- Open Access
Equine strongyle communities are constrained by horse sex and species dipersal-fecundity trade-off
© The Author(s). 2018
- Received: 10 January 2018
- Accepted: 18 April 2018
- Published: 2 May 2018
Equine strongyles are a major health issue. Large strongyles can cause death of horses while cyathostomins (small strongyles) have shown increased resistance to anthelmintics worldwide. Description of strongyle communities have accumulated but little is known about the diversity of these communities and underpinning environmental factors.
Strongyles were recovered after ivermectin treatment from 48 horses located in six premises in Poland. Correlation between previously published species fecundity and the observed relative abundance and prevalence were estimated. Significance of horse sex was determined at the species level (prevalence, relative abundance) and at the community level (species richness and dissimilarity between communities).
Strongyle species fell into two groups, contrasted by their prevalence and relative abundance. Six to nine horses were necessary to sample at least 90% of strongyle community diversity, providing a minimal cut-off to implement sampling trial in the field. Strongyle communities entertained a network of mostly positive interactions and species co-occurrence was found more often than expected by chance. In addition, species fecundity and prevalence were negatively correlated (Pearson’s r = -0.71), suggesting functional trade-offs between species dispersal abilities and fecundity. This functional trade-off may underpin species coexistence. Horse sex was also a significant constraint shaping strongyle communities. Indeed, mares generally displayed more similar strongyle communities than stallions (P = 0.003) and Cylicostephanus calicatus was more abundant in stallions suggesting sex-specific interactions (P = 0.006).
While niche partitioning is likely to explain some of the positive interactions between equine strongyle species, coexistence may also result from a functional trade-off between dispersal ability and fecundity. There is significant evidence that horse sex drives strongylid community structure, which may require differential control strategies between mares and stallions.
Grazing horses are infected by a wide variety of intestinal strongyle parasites belonging to the subfamilies Strongylinae and Cyathostominae . Among the Strongylinae, Strongylus vulgaris has been identified as a major cause of colic in horses . This results from the accumulation of larval stages in the cranial mesenteric artery that leads to an arteritis responsible for fatal intestinal infarction . However, modern anthelmintic treatments have dramatically decreased its prevalence . Cyathostominae (cyathostomes or small strongyles) form a wider tribe than equine Strongylinae, encompassing 51 species, 40 of which infect horses . Unlike the Strongylinae, these nematodes can reach prevalences up to 100% in horses . Cyathostomes have been associated with milder clinical signs like poor hair coat and weight loss , although the massive emergence of larval stages from the large intestine mucosa where they reside can lead to larval cyathostominosis cases, characterised by diarrhoea and protein-losing enteropathy . Failure to control larval cyathostominosis can also lead to the death of affected horses in at least a third of cases, as suggested by a report on 15 clinical cases in the UK . More importantly, cyathostomes have been involved in multiple reports of anthelmintic failures throughout the world thus representing a major issue in equine medicine [8–11].
Despite the wide variety of species, cyathostome communities are consistently described as a core assemblage of 10–13 species [4, 12–16]. While this has been frequently reported, only scant knowledge has been gathered about the drivers underpinning strongyle biodiversity or community assemblage. Nonetheless, some efforts have been made to characterise the consequences of deworming treatments on strongyle diversity as an attempt to better understand widespread anthelmintic failures. First, a reduced diversity in strongyle communities was observed in Ukrainian farms applying frequent deworming . Secondly, investigations of strongyle community structure in horse populations after anthelmintic treatment found that the first species to reappear represented a limited subset of total community [18, 19]. Cylicocyclus nassatus and Cylicostephanus longibursatus were consistently found among the major species after a combination of pyrantel followed by fenbendazole treatment  or after ivermectin treatment . Another study also suggested that these two species were driving the drug resistance phenotype [20, 21]. However, these observations might be confounded by the reported variation in the number of eggs found in utero across strongyle species , dispersal ability (measured by the prevalence of infection) or relative abundance [12, 13, 16]. Indeed, these latter properties may affect the post-treatment community structure, e.g. the most abundant species contributing most to the post-treatment community, without any genuine association with anthelmintic susceptibility.
Some insights into the structure of equine strongyle communities have been provided by a report focusing on pair-wise correlations between strongyle species abundance . This analysis revealed negative interactions between major species, suggesting competition might be involved . In addition, an attempt to bring together environmental factors with equine strongyle diversity in Ukraine concluded that foals and horses older than 16 years displayed higher species richness . However, species richness is only a limited facet of the actual biodiversity as it does not account for the relative proportions of every species found. Furthermore, the impact of host sex was not considered .
Host sex effect is a major driver of helminth community assemblages, male mammals being generally more frequently and more heavily parasitized [25, 26], although some discrepancies exist to this general pattern . In horses, no clear consensus has been reached so far. The analysis of necropsy reports in Australia found differential prevalence and abundance of 13 endoparasites between the two sexes . However, no general trend emerged as females were more heavily infected by Cyathostomum pateratum but less frequently infected by Cylicodontophorus bicoronatus, Cylicocyclus insigne and Cylicocyclus elongatus than stallions and geldings . Study of faecal egg count in a feral horse population reported a spatially contrasted polarity of the sex effect, stallions being more affected than females on one side of the island while the opposite trend was found on the other side . Other studies reported higher faecal egg count in geldings or could not evidence any difference [30, 31].
In this study, we analysed strongyle communities recovered from 48 horses in Poland to investigate species community structure and diversity, the link between previously published fecundity estimates and species dispersal ability and to assess how they were affected by horse sex.
Strongyles were collected in spring 2011 and 2012 from 48 horses scattered across six premises from Poland (Additional file 1: Table S1). Premises had been enrolled for an ivermectin efficacy test. Horses were selected based on their faecal egg count before treatment to allow for strongyle recovery. The study population was composed of 37 mares and 11 stallions. The Małopolska breed accounted for most of the sampled horses (n = 25), in addition to some Hucul (n = 6) and pure blood Arabian horses (n = 17) that were found in only two sites (Additional file 1: Table S1). Two thirds of the individuals were born before 2007 (Additional file 1: Table S1).
Premise features and ecological properties of recovered strongyle communities. Average species richness (number of recovered strongyle species) and Shannon’s index of diversity are provided for each premise
No. of horses (n)
Species richness ± SD
Shannon index ± SD
12.17 ± 2.04
2.07 ± 0.17
9.86 ± 3.74
1.59 ± 0.48
6.00 ± 0.01
1.46 ± 0.23
6.67 ± 1.53
1.43 ± 0.12
11.67 ± 6.51
1.75 ± 0.38
11.00 ± 2.16
1.90 ± 0.14
10.6 ± 3.4
1.8 ± 0.38
Parasite control strategy in every location relied on ivermectin treatments administered in March (or April) and October, before and after pasture season, respectively.
Strongyle collection and identification procedure
The species composition of strongylid nematodes was performed by collecting 500 g of faecal material expelled 24 h after ivermectin treatment following the strategy of other trials [14, 32]. Subsequently, samples were rinsed with tap water on 250 μm mesh sieves and examined under stereomicroscope for the presence of strongylids. Collected nematodes were fixed in 70% ethyl alcohol with 5% glycerine additive to clear their body structure. Strongylids were identified according to previously published morphological keys .
Faecal egg count before treatment was performed following a modified McMaster technique  on 5 g of faecal material, diluted in 70 ml of a flotation solution (NaCl, d = 1.18), with a sensitivity of 50 eggs/g.
Community structure analyses
Statistical analyses were implemented with R v 3.4.1 . Unless stated otherwise, any P-value below 5% was regarded as significant. Strongyles recovered from each horse are hereafter referred to as a community. Within each community, species intensity refers to the number of worms recovered from a given horse, while species relative abundance in a given community corresponds to the proportion of worms found relative to the total worm burden. Species prevalence was defined at the premise level as the proportion of horses infected by a given strongyle species.
Species fecundity may contribute to observed relative abundance and prevalence. To investigate this point, the correlation between previously reported number of eggs in utero recovered from strongyle females  and observed species abundance and prevalence were estimated (rcorr function of the Hmisc package v.4.0-3 ). Species fecundity estimates were log-transformed to obtain a linear relationship between variables.
Our sampling procedure involved a limited amount of faecal material which may have biased our prevalence and abundance estimates. Therefore, our observations were compared against a dataset  of previously published equine strongyle species prevalence (n = 29 papers) and relative abundances (n = 14 papers) provided as Additional file 2: Table S2. These studies spanned all continents and involved various methodologies (necropsy, deworming), thus limiting confounding factors linked to climatic conditions or sampling methods. For each paper, species relative abundance and prevalence were computed from the data if not already provided. These individual estimates were subsequently averaged across studies for comparison with the observed values from our 48 horses.
Species turnover can occur along environmental gradients, hence resulting in variation among individual communities from a given group. This measure of dissimilarities between communities was originally coined as β-diversity , and will contribute only marginally to the global diversity if individual communities show little or no variation among groups. Difference in β-diversity among environmental factors (location, horse age and horse sex) was tested following a multivariate framework [40, 41], implemented in the adonis function of the vegan package . This framework measures β-diversity as the distance of every community to the average group community, determined as the centroid of a principal components analysis of community structures .
Non-random species co-occurrence was tested following a probabilistic framework that compares observed species frequencies to the expected frequencies under species independence (discarding species pairs when the expected number of co-occurrence is less than 1) [42, 43]. Species interactions could also result in positive or negative feedbacks that could impact on species relative abundances. To test for these interactions, species counts were regressed upon other species intensity in a pairwise manner after accounting for environmental variables (horse sex and sampling site) and by means of a Poisson regression. For this analysis, the 13 species with more than 200 individuals across horses were considered, as failure to do so results in strong positive associations for the minor species present. Because of the high number of statistical tests (n = 105), a Bonferroni correction was applied and a P-value below 0.05/105 = 5 × 10-4 was considered significant. Significant pairwise regression estimates (P < 5 × 10-4) were used to generate a species network, visualized with the ggnet package . The network uses a force-directed algorithm from the matrix of interactions. Nodes act as repelling objects that are organized to minimize forces in the network.
Host sex effect on species relative abundance and prevalence
The impact of host sex on strongyle abundance (worm counts) and prevalence was investigated for the 11 core strongyle species, i.e. most abundant and most prevalent. Cyathostomum catinatum showed the highest prevalence (47 horses infected) and was not included in the prevalence data analysis as not enough variability was present to assess factors of variation. To account for the data structure (Additional file 1: Table S1), these effects were investigated using only the data from premises where horses of each gender were present (premises 2, 3, 4 and 6; n = 27 horses). Worm counts and species prevalence were modelled using a negative binomial and logistic regression, respectively.
Samples were recovered in 2011 and 2012, hence introducing a putative confounding annual variation. This was tested in two ways. First, Pearson’s correlation between prevalence and relative abundance measured in 2011 and 2012 were estimated to support their congruence. Secondly, worm counts and species prevalence were regressed on a universal year effect shared across species and a species-specific inter-annual variation.
A linear regression analysis was applied to Shannon’s index values to evaluate variation between premises and horse ages and sexes. For every model, the sex effect on species relative abundance and prevalence was estimated across premises (19 mares and 8 stallions). The premise effect accounted for both management and breed type differences.
Strongyle dispersal abilities were contrasted and inversely correlated with their known fecundity estimates
Considered parasite populations were all ivermectin-susceptible as post-treatment FEC were back to 0 in every horse. On average, 608.7 worms per horse were collected, ranging from 111 to 2884 (Additional file 1: Table S1). Overall, 23 species were found across premises (Additional file 1: Table S1), with average species richness ranging from 6 to 12 species (Table 1).
Between 4 and 20 species could be recovered at the horse level (Additional file 1: Table S1). The male to female worm ratio was 0.58 on average (Additional file 3: Table S3). Total worm count was not significantly correlated with pre-treatment faecal egg count (Spearman’s r(48) = 0.22, P = 0.13).
A similar pattern was found when using the 29 previously published prevalence estimates (Pearson’s r(13) = -0.86, P < 0.0001), but the relationship with 14 published species relative abundance was not significant (Pearson’s r(10) = -0.45, P = 0.19).
Communities were structured by a network of mostly positive interactions
Horse gender affects dissimilarity between strongyles communities and species abundance
Little inter-annual variation was found as the correlation for prevalence and relative abundances across the two years were 0.89 and 0.91, respectively (Pearson’s r(23), P < 0.0001 in both cases). In addition, neither a universal inter-annual effect shared across species (Wald test χ2 = 1.35, df = 1, P = 0.25 for prevalence; Wald test χ2 = 0.28, df = 1, P = 0.59 for relative abundance) nor a species-specific annual variation (Wald test χ2 = 14.48, df = 10, P = 0.15 for prevalence; Wald test χ2 = 11.01, df = 10, P = 0.36 for relative abundance) were found.
Strongyle community diversity ranged from 0.6 to 2.6 at the horse level but was more consistent at the premise level with average values between 1.43–2.07 (Table 1). No significant variation in species α-diversity was found between premises (F(3, 21) = 2, P = 0.15).
Neither horse age (F(1, 21) = 2.33, P = 0.14) nor horse sex affected significantly community diversity (F(1, 21) = 0.33, P = 0.57), suggesting that α-diversity was equivalent between mares and stallions.
An analysis of community dissimilarity was performed to assess the extent of species turnover across horse gender, horse age and premises. Strongyle communities structure was similar across horse ages (F(1, 21) = 1.60, P = 0.24) but significantly varied between premises (F(3, 21) = 2.38, P = 0.05) and were also significantly more homogeneous in mares than in stallions (F(1, 21) = 8.72, P = 0.006).
Strongyle dispersal ability measured by the prevalence of each species did not vary significantly between mares and stallions, although C. nassatus was found slightly more often in mares (t(271) = -1.94, P = 0.05, Fig. 6, Additional file 7: Table S6).
This study focused on the structure of equine strongyle communities under eastern Europe climatic conditions. The data suggested that reported species fecundity, approximated by the number of eggs in utero, was negatively correlated with species prevalence. This relationship was found both in our dataset and across previously published prevalence reports. In addition, horse sex had a statistically significant effect on strongyle community structure and diversity.
Numerous reports on equine strongyle community structure have already evidenced the bimodal pattern of their assemblages, with five to ten highly prevalent and abundant species and additional minor species [4, 12–16]. Our data also highlighted the same split between core and satellite species , with a set of three successful dispersers, i.e. C. catinatum, C. nassatus and C. longibursatus, which were found in 75% of horses and represented between 13–21% of the total worm burden. This pattern was also corroborated by estimates from available literature.
Not only corroborating the known literature, this finding also supported the chosen sampling strategy [14, 32]. First, only a limited amount of faecal material was taken from each horse. This could have biased downwards worm counts, eventually resulting in increasing the missing rate of some species. However, it seems that our prevalence and relative abundance fit the pattern observed across previous reports that relied on necropsy or deworming for worm collection. Secondly, a single sampling 24 h after treatment might have biased the sampling efficiency downwards as it has been suggested that a significant proportion of parasite material could still be recovered after 36 and up to 60 h . From our results, some species reported as minor in the present study (S. edentatus, S. vulgaris, T. serratus and C. elongatus) may have suffered from the sampling strategy as most of them were expelled 48 h after treatment onwards in a previous trial . Notably, this prevents any firm conclusion regarding the minor contribution of S. vulgaris to the strongyle communities, even though displayed prevalence levels were in agreement with other reports from regularly dewormed horses [46, 47]. Nevertheless, community structure and species richness estimates were similar to previous reports under eastern European conditions [14, 17], supporting the implemented sampling method.
Under the considered conditions, a limited number of horses were required to sample 90% of the strongyle community diversity. This is of particular relevance for the implementation of field sampling where necropsy is not an option and minimal interference with premise activity are expected.
Although the overall structure of strongyle communities has been well characterized in equids [4, 12–15], little is known about the mechanisms and variation factors underpinning their stability. Remarkably, sampled communities were entertaining positive interactions, both in terms of presence/absence patterns or in their intensity covariation. This finding was in contradiction with previously reported results from an abattoir survey, which highlighted negative interactions between major species . However, the negative interactions mostly occurred between species that were less represented in our present report, i.e. S. vulgaris and S. edentatus or Triodontophorus species . In addition, our analyses were restricted to the best dispersers (species with highest prevalence); hence preventing spurious positive associations that can occur when correlating low counts . Our results were in line with known positive associations between core species . Reports of helminths species co-occurring more often than expected by chance have also been made for human and rodent systems . These positive interactions could arise from niche partitioning between species within horses. The latter could explain for instance, positive feedbacks between C. goldi and C. nassatus, which mostly occupy the dorsal and ventral colon, respectively [16, 23], but does not support positive interactions between C. minutus and C. calicatus, which tend to share the same organs [16, 23]. Observed positive interactions may hence suggest that some of the equine strongyle species share mutualistic interactions as already reported for rodent models . However, the negative interactions of C. pateratum with other species remains unexplained. It could be the result of competition between species for space or nutrients (exploitation competition); it may also suggest interference between species due to local inflammation mediated by one species and affecting others or cross-reactivity of the host immune system towards multiple species .
The existence of functional trade-offs can result in positive associations between species, as demonstrated in plants  or fig wasps . Because of the sparsity of hosts and environmental constraints put on eggs and larvae on pasture, strongyle species with best competing abilities, like higher fecundity, may not be able to colonize every available horse. As a result, horses can be colonized by species with lower competing abilities, e.g. lower fecundity. This ultimately leads to species co-existence despite highly differential competing abilities and an apparent trade-off between species fecundity and prevalence. However, our results may suffer from the proxy used for species fecundity. These estimates are based on the number of eggs found in utero in female worms, and were generated for a worm population from the USA . A precise assessment of each species egg production rate by means of barcode sequencing may help to better resolve this point.
The negative correlation between species female relative abundance and their inferred fecundity may be related to some crowding effect. It has been described in sheep trichostrongylids  and a negative feedback between mature worms and incoming larvae has been suggested in horses [55, 56].
Our results suggested that horse sex was not exerting a universal influence on worm relative abundance across species, but that mares had more consistent strongyle communities. In addition, higher C. calicatus worm counts were found in stallions. This finding was already reported in a previous Australian survey, which also evidenced additional host sex interactions for C. coronatus and C. catinatum . Variation in the qualitative composition of strongyle structure might hence contribute to the lack of clear differences between stallion and mare excretion patterns. However, mechanistic explanations to support a higher species turnover among stallions remain unclear and deserve further exploration.
This survey provided insights into applied and more fundamental knowledge about equine strongyle communities and how host sex drives their structure and diversity. The bimodal structure of equine strongyle communities split into core and satellite species was confirmed, underscoring the overwhelming contribution of C. nassatus, C. catinatum and C. longibursatus. We also found that less than ten horses were needed to sample most of the diversity, which is particularly relevant for logistically constrained surveys. More fundamentally, it seems that equine strongyle communities are largely structured around a network of positive, if at all, interactions, with the only exception of C. pateratum. While mutualistic interactions and niche partitioning could explain this pattern, the observed trade-offs between fecundity and dispersal abilities may also explain this coexistence. Horse sex did not appear to influence the overall worm counts, but a higher species turnover was found among stallions leading to more dissimilar strongyle communities for this gender. While our data provided new insights into the structuring equine strongyle communities, only a limited set of the potential factors shaping these communities have been considered. Further research in this area should make use of recent advances in sequencing technology to increase the sensitivity of worm sampling and also integrate putative interactions with the host gut microbiota.
The authors are particularly indebted to the premise managers who took part to this survey.
Availability of data and materials
The datasets supporting the conclusions of this article are included within the article and its additional files.
SK designed the study. SK and MB collected samples and performed cyathostomin species identification. GS analysed the data. GS and SK drafted the manuscript. All authors read and approved the final manuscript.
Ethics approval and consent to participate
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Lichtenfels JR, Kharchenko VA, Dvojnos GM. Illustrated identification keys to strongylid parasites (Strongylidae: Nematoda) of horses, zebras and asses (Equidae). Vet Parasitol. 2008;156:4–161.View ArticlePubMedGoogle Scholar
- Duncan JL, Campbell JR. Further observations on the maintenance of a monospecific infection of Strongylus vulgaris in the horse. Vet Rec. 1973;92:533.View ArticlePubMedGoogle Scholar
- Nielsen MK, Vidyashankar AN, Olsen SN, Monrad J, Thamsborg SM. Strongylus vulgaris associated with usage of selective therapy on Danish horse farms-is it reemerging? Vet Parasitol. 2012;189:260–6.View ArticlePubMedGoogle Scholar
- Lyons ET, Tolliver SC, Drudge JH. Historical perspective of cyathostomes: prevalence, treatment and control programs. Vet Parasitol. 1999;85:97–112.View ArticlePubMedGoogle Scholar
- Murphy D, Love S. The pathogenic effects of experimental cyathostome infections in ponies. Vet Parasitol. 1997;70:99–110.View ArticlePubMedGoogle Scholar
- Love S, Murphy D, Mellor D. Pathogenicity of cyathostome infection. Vet Parasitol. 1999;85:113–22.View ArticlePubMedGoogle Scholar
- Giles CJ, Urquhart KA, Longstaffe JA. Larval cyathostomiasis (immature trichonema-induced enteropathy): a report of 15 clinical cases. Equine Vet J. 1985;17:196–201.View ArticlePubMedGoogle Scholar
- Canever RJ, Braga PR, Boeckh A, Grycajuck M, Bier D, Molento MB. Lack of Cyathostomin sp. reduction after anthelmintic treatment in horses in Brazil. Vet Parasitol. 2013;194:35–9.Google Scholar
- Traversa D, Castagna G, von Samson-Himmelstjerna G, Meloni S, Bartolini R, Geurden T, et al. Efficacy of major anthelmintics against horse cyathostomins in France. Vet Parasitol. 2012;188:294–300.View ArticlePubMedGoogle Scholar
- Relf VE, Lester HE, Morgan ER, Hodgkinson JE, Matthews JB. Anthelmintic efficacy on UK Thoroughbred stud farms. Int J Parasitol. 2014;44:507–14.View ArticlePubMedGoogle Scholar
- Geurden T, van Doorn D, Claerebout E, Kooyman F, De Keersmaecker S, Vercruysse J, et al. Decreased strongyle egg re-appearance period after treatment with ivermectin and moxidectin in horses in Belgium, Italy and The Netherlands. Vet Parasitol. 2014;204:291–6.View ArticlePubMedGoogle Scholar
- Mfitilodze MW, Hutchinson GW. Prevalence and abundance of equine strongyles (Nematoda: Strongyloidea) in tropical Australia. J Parasitol. 1990;76:487–94.View ArticlePubMedGoogle Scholar
- Ogbourne CP. The prevalence, relative abundance and site distribution of nematodes of the subfamily Cyathostominae in horses killed in Britain. J Helminthol. 1976;50:203–14.View ArticlePubMedGoogle Scholar
- Kuzmina TA, Kharchenko VA, Starovir AI, Dvojnos GM. Analysis of the strongylid nematodes (Nematoda: Strongylidae) community after deworming of brood horses in Ukraine. Vet Parasitol. 2005;131:283–90.View ArticlePubMedGoogle Scholar
- Traversa D, Milillo P, Barnes H, von Samson-Himmelstjerna G, Schurmann S, Demeler J, et al. Distribution and species-specific occurrence of cyathostomins (Nematoda, Strongylida) in naturally infected horses from Italy, United Kingdom and Germany. Vet Parasitol. 2010;168:84–92.View ArticlePubMedGoogle Scholar
- Collobert-Laugier C, Hoste H, Sevin C, Dorchies P. Prevalence, abundance and site distribution of equine small strongyles in Normandy, France. Vet Parasitol. 2002;110:77–83.View ArticlePubMedGoogle Scholar
- Kuzmina TA, Kharchenko VO. Anthelmintic resistance in cyathostomins of brood horses in Ukraine and influence of anthelmintic treatments on strongylid community structure. Vet Parasitol. 2008;154:277–88.View ArticlePubMedGoogle Scholar
- Hodgkinson JE, Freeman KL, Lichtenfels JR, Palfreman S, Love S, Matthews JB. Identification of strongyle eggs from anthelmintic-treated horses using a PCR-ELISA based on intergenic DNA sequences. Parasitol Res. 2005;95:287–92.View ArticlePubMedGoogle Scholar
- Ionita M, Howe DK, Lyons ET, Tolliver SC, Kaplan RM, Mitrea IL, et al. Use of a reverse line blot assay to survey small strongyle (Strongylida: Cyathostominae) populations in horses before and after treatment with ivermectin. Vet Parasitol. 2010;168:332–7.View ArticlePubMedGoogle Scholar
- Kooyman FN, van Doorn DC, Geurden T, Mughini-Gras L, Ploeger HW, Wagenaar JA. Species composition of larvae cultured after anthelmintic treatment indicates reduced moxidectin susceptibility of immature Cylicocyclus species in horses. Vet Parasitol. 2016;227:77–84.View ArticlePubMedGoogle Scholar
- van Doorn DC, Ploeger HW, Eysker M, Geurden T, Wagenaar JA, Kooyman FN. Cylicocyclus species predominate during shortened egg reappearance period in horses after treatment with ivermectin and moxidectin. Vet Parasitol. 2014;206:246–52.View ArticlePubMedGoogle Scholar
- Kuzmina TA, Lyons ET, Tolliver SC, Dzeverin II, Kharchenko VA. Fecundity of various species of strongylids (Nematoda: Strongylidae)-parasites of domestic horses. Parasitol Res. 2012;111:2265–71.View ArticlePubMedGoogle Scholar
- Stancampiano L, Mughini Gras L, Poglayen G. Spatial niche competition among helminth parasites in horse's large intestine. Vet Parasitol. 2010;170:88–95.View ArticlePubMedGoogle Scholar
- Kuzmina TA, Dzeverin I, Kharchenko VA. Strongylids in domestic horses: Influence of horse age, breed and deworming programs on the strongyle parasite community. Vet Parasitol. 2016;227:56–63.View ArticlePubMedGoogle Scholar
- Poulin R. Sexual inequalities in helminth infections: a cost of being a male? Am Nat. 1996;147:287–95.View ArticleGoogle Scholar
- Zuk M, McKean KA. Sex differences in parasite infections: patterns and processes. Int J Parasitol. 1996;26:1009–23.View ArticlePubMedGoogle Scholar
- Grzybek M, Bajer A, Behnke-Borowczyk J, Al-Sarraf M, Behnke JM. Female host sex-biased parasitism with the rodent stomach nematode Mastophorus muris in wild bank voles (Myodes glareolus). Parasitol Res. 2015;114:523–33.View ArticlePubMedGoogle Scholar
- Bucknell DG, Gasser RB, Beveridge I. The prevalence and epidemiology of gastrointestinal parasites of horses in Victoria, Australia. Int J Parasitol. 1995;25:711–24.View ArticlePubMedGoogle Scholar
- Debeffe L, McLoughlin PD, Medill SA, Stewart K, Andres D, Shury T, et al. Negative covariance between parasite load and body condition in a population of feral horses. Parasitology. 2016;143:983–97.View ArticlePubMedGoogle Scholar
- Kornaś S, Sallé G, Skalska M, David I, Ricard A, Cabaret J. Estimation of genetic parameters for resistance to gastro-intestinal nematodes in pure blood Arabian horses. Int J Parasitol. 2015;45:237–42.View ArticlePubMedGoogle Scholar
- Kornaś S, Cabaret J, Skalska M, Nowosad B. Horse infection with intestinal helminths in relation to age, sex, access to grass and farm system. Vet Parasitol. 2010;174:285–91.View ArticlePubMedGoogle Scholar
- Osterman Lind E, Eysker M, Nilsson O, Uggla A, Hoglund J. Expulsion of small strongyle nematodes (Cyathostomin spp.) following deworming of horses on a stud farm in Sweden. Vet Parasitol. 2003;115:289–99.Google Scholar
- Raynaud JP. Study of the efficiency of a quantitative coproscopic technic for the routine diagnosis and control of parasitic infestations of cattle, sheep, horses and swine. Ann Parasitol Hum Comp. 1970;45:321–42.View ArticlePubMedGoogle Scholar
- R Core Team. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2016.Google Scholar
- Harrell FE, Dupont C. Hmisc: Harrell Miscellaneous. 2017.Google Scholar
- Sallé G, Cabaret J. Meta-analysis of cyathostomins community structure and diversity. Liverpool: International Conference of the World Association for the Advancement of Veterinary Parasitology; 2015.Google Scholar
- Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package. R package version 2.4-3. 2017.Google Scholar
- Witthaker RH. Vegetation of Siskiyou mountains, Oregon and California. Ecol Monogr. 1960;30:279–338.View ArticleGoogle Scholar
- Shannon CE. A mathematical theory of communication. Bell Syst Tech J. 1949;27:379–423.View ArticleGoogle Scholar
- Anderson MJ, Ellingsen KE, McArdle BH. Multivariate dispersion as a measure of beta diversity. Ecol Lett. 2006;9:683–93.View ArticlePubMedGoogle Scholar
- Anderson MJ. Distance-based tests for homogeneity of multivariate dispersions. Biometrics. 2006;62:245–53.View ArticlePubMedGoogle Scholar
- Griffith DM, Veech JA, Marsh CJ. cooccur: Probabilistic Species Co-Occurrence Analysis in R. J Stat Softw Code Snips. 2016;69(2):1–17. https://doi.org/10.18637/jss.v069.c02.
- Veech JA. A probabilistic model for analysing species co-occurrence. Glob Ecol Biogeogr. 2013;22:252–60.View ArticleGoogle Scholar
- Briatte F. ggnet: Functions to plot networks with ggplot2. 2018. https://briatte.github.io/ggnet/.
- Hanski I. Dynamics of regional distribution - the core and satellite species hypothesis. Oikos. 1982;38:210–21.View ArticleGoogle Scholar
- Boxell AC, Gibson KT, Hobbs RP, Thompson RCA. Occurrence of gastrointestinal parasites in horses in metropolitan Perth, Western Australia. Aust Vet J. 2004;82:91–5.View ArticlePubMedGoogle Scholar
- Lind EO, Hoglund J, Ljungstrom BL, Nilsson O, Uggla A. A field survey on the distribution of strongyle infections of horses in Sweden and factors affecting faecal egg counts. Equine Vet J. 1999;31:68–72.View ArticleGoogle Scholar
- Poulin R. Interactions between species and the structure of helminth communities. Parasitology. 2001;122(Suppl):S3–11.View ArticlePubMedGoogle Scholar
- Holmes JC. The structure of helminth communities. Int J Parasitol. 1987;17:203–8.View ArticlePubMedGoogle Scholar
- Behnke JM. Structure in parasite component communities in wild rodents: predictability, stability, associations and interactions .... or pure randomness? Parasitology. 2008;135:751–66.PubMedGoogle Scholar
- Bottomley C, Isham V, Basanez MG. Population biology of multispecies helminth infection: competition and coexistence. J Theor Biol. 2007;244:81–95.View ArticlePubMedGoogle Scholar
- Angert AL, Huxman TE, Chesson P, Venable DL. Functional tradeoffs determine species coexistence via the storage effect. Proc Natl Acad Sci USA. 2009;106:11641–5.Google Scholar
- Duthie AB, Abbott KC, Nason JD. Trade-offs and coexistence in fluctuating environments: evidence for a key dispersal-fecundity trade-off in five nonpollinating fig wasps. Am Nat. 2015;186:151–8.View ArticlePubMedGoogle Scholar
- Stear MJ, Bishop SC. The curvilinear relationship between worm length and fecundity of Teladorsagia circumcincta. Int J Parasitol. 1999;29:777–80.View ArticlePubMedGoogle Scholar
- Smith HJ. Strongyle infections in ponies. I. Response to intermittent thiabendazole treatments. Can J Comp Med. 1976;40:327–33.PubMedPubMed CentralGoogle Scholar
- Gibson TE. The effect of repeated anthelmintic treatment with phenothiazine on the faecal egg counts of housed horses, with some observations on the life cycle of Trichonema spp. in the horse. J Helminthol. 1953;27:29–40.View ArticleGoogle Scholar