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Parasitol Res (2012) 111:22652271 DOI 10.

1007/s00436-012-3077-5

ORIGINAL PAPER

Fecundity of various species of strongylids (Nematoda: Strongylidae)parasites of domestic horses


T. A. Kuzmina & E. T. Lyons & S. C. Tolliver & I. I. Dzeverin & V. A. Kharchenko

Received: 29 May 2012 / Accepted: 6 August 2012 / Published online: 19 August 2012 # Springer-Verlag 2012

Abstract The aims of the study were to determine fecundity of several strongylid species parasitizing domestic horses and analyze possible relations between numbers of eggs in female uteri and size of both the eggs and the nematodes as well as the influence of fecundity on proportion of species in the strongylid community. Twenty-five specimens from each of 15 strongylid species (Strongylus vulgaris, Strongylus edentatus, Triodontophorus serratus, Triodontophorus brevicauda, Triodontophorus tenuicollis, Cyathostomum catinatum, Coronocyclus coronatus, Cylicocyclus nassatus, Cylicocyclus insigne, Cylicocyclus leptostomus, Cylicostephanus calicatus, Cylicostephanus goldi, Cylicostephanus longibursatus, Cylicostephanus minutus, and Poteriostomum imparidentatum) collected after necropsy were studied. The reproductive system was extracted from the female body; all eggs were removed, counted, and measured under a light microscope. Significant differences in number of eggs in female uteri of various strongylid species were observed (KruskalWallis test, p <0.001); the least numbers of eggs were registered in C. longibursatus (average 0 49) and C. leptostomus (63) and the largest number in S. edentatus (5,918). Significant correlation between nematode body size and number of eggs was observed (p <0.001). Correlation between size of eggs and body size was insignificant (Spearman R 0 0.11, p 0 0.70). Negative correlation was observed between number of eggs in female uteri and proportion of these species in strongylid community (Spearman R 0 0.78, p <0.001). Multiple linear regression of species proportion in the community on three
T. A. Kuzmina (*) : I. I. Dzeverin : V. A. Kharchenko Schmalhausen Institute of Zoology NAS of Ukraine, vul. B. Khmelnytskogo, 15, Kyiv 01601, Ukraine e-mail: taniak@izan.kiev.ua E. T. Lyons : S. C. Tolliver Department of Veterinary Science, Gluck Equine Research Center, University of Kentucky, Lexington, KY 40546-0099, USA

predictors (number of eggs, body size, and egg size) was not significant (p >0.05). However, the question on influence of fecundity on proportion of species in strongylid community needs further studies.

Introduction Nowadays, 64 strongylid (Nematoda: Strongylidae) species are described in wild and domestic equids worldwide; 14 species belong to the subfamily Strongylinae or large strongyles and 51 species to the subfamily Cyathostominae or small strongyles (Lichtenfels et al. 2008). Usually, from 10 to 20 strongylid species simultaneously parasitize one horse (Mfitilodze and Hutchinson 1990; Dvojnos and Kharchenko 1994; Silva et al. 1999; Kuzmina et al. 2005, 2007). The structure of the strongylid community in horses is not uniform; dominant, subdominant, background, and rare species are separated according to prevalence and abundance of every species (Kuzmina et al. 2007). However, 1012 of the most widespread species form the core of strongylid communities in domestic horses worldwide (Ogbourne 1976; Reinemeyer et al. 1984; Mfitilodze and Hutchinson 1990; Dvojnos and Kharchenko 1994; Gawor 1995; Bucknell et al. 1995; Lyons et al. 1996; Silva et al. 1999; Collobert-Laugier et al. 2002; Osterman Lind et al. 2003; Kuzmina et al. 2005). The number of eggs per one gram of feces (EPG) is the main measure of the level of animal infection with intestinal helminths; this level is determined by various coprological techniques such as the methods of McMaster, Stoll, etc. (Stoll 1930; Herd 1992; Bowman and Lynn 1995). The EPG data are used to determine the level of horse infection by intestinal nematodes, such as strongylids or ascarids that require deworming to prevent clinical signs of these nematodosis. Nowadays, it is widely recommended to perform routine surveillance of counts of EPG counts and use

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Parasitol Res (2012) 111:22652271

targeted strategic treatments (Kaplan 2004; Matthee and McGeoch 2004; Corning 2009). Even though the level of strongyle egg-shedding has been found to be consistent in individual horses over time (Gomez and Georgi 1991; Dpfer et al. 2004; Nielsen et al. 2006), no relationship between strongyle egg count (EPG) and adult strongylid numbers in the large intestine of horses was observed (Duncan 1974; Chapman et al. 2003; Nielsen et al. 2010). Apparently, a lack of such correlation is connected with differences in fecundity of various strongylid species that simultaneously parasitized the horse intestine. Studies in horse strongylid biology, morphology, and epidemiology were carried out for more than 100 years (Looss 1900; Boulenger 1920; Theiler 1923; Poynter 1954; Ogbourne 1971, 1975; Duncan 1974; Lichtenfels 1975; Dvojnos and Kharchenko 1994), and more than 60 species of these nematodes were described (Lichtenfels et al. 2008); however, no data on fecundity or egg productivity of various strongylids were published until now. The main objective of our study was to determine fecundity of several species of strongylids (large and small strongyles) parasitizing domestic horses. All possible relationships between number of eggs in female uteri, size of eggs, and body sizes of separate species were analyzed statistically as well as the influence of egg productivity of separate species and their proportion in the nematode community.

Materials and methods Our studies were carried out using the strongylid nematodes collected from domestic horses kept in the long-standing standard herd on the experimental farm of the Department of Veterinary Science, University of Kentucky. Research in the animals used in the study was approved by the University of Kentucky Institutional Animal Care and Use Committee under Protocol 2008-0257. Horses used for collecting strongylids in the current study never had been treated with any anthelmintic drugs. This excluded any possible influence of anthelmintics on egg production in the strongylids. All nematodes examined were collected after necropsy of horses that were used as a nontreated control group for experimental studies of efficacy of various anthelmintics. Nematodes were collected manually from the intestinal contents, fixed in 70% ethanol or alcoholformalinglycerin solution (Soulsby 1982). Only mature females that had postcopulative plugs were selected for calculation of eggs; no juvenile females without or with small number of eggs (L-5 according to Dvojnos and Kharchenko 1994) were selected for the study. All strongylids were clarified in a solution of beechwood creosote (Riedel-de Han GmbH,

Germany) for 1 h. Then, the reproductive system was extracted from the female body using a pair of entomological insect pinning needles; all eggs were removed and placed in a drop of beechwood creosote solution on a microscope slide and counted under a light microscope. Twenty-five specimens from each of 15 strongylid species (N 0 375) from seven genera were examined (Table 1). The number of eggs was measured for these specimens. ShapiroWilk test has shown that the distribution of egg number in this sample significantly differs from the normal distribution (ShapiroWilk W 0 0.67 and p <0.001 for initial data, and W 0 0.93 and p <0.001 for log-transformed data). Fifty eggs from each of these species (N 0 750) were measured using a light microscope (Zeiss Axio Imager M1). The distribution of egg size in this sample significantly differs from the normal distribution (W 0 0.93 and p <0.001 for initial data, and W 0 0.97 and p <0.001 for log-transformed data). Therefore, we used nonparametrical KruskalWallis test (H) to evaluate whether strongylid species differ in egg size and in egg number. From these data, we obtained the average egg number and egg size for each of the species. Data on mean body size of females of each of the 15 species were taken from identification keys (Lichtenfels et al. 2008). The proportion of each species in the strongylid community was calculated using the published data collected from the same herd of horses (Lyons et al. 2001). None of the variables examined appeared to be normally distributed (W 0 0.67 and p <0.001 for egg number; W 0 0.85 and p 0 0.019 for body size; W 0 0.84 and p 0 0.014 for egg size; W 0 0.57 and p <0.001 for species proportion in the community). However, they can be treated as approximately normally distributed after log transformation (W 0 0.92 and p 0 0.18 for egg number; W 0 0.92 and p 0 0.18 for body size; W 0 0.90 and p 0 0.07 for egg size; W 0 0.96 and p 0 0.66 for species proportion in community).We studied the correspondence of these estimates on a sample of 15 species using Spearman correlation coefficient and multiple regression analysis. In the regression analysis, we used species proportion as the response variable, while body size, egg size, and number of eggs as predictors. We performed the regression analysis on log-transformed data. All the calculations were performed using R software version 2.12.2 (R Development Core Team 2011).

Results Significant differences in the number of eggs in female uteri of various strongylid species were observed (N 0 375, H 0 353.3, p <0.001) (Fig. 1). The least numbers of eggs were registered in Cylicostephanus longibursatus (average, 49.0 eggs) and Cylicocyclus leptostomus (average, 63.4),

Parasitol Res (2012) 111:22652271 Table 1 Number of eggs, body, and egg size and proportion in community of 15 strongylid species examined
Species Number of eggs Average (minmax) Strongylus vulgaris (Looss, 1900) Railliet et Henry, 1909 (SVU) S. edentatus (Looss, 1900) Railliet et Henry, 1909 (SED) Triodontophorus serratus (Looss, 1900) Looss, 1902 (TSE) T. brevicauda Boulenger, 1916 (TBR) T. tenuicollis Boulenger, 1916 (TTE) Cyathostomum catinatum Looss, 1900 (CAT) Coronocyclus coronatus (Looss, 1900) Hartwich, 1986 (COR) Cylicocyclus nassatus (Looss, 1900) Foster, 1936 (NAS) C. insigne (Boulenger, 1917) Foster, 1936 (INS) C. leptostomum (Kotln, 1920) Foster, 1936 (LEP) Cylicostephanus calicatus (Looss, 1900) Ihle, 1922 (CAL) C. goldi (Boulenger, 1917) Lichtenfels, 1975 (GOL) C. longibursatus (Yorke & Macfie, 1918) Cram, 1924 (LON) C. minutus (Yorke and Macfie, 1918) Cram, 1924 (MIN) Poteriostomum imparidentatum (Quiel, 1919) (IMP) 1,641 (1,0422,098) 5,918 (4,9747,011) 1,033 (8371,185) 1,321 (6921,834) 1,377 (8632,082) 117 (60180) 136 (62228) 212 (109280) 455 (312551) 63 (47101) 114 (67151) 149 (102205) 49 (3172) 99 (48133) 3,225 (2,3733,470) SD 249.1 597.7 94.0 368.6 351.1 32.0 50.2 44.7 65.3 13.1 20.9 29.0 12.3 23.2 244.6 Body size Average (mm) 22.0 37.5 18.2 16.9 19.8 7.4 9.0 9.3 14.9 7.2 7.5 7.4 6.4 5.7 14.9 80.46 45.16 (5,713.51) 79.80 45.26 (5,679.95) 97.98 54.09 (8,332.70) 83.02 48.86 (6,374.61) 102.83 55.66 (8,988.14) 92.85 43.10 (6,287.85) 90.36 50.14 (6,072.12) 86.86 43.87 (5,989.95) 86.56 45.57 (6,202.32) 77.95 40.39 (4,946.51) 91.06 43.63 (6,243.43) 96.14 46.64 (7,053.05) 99.14 41.26 (6,427.50) 87.66 41.93 (5,777.01) 84.78 48.97 (6,520.53) Mean size of eggs (m) (area, m2)

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Proportion of the species in community (%) 0.20 0.04 0.10 0.11 0.30 37.31 0.81 7.25 0.73 2.42 2.30 9.56 35.73 1.32 0.30

and the largest number in Strongylus edentatus (average, 5,917.7) (Table 1). Significant correlations between body size of the nematodes and number of eggs in female uteri were observed (Spearman R 0 0.94, p <0.001) (Fig. 2). Species of subfamily Cyathostominae (NAS, INS, LEP, CAT, GOL, LON, MIN, CAL, COR, and IMP) significantly differed from Strongylinae species (SVU, SED, TSE, TTE, and TBR) in body size (Welchs t 0 5.83, p <0.001, for log-transformed data), number of eggs (t 0 4.78, p <0.001, for log-transformed data) as well as in proportion of species in community (t 0 5.26, p <0.001, for log-transformed data), but not in mean egg size (t 0 1.16, p 0 0.30, for log-transformed data). Significant differences were observed in the size of eggs in various strongylids species (N 0 750, H 0 469.6, p <0.001); furthermore, average egg sizes of most of species examined are similar (Fig. 3). The smallest eggs were observed in C.
Fig. 1 Variation in numbers of eggs in various strongylid species. The scaling of Y-axis is logarithmic

leptostomus (average, 77.9540.39 m), the largest eggs were observed in Triodontophorus tenuicollis (102.83 55.66 m). No statistically significant dependence between egg sizes and number of eggs in female uteri was observed (Spearman R 0 0.14, p 0 0.62). Correlation between size of eggs and body size in strongylid species was not observed (Spearman R 0 0.11, p 0 0.70; Fig. 4). Negative correlation was observed between number of eggs in female uteri and proportion of these species in the strongylid community (Spearman R 0 0.78, p < 0.001; Fig. 5). Rare species with low prevalence and the smallest proportion in the community (from 0.04 to 0.3 %) appeared to have more eggs. We tried to evaluate whether species proportion in community can be evaluated from the data on their body size and fecundity. The model of multiple linear regression of

2268 Fig. 2 Scatterplot of mean number of eggs vs. body size in various strongylid species. The scaling of Y-axis is logarithmic

Parasitol Res (2012) 111:22652271

species proportion on the set of three predictors (number of eggs, body size, and egg size) was significant [Fisher F(3, 1 1 ) 0 10.09, p 0 0.002; all the variables were logtransformed], but none of the predictors appeared to affect the response variable significantly (p 0 0.40 for number of eggs, p 0 0.35 for body size, and p 0 0.60 for egg size). Thus, it is impossible to link the abundance of strongylid species in the community with the specific values of the studied traits using this model. Most probably, it is due to the high correlation between body size and egg number (Spearman R 0 0.94, p <0.001, Fig. 2). To avoid this difficulty, we excluded body size from the analysis. We obtained the regression model of species proportion on two predictors (number of eggs and egg size) of the form of Y 8:09 1:19X1 1:21X2 where Y is the log-transformed value of species proportion in community, while X1 and X2 are log-transformed values of number of eggs and egg size, respectively. This model was significant [F(3, 11) 0 14.74, p <0.001). The input of the number of eggs in this model was significant (p <0.001), while the effect of egg size was not (p 0 0.60). It can thus be
Fig. 3 Variation in egg size in various strongylid species. The scaling of Y-axis is logarithmic

concluded that the species abundance in strongylids depends on the species fecundity (or the mean size of the adult specimens since it closely connected with fecundity) rather than the size of their eggs.

Discussion This paper presents new information regarding fecundity of various species of horse strongylids. Data on number of eggs in female uteri of 15 strongylid species are the first to broaden our knowledge on biology, morphology, and epidemiology of this group of parasites and give new information for future researched on functioning of the parasite system StrongylidesHorses and for model studies of transmission of this group of parasitic nematodes. Despite the high number of publications on biology of horse strongylids, especially Strongylus vulgaris and S. edentatus (Skarbilovich 1948; Velichkin 1955; Round 1969; Duncan and Pirie 1972; Ogbourne and Duncan 1985, etc.), no exact data on duration of life of separate strongylid species or on number of eggs they produce have been published. Data obtained in the current study give us

Parasitol Res (2012) 111:22652271 Fig. 4 Scatterplot of egg size vs. body length in various strongylid species

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approximate estimation on their fecundity and egg productivity. As observed, most of the cyathostomes produce a rather low number of eggs comparable to some parasitic nematodes of ruminants, such as Nematodirus, Ostertagia, or Trichostrongylus that produce 50100200 eggs per day (Hansen and Perry 1994), while the large strongyles (Strongylinae) produce thousands of eggs like Cooperia, Haemonchus, or Oesophagostomum. The current data showed significant differences in number of eggs in female uteri in various strongylid species (KruskalWallis test; p <0.001); herewith, the egg number differs 50100 times between species. We observed intraspecific differences in egg number two to three times that we attributed to age of the nematodes or influence of the host immunity (Michel 1976; Armour 1980; Stear et al. 1997). For the current studies, we selected only fertilized females with copulatory plugs to avoid drawbacks related to examination of juvenile or immature specimens. The correlation between the number of eggs in the female reproductive system and female size, which we observed in the current study, are typical for the majority of nematodes and other parasites (Ractliffe and Lejambre 1971; Anderson and May 1978; Morand 1996; Medica and Sukhdeo 2001).
Fig. 5 Scatterplot of number of egg vs. proportion of the strongylid species in the community. The scaling of both axes is logarithmic

However, no correlation was observed between comparing the average size of eggs of various strongylid species and body sizes of the females (Skorping et al. 1991). Comparison of the size of eggs in different species of strongylids showed that, despite the statistically significant differences in the size of eggs (KruskalWallis test, p <0.0001), it is impossible to distinguish strongylid eggs morphologically. In recent years, different molecular methods were applied to identify eggs of some strongylid species in horse feces (Hodgkinson et al. 2005; Traversa et al. 2007; Ionita et al. 2010). However, none of these methods is successful in estimating the proportion of these species in horse feces and assessing their transmission potential. In our study, the proportions of eggs expulsed by different species correlated with their proportions in strongylid community. This indicates that transmission potential of the main strongylid species depends on their fecundity more than on the survival of their free-living stages on pasture or any influence of various internal factors of the host organism (Stear et al. 1997; Medica and Sukhdeo 2001). Our data support previous observations on absence of correlation between strongyle EPG and number of adult worms in a horse intestine (Duncan 1974; Uhlinger 1993;

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Parasitol Res (2012) 111:22652271 during different seasons of the year in Louisiana. J Parasitol 89:309314 Collobert-Laugier C, Hoste H, Sevin C, Dorchies P (2002) Prevalence, abundance and site distribution of equine small strongyles in Normandy, France. Vet Parasitol 110:7783 Corning S (2009) Equine cyathostomins: a review of biology, clinical significance and therapy. Parasite Vectors 2(Suppl 2):16 Crofton HD (1971) Quantitative approach to parasitism. Parasitol 62:179193 Denwood MJ, Love S, Innocent GT, Matthews L, McKendrick IJ, Hillary N, Smith A, Reid SW (2012) Quantifying the sources of variability in equine faecal egg counts: implications for improving the utility of the method. Vet Parasitol 188:120126 Dpfer D, Kerssens CM, Meijer YG, Boersema JH, Eysker M (2004) Shedding consistency of strongyle-type eggs in Dutch boarding horses. Vet Parasitol 124:249258 Duncan JL (1974) Field studies on the epidemiology of mixed strongyle infection in the horse. Vet Rec 94:337345 Duncan JL, Pirie HM (1972) The life cycle of Strongylus vulgaris in the horse. Res Vet Sci 13:374379 Dvojnos GM, Kharchenko VA (1994) Strongilidy dikikh i domashnikh loshadej. [Strongylida of wild and domestic horses] Naukova Dumka, Kiev (in Russian) Gawor JJ (1995) The prevalence and abundance of internal parasites in working horses autopsied in Poland. Vet Parasitol 58:99108 Gomez HH, Georgi JR (1991) Equine helminth infections: control by selective chemotherapy. Equine Vet J 23:198200 Hansen J and Perry B (1994) The epidemiology, diagnosis and control of helminthes parasites of ruminants. A hand book. ILRAD, Nairobi, pp 158168 Herd RP (1992) Performing equine faecal egg counts. Vet Med 87:240244 Hodgkinson JE, Freeman KL, Lichtenfels JR, Palfreman S, Love S, Matthews JB (2005) Identification of strongyle eggs from anthelmintic-treated horses using a PCR-ELISA based on intergenic DNA sequences. Parasitol Res 95:287292 Ionita M, Howe DK, Lyons ET, Tolliver SC, Kaplan RM, Mitrea IL, Yeargan M (2010) Use of a reverse line blot assay to survey small strongyle (Strongylida: Cyathostominae) populations in horses before and after treatment with ivermectin. Vet Parasitol 168:332337 Kaplan RM (2004) Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol 20:477481 Kennedy CR (1975) Ecological animal parasitology. Blackwell, Oxford Kuzmina TA, Kharchenko VA, Starovir AI, Dvojnos GM (2005) Analysis of the strongylid nematodes (Nematoda: Strongylidae) community after deworming of brood horses in Ukraine. Vet Parasitol 131:283290 Kuzmina TA, Kharchenko VA, Zvegintsova NS (2007) Comparative study of the intestinal strongylid communities of equidae in the AskaniaNova biosphere reserve. Ukraine Helminthol 44:6269 Lichtenfels JR (1975) Helminths of domestic equids. Proc Helm Soc Wash 42:192 Lichtenfels JR, Kharchenko VA, Dvojnos GM (2008) Illustrated identification keys to strongylid parasites (Strongylidae: Nematoda) ofhorses, zebras and asses (Equidae). Vet Parasitol 156:4161 Looss A (1900) Notizen zur Helminthologie Egipten 3. Die Sclerostomen der Pferde und Esel in Egypten. Zbl Bakteriol 27 (S150 160): 184192 Lyons E, Tolliver S, Drudge J, Stamper S, Swerczek T, Granstrom D (1996) A study (19771992) of population dynamics of endoparasites featuring benzimidazole-resistant small strongyles (population S) in Shetland ponies. Vet Parasitol 66:7586 Lyons ET, Tolliver SC, Collins SS, Drudge JH (2001) Transmission of endoparasites in horse foals born on the same pasture on a farm in central Kentucky (19961999). Vet Parasitol 97:113121

Chapman et al. 2003; Nielsen et al. 2010; Denwood et al. 2012). As a horse is usually parasitized by at least 1015 strongylid species, the same EPG value can be shown by thousands of small strongyles with low egg production or by a dozen large strongyles producing thousands of eggs. Nevertheless, we cannot deny the necessity of preliminary diagnosing of horses before their deworming. As shown by long-term studies of the research group of Prof. Eugene T. Lyons at the University of Kentucky, USA, a low level of horse infection by strongylids (EPG<100) usually correlates with low number of these nematodes in horses intestine (Nielsen et al. 2010). Therefore, considering overdispersed distribution of parasites in a population of their hosts (Crofton 1971; Kennedy 1975; Anderson and May 1978), we suppose that deworming of horses with the highest levels of EPG values can significantly reduce the level of environment contamination by strongyle infective larvae and lessen spreading infection between horses. Nowadays, wide distribution of anthelmintic resistance in horse strongylids (Kaplan 2004; von SamsonHimmelstjerna 2012) requires new approaches to parasite control, and the selective treatment of the most infected animals is the most promising approach (Nielsen 2012). Besides, taking into account differences in pathogenesis of various strongylid species, we can conclude that selective treatment of horses with the highest EPG values, especially when Strongylus spp are present, should not always replace traditional routine deworming of all horses on farms and be considered as the only effective method of strongylid control.
Acknowledgments This research (paper no. 12-14-055) is published with the approval of the director of the Kentucky Agricultural Experiment Station. Appreciation is expressed to the Albert and Lorraine Clay Fellowship for partial financial support for one of the authors, Tetiana Kuzmina, to come as a visiting scientist from Ukraine to the University of Kentucky to study parasites of equids. The authors thank Dr. Iurii (Yuriy) Kuzmin from the Institute of Zoology NAS of Ukraine for his consultations and assistance in preparation of the manuscript.

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