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A comparison of two methods for quantifying parasitic nematode fecundity

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Abstract

Accurate measures of nematode fecundity can provide important information for investigating parasite life history evolution, transmission potential, and effects on host health. Understanding differences among fecundity assessment protocols and standardizing methods, where possible, will enable comparisons across different studies and host and parasite species and systems. Using the trichostrongyle nematode Cooperia fuelleborni isolated from wild African buffalo (Syncerus caffer), we compared egg recovery and enumeration between two methods for measuring the fecundity of female worms. The first method, in utero egg count, involves visual enumeration of the eggs via microscopic inspection of the uterine system. The second method, ex utero egg count, involves dissolving the same specimens from above in a sodium chloride solution to release the eggs from the female’s uterus, then enumeration under an inverted microscope. On average, the ex utero method resulted in 34% more eggs than the in utero method. However, results indicate that the two methods used to quantify parasitic nematode fecundity are highly correlated. Thus, while both methods are viable options for estimating relative nematode fecundity, we recommend caution in undertaking comparative studies that utilize egg count data collected using different methods.

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References

  • Albon SD, Stien A, Irvine RJ, Langvatn R, Ropstad E, Halvorsen O (2002) The role of parasites in the dynamics of a reindeer population. Proc R Soc Lond Ser B-Biol Sci 269:1625–1632. doi:10.1098/rspb.2002.2064

    Article  CAS  Google Scholar 

  • Benesh DP (2011) Intensity-dependent host mortality: what can it tell us about larval growth strategies in complex life cycle helminths? Parasitology 138:913–925. doi:10.1017/S0031182011000370

    Article  CAS  PubMed  Google Scholar 

  • Budischak SA, Hoberg EP, Abrams A, Jolles AE, Ezenwa VO (2015) A combined parasitological molecular approach for noninvasive characterization of parasitic nematode communities in wild hosts. Mol Ecol Resour 15:1112–1119. doi:10.1111/1755-0998.12382

    Article  PubMed  Google Scholar 

  • Chauhan PPS, Pande BP, Singh M (1972) A new species of Ashworthius Le Roux, 1930 (Haemonchinae: Trichostrongylidae) from two wild ruminants with a note on associated lesions. J Helminthol 46:149–155. doi:10.1017/S0022149X00022239

    CAS  PubMed  Google Scholar 

  • Coles GC, Bauer C, Borgsteede FHM, Geerts S, Klei TR, Taylor MA (1992) World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 44:35–44. doi:10.1016/0304-4017(92)90141-U

    Article  CAS  PubMed  Google Scholar 

  • Ezenwa VO, Jolles AE (2015) Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales. Science 347:175–177. doi:10.1126/science.1261714

    Article  CAS  PubMed  Google Scholar 

  • Faust EC, D’Antoni JS, Odom V, Miller MJ, Peres C, Sawitz W, Thomen LF, Tobie J, Walker JH (1938) A critical study of clinical laboratory technics for the diagnosis of protozoan cysts and helminth eggs in feces. AmJTrop Med Hyg 18:169–183

    Google Scholar 

  • Godfray HCJ, Partridge L, Harvey PH (1991) Clutch size. Annu Rev Ecol Syst 22:409–429. doi:10.1146/annurev.es.22.110191.002205

    Article  Google Scholar 

  • Grencis RK, Humphreys NE, Bancroft AJ (2014) Immunity to gastrointestinal nematodes: mechanisms and myths. Immunol Rev 260:183–205. doi:10.1111/imr.12188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoberg EP, Lichtenfels JR, Rickard LG (2005) Phylogeny for genera of Nematodirinae (Nematoda: Trichostrongylina). J Parasitol 91:382–389. doi:10.1645/GE-3408

    Article  PubMed  Google Scholar 

  • Hoberg E, Abrams A, Pilitt PA, Jenkins EJ (2012) Discovery and description of a new trichostrongyloid species (Nematoda: Ostertagiinae), abomasal parasites in mountain goat, Oreamnos americanus, from the western cordillera of North America. J Parasitol 98:817–846

    Article  PubMed  Google Scholar 

  • Holand H, Jensen H, Tufto J, Parn H, Saether BE, Ringsby TH, Cimmaruta R (2015) Endoparasite infection has both short- and long-term negative effects on reproductive success of female house sparrows, as revealed by faecal parasitic egg counts. PLoS One 10:e0125773. doi:10.1371/journal.pone.0125773

    Article  PubMed  PubMed Central  Google Scholar 

  • Hudson PJ, Newborn D, Dobson AP (1992) Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in red grouse. I. Monitoring and parasite reduction experiments. J Anim Ecol 61:477–486. doi:10.2307/5338

    Article  Google Scholar 

  • Kanobana K, Ploeger HW, Vervelde L (2002) Immune expulsion of the trichostrongylid Cooperia oncophora is associated with increased eosinophilia and mucosal IgA. Int J Parasitol 32:1389–1398. doi:10.1016/S0020-7519(02)00132-7

    Article  CAS  PubMed  Google Scholar 

  • Karvonen A, Cheng G-H, Seppälä O, Valtonen ET (2006) Intestinal distribution and fecundity of two species of Diplostomum parasites in definitive hosts. Parasitology 132:357–362. doi:10.1017/S0031182005009091

    Article  CAS  PubMed  Google Scholar 

  • Koprivnikar J, Marcogliese DJ, Rohr JR, Orlofske SA, Raffel TR, Johnson PTJ (2012) Macroparasite infections of amphibians: what can they tell us? EcoHealth 9:342–360. doi:10.1007/s10393-012-0785-3

    Article  PubMed  Google Scholar 

  • Kuzmina TA, Lyons ET, Tolliver SC, Dzeverin II, Kharchenko VA (2012) Fecundity of various species of strongylids (Nematoda: Strongylidae)-parasites of domestic horses. Parasitol Res 111:2265–2271. doi:10.1007/s00436-012-3077-5

    Article  CAS  PubMed  Google Scholar 

  • Lichtenfels JR, Pilitt PA, Gibbons LM, Hoberg EP (2002) Redescriptions of Haemonchus mitchelli and Haemonchus okapiae (Nematoda: Trichostrongyloidea) and description of a unique synlophe for the Haemonchinae. J Parasitol 88:947–960. doi:10.1645/0022-3395(2002)088[0947:ROHMAH]2.0.CO;2

    Article  PubMed  Google Scholar 

  • May RM, Anderson RM (1979) Population biology of infectious diseases: part II. Nature 280:455–461. doi:10.1038/280455a0

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (1995) Clutch size and egg size in free-living and parasitic copepods: a comparative analysis. Evolution 49:325–336. doi:10.2307/2410343

    Article  Google Scholar 

  • Poulin R (1997) Egg production in adult trematodes: adaptation or constraint? Parasitology 114:195–204. doi:10.1017/S0031182096008372

    Article  PubMed  Google Scholar 

  • Romeo C, Wauters LA, Cauchie S, Martinoli A, Matthysen E, Saino N, Ferrari N (2014) Faecal egg counts from field experiment reveal density dependence in helminth fecundity: Strongyloides robustus infecting grey squirrels (Sciurus carolinensis). Parasitol Res 113:3403–3408. doi:10.1007/s00436-014-4005-7

    Article  PubMed  Google Scholar 

  • Rowe A, McMaster K, Emery D, Sangster N (2008) Haemonchus contortus infection in sheep: parasite fecundity correlates with worm size and host lymphocyte counts. Vet Parasitol 153:285–293. doi:10.1016/j.vetpar.2008.01.040

    Article  PubMed  Google Scholar 

  • Shaw DJ, Dobson AP (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111:S111–S133. doi:10.1017/S0031182000075855

    Article  PubMed  Google Scholar 

  • Singleton DR, Stear MJ, Matthews L (2011) A mechanistic model of developing immunity to Teladorsagia circumcincta infection in lambs. Parasitology 138:322–332. doi:10.1017/S0031182010001289

    Article  CAS  PubMed  Google Scholar 

  • Skorping A, Read AF, Keymer AE (1991) Life history covariation in intestinal nematodes of mammals. Oikos 60:365. doi:10.2307/3545079

    Article  Google Scholar 

  • Skrjabin KI, Shikobalova NP, Shul’tz RS (1954) Trichostrongylids of animals and man. Osnovy Nematodologii III. Isdatel’stvo Akademii Nauk SSSR. English Translation, 1960, US Department of Agriculture and Israel Program for Scientfic Translations, Jerusalem, Moskva

  • Stien A, Irvine RJ, Ropstad E, Halvorsen O, Langvatn R, Albon SD (2002) The impact of gastrointestinal nematodes on wild reindeer: experimental and cross-sectional studies. J Anim Ecol 71:937–945. doi:10.1046/j.1365-2656.2002.00659.x

    Article  Google Scholar 

  • Stjernman M, Råberg L, Nilsson J-Å (2008) Maximum host survival at intermediate parasite infection intensities. PLoS One 3:e2463. doi:10.1371/journal.pone.0002463

    Article  PubMed  PubMed Central  Google Scholar 

  • Wood IB, Amaral NK, Bairden K, Duncan JL, Kassai T, Malone JB, Pankavich JA, Reinecke RK, Slocombe O, Taylor SM, Vercruysse J (1995) World Association for the Advancement of Veterinary Parasitology (WAAVP) of guidelines for evaluating the efficacy of anthelmintics in ruminants (bovine, ovine, caprine). Vet Parasitol 58:181–213. doi:10.1016/0304-4017(95)00806-2

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Many thanks to South Africa National Parks Veterinary Services for assistance with the animal capture operations. We thank R. Spaan, J. Spaan, A. Majewska, J. Alagappan, C. Becker, B. Beechler, E. Belinfante, E. Gorsich, C. Gondhalekar, C. Hebbale, T. Lavelle, L. Leathers, L. Megow, T. Mowla, A. Petrelli, K. Raum, N. Rogers, K. Sakamoto, P. Snyder, and M. Smith for invaluable assistance in the field and in the lab. All animal protocols were approved by the UGA Institutional Animal Care and Use Committee (AUP#: A2013 08-017-Y1-A0; AUP#: A2010 10-190-Y3-A5). This work was funded by the National Science Foundation Ecology of Infectious Diseases Grant to VOE and AEJ (DEB-1102493, EF-0723928). LVA was supported by a Georgia Museum of Natural History’s Joshua Laerm Academic Support Award for Undergraduate Research and an NSF REU supplement to DEB-1102493; JR was supported by the NSF Population of Infectious Diseases REU Program at the University of Georgia (DBI-1156707).

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Correspondence to Sarah A. Budischak.

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Austin, L.V., Budischak, S.A., Ramadhin, J. et al. A comparison of two methods for quantifying parasitic nematode fecundity. Parasitol Res 116, 1597–1602 (2017). https://doi.org/10.1007/s00436-017-5436-8

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