm length were investigated with a segmented regression analysis. For CEE, lifetime fecundity and female worm length, we determined highly similar parasite intensity thresholds 52—54 worms , which separated infrapopulations for influences of inverse density- and density dependence.
CEE increased as parasite intensity increased up to an intensity of 52 worms. After this threshold, the relationship followed more of a horizontal line indicating impaired worm fecundity at higher parasite intensities. Lifetime fecundity was enhanced linearly in infrapopulations with up to 54 worms, but thereafter decreased gradually with increasing infrapopulation size.
Female worm length increased linearly with elevating parasite intensity up to a threshold of 54 worms and thereafter declined with a rate of Egg production of H.
In infrapopulations below the intensity thresholds, inverse density dependence effects on lifetime fecundity appear to result partly from sex-ratio fluctuations and impaired mating success of the nematode. Host immune responses are considered as the primary mechanisms regulating population dynamics of nematodes within host [ 1 , 2 ]. In addition, density-dependent effects, which may partly be generated through immune responses, are known to contribute regulating parasite population dynamics [ 1 , 3 , 4 ].
For parasitic nematodes, the most pronounced density-dependent effects are mainly observed on establishment rate [ 5 — 7 ], worm length [ 2 , 8 ], fecundity [ 9 , 10 ] and sex-ratio [ 11 ].
In already established parasite infrapopulations, density-dependent effects may partly result in intraspecific interactions leading to increasing competition for finite resources e. As demonstrated by Bishop and Stear [ 9 ], density-dependent effects may not only cause a decrease in fecundity of individual worms, defined as faecal egg concentration per female worm, but may also conspicuously decrease total egg production of infrapopulations.
Density-dependent effects apply in poultry nematodes, too. Permin et al. Establishment rate of the caecal worm, Heterakis gallinarum , has also been shown to be density dependent in a pheasant host-system [ 8 ].
Density related effects are, however, not limited to density dependence only, and thus are not always negative. Such a relationship has been demonstrated for the mean weight of female Ascaris lumbricoides which follows a pattern of initial facilitation followed by limitation with further increasing parasite density [ 13 ]. Similarly, H. Although Thompkins and Hudson [ 8 ] considered the length of female H.
Therefore, this study aimed at investigating whether density related effects are regulating total egg excretion and fecundity of H. As the outcome of single faecal egg counts can suffer from methodological restrictions to some extent, we investigated density-related effects on long-term egg production outcomes including cumulative egg excretion of infrapopulations and lifetime fecundity of the nematode.
A total of 39 female white Leghorn Lohmann Selected Leghorn chicks were inoculated orally at the age of three weeks wk with approximately embryonated eggs of Heterakis gallinarum that originated from Histomonas meleagridis -free batches. The preparation of the H.
Thereafter, they were placed into individual cages that provided the birds with free access to feed and water, and also allowed quantitative daily collection of individual faeces. No vaccination or anthelmintic treatment was applied.
After a two-days adaptation period that ensured regular feed and water intake by the birds, daily faeces collections were started at the beginning of 4th wk post-infection p. Faecal droppings excreted by each bird accumulated in a plastic bag-covered box underneath the cage. A well-mixed sub-sample was derived from the daily amount of faeces of each bird. A total of fecal samples were analyzed for EPG. All the birds were necropsied 8 wk p.
Gender specific average worm length was determined by measuring all intact female and male worms of each bird. At necropsies, caecum size was also determined by measuring caecal lengths and full and empty washed weights. Cumulative egg excretion CEE by each nematode infrapopulation was estimated as the sum of total daily egg excretions EPD during the days collection period. Cumulative egg excretion and fecundity parameters were logarithmically natural transformed by using a function in the form of [Ln y ] to correct for heterogeneity of variance and to produce approximately normally distributed data.
The statistical model included fixed effects of days post-infection 22—56 on which faeces samples were collected. Daily fecundity was assumed to be correlated across measurements, and thus the covariance structure was set to be compound symmetry.
A segmented regression analysis [ 17 ] was used to investigate responses in the outcomes of infrapopulations cumulative egg excretion, lifetime fecundity and worm length to increasing parasite intensity.
The parameters a , b and c can be considered as a constant a and slopes of the first b and the second c regression lines, respectively. The breakpoint x 0 is considered as a measure of threshold at parasite intensity after which outcomes of the response variables behave differently.
To assess model adequacy, the error mean square EMS and a pseudo-goodness of fit pseudo-R 2 for non-linear regression were used. Graphical representation of data was carried out with SigmaPlot V The infection dose eggs given to each bird was within the range of the worm burdens that can be observed in natural sub-clinical infections.
All the experimental procedures followed the animal welfare rules. On the first sampling day i. The experimental infection produced patent infections in all the birds. All the worms were mature i.
On average, every third inoculated egg was recovered as mature worm, corresponding to an establishment rate of Almost equal average numbers of female and male worms per chicken were harvested while overall average sex ratio was in favor of female worms Goodnesses of model fit pseudo-R 2 ranged from 0. For all the predicted lines, joined with a breakpoint x 0 as a measure of threshold, the first slopes b were positive while the second c slopes were negative.
Above this threshold, the relationship between CEE and worm burden followed more of a horizontal line. Similar to CEE, lifetime fecundity enhanced linearly in birds infected with up to 54 worms, but thereafter decreased with increasing parasite intensity. Cumulative egg excretion ln in Heterakis gallinarum infrapopulations in relation to parasite intensity. Lifetime fecundity ln in Heterakis gallinarum infrapopulations in relation to parasite intensity.
Average female worm length in Heterakis gallinarum infrapopulations in relation to parasite intensity. We investigated whether and to what extent density related effects, both inverse density and density-dependent, influence long-term egg production outcomes of Heterakis gallinarum infrapopulations in a chicken-host system.
It was demonstrated for the first time for H. In addition, our results confirm fully the inverse density and density-dependence in female worm length that was previously demonstrated by Thompkins and Hudson [ 8 ].
Thompkins and Hudson [ 8 ] determined a higher threshold 96 worms above which density dependent effects replaced inverse density dependency. The differences in the thresholds may not only be attributed to different host species, but also to some other factors e. Co-existence of both inverse density and density dependency mechanisms regulating parasite population dynamics, particularly in nematodes, seems to be rare.
Although there are at least two studies describing existence of both inverse density and density dependency in parasitic nematodes [ 8 , 13 ], these studies rely on evidence obtained from relationships between parasite intensity and female worm size, measured either as length [ 8 ] or weight [ 13 ]. As confirmed in the present study, female worm length, but not male worm length, is a valuable indicator of fecundity and responds to increasing parasite intensity in a parallel way as lifetime fecundity does.
In the existence of both inverse density and density dependent mechanisms on both lifetime fecundity and on female worm length, linear relationships between worm length and fecundity might have weakened.
The model fit parameters of the segmented regression were better for lifetime fecundity than for female worm length. Since parasite survival and fecundity, but not parasite size, are the two parameters of importance in the generation of epidemiological patterns and the determination of evolutionary fitness of a parasite species, density related effects on parasite size must be translated into influences on parasite survival and fecundity [ 1 ].
Our results suggest that the effects on length translate into effects on fecundity. For H. This was probably due to difficulties in quantification of egg excretion, which has often been problematic mainly because of the periodicity in the caecal faeces excretion of the birds. The caecal faeces, which contains Heterakis eggs, is passed to the external environment periodically [ 19 ], according to Klasing [ 20 ] only once or twice a day.
That is why examining random regular faecal samples, which mostly originate from non-caeca-intestines, may result in false negative faecal egg counts FEC even though in heavily Heterakis-infected animals [ 21 ]. We have previously shown that analyzing well-mixed samples obtained from the daily total amount of faeces provides highly repeatable FEC that are also representative of H. Excluding technical limitations with egg counting methods [ 22 ], egg concentration in faeces EPG is easy to determine and it ensures contribution of all prolific females in an infrapopulation, although accuracy and precision of EPG are also influenced by a couple of faeces-related factors.
The most pronounced ones are the daily amount and the water content of faeces, which may result in under- or overestimation of EPG [ 15 , 23 ]. On the other hand, accuracy of worm recoveries may not always be high, particularly in large hosts with predilection sites of high volumes.
Additionally, plotting worm burden against its inverse multiplied by FEC may obscure the true biological relationships [ 2 ]. The most apparent feature of the data used for the present study was that the total egg excretion outcomes of the infrapopulations were on the basis of the sum of 35 individual daily total egg excretions. Thus, compared with measurement error of a fecundity estimate relying on a single faecal egg count e.
However, lifetime fecundity estimates do not rely only on the cumulative egg excretions, but also on the worm counts, which could be quantified only once and just at the end of the experimental period. Therefore, any change that might have taken place in the worm counts of the birds during the faeces collection period has the potential to influence accuracy of the lifetime fecundity estimates.
However, this seems unlikely for three reasons. First, experimental infections with H. This implies stability of the patent infections with mature worms descending from a single inoculation.
This also supports the stability when patency is achieved. Third, as reinfections were prevented in the experimentally-infected birds through daily removal of faeces, the number of egg-producing female worms is unlikely to have increased over the course of the study.
Thus it can be inferred that total egg excretion and lifetime fecundity data shown in this study resulted from stable patent-infrapopulations. Population stability is indeed a characteristic feature of helminth infections [ 25 ].
It may therefore be hypothesized that cumulative egg excretion is not merely an outcome of certain number of female worms within a given time, but it may also reflect follow-up regulatory effects of the host immune system which initially have to act on establishment of larvae [ 8 ] and eventually contribute to determining number of egg producing females as well as their fecundity.
The experimental infection produced worm burdens that were comparable to the levels observed both in naturally occurring [ 21 , 26 , 27 ] and in experimentally performed H. In contrast to natural infections, experimental infections may provide the possibility of investigating the effects of different mechanisms regulating parasite population dynamics separately. We previously showed that concomitant infections of chickens with H. For the present study, however, we eliminated H. Therefore, in this study regulatory effects on population dynamics of H.
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PCR Detection of Heterakis Gallinarum in Environmental Samples
Prevalence and pathology of the nematode Heterakis gallinarum , the trematode Paratanaisia bragai, and the protozoan Histomonas meleagridis in the turkey, Meleagris gallopavo. The prevalence of infection and associated pathology induced by two helminth and one protozoan species infecting Brazilian turkeys are reported. Histological findings in the ceca were represented by the presence of H. The prevalence of the protozoan H. The walls of the ducts presented a discrete heterophilic infiltrate among mononuclear cells. Key words: helminths - protozoan - turkeys - Meleagris gallopavo - pathology - Brazil.
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Heterakis gallinarum
Heterakis gallinarum is a widely distributed cecal nematode that parasitizes gallinaceous birds including chickens and turkeys. The only means of detecting H. Three primer sets were designed from sequences cloned from the H. Each of these primer sets amplified a single product from H. This site needs JavaScript to work properly. Please enable it to take advantage of the complete set of features!