Skip to main content
SpringerLink
Log in

Is there life after parasitism? Survival, longevity, and oogenesis in Acheta domesticus (Orthoptera: Gryllidae) infected with the hairworm, Paragordius varius (Phylum: Nematomorpha)

  • Arthropods and Medical Entomology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

The costs parasites impose on hosts can lead to reductions in survival and fecundity, but few studies have evaluated the impacts after infection. Hairworms are parasites of terrestrial arthropods that are free-living in aquatic systems as adults. As parasitic juveniles, hairworms acquire nutrients from their definitive hosts, shifting resources away from host development to parasite growth. However, until now, only one study has examined survivorship of naturally infected hosts with hairworms. Using a different hairworm and host system, we conducted experimental infections to examine growth, survivorship, and egg production in virgin female Acheta domesticus infected with the hairworm, Paragordius varius. We found that infected crickets grew significantly less during hairworm development compared to sham-infected control crickets. After releasing their worms, infected crickets survived for 73 ± 32 days but had significantly shorter life spans by an average of 13 days compared to sham-infected control crickets. However, we found that 50% of previously infected crickets produced eggs after releasing their worms. Taken together, these observations suggest that female crickets infected with hairworms may experience less mortality than previous anecdotal evidence suggests. Finally, we discuss the definition of parasitoid and how it relates to nematomorphs, and we suggest that more field and laboratory research is required before suggesting hairworms are parasitoids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adamo SA, Fidler TL, Forestell CA (2007) Illness-induced anorexia and its possible function in the caterpillar, Manduca sexta. Brain. Behav and Immun 21:292–300

    Article  CAS  Google Scholar 

  • Alleyne M, Beckage NE (1997) Parasitism-induced effects on host growth and metabolic efficiency in tobacco hornworm larvae parasitized by Cotesia congregate J. Insect Physiol 43:407–424

    Article  CAS  Google Scholar 

  • Anaya C, Schmidt-Rhaesa A, Hanelt B, Bolek MG (2019) A new species of Gordius (Phylum Nematomorph) from terrestrial habitats in North America. ZooKeys 892:59–75. https://doi.org/10.3897/zookeys.892.38868

    Article  PubMed  PubMed Central  Google Scholar 

  • Anaya C, Hanelt B, Bolek MG (2021) Field and laboratory observations on the life history of Gordius terrestris (Phylum Nematomorpha), a terrestrial nematomorph. J Parasitol 107:48–58 https://doi.org/10.1645/20-53

    Article  PubMed  Google Scholar 

  • Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker GH (1985) Parasites of the millipede Ommatoiulus moreletii (Lucas) (Diplopoda: Iulidae) in Portugal, and their potential as biological control agents in Australia. Aust J Zool 33:23–32

    Article  Google Scholar 

  • Biron DG, Ponton F, Joly C, Menigoz A, Hanelt B, Thomas F (2005) Water seeking behavior in insects harboring hairworms: should the host collaborate? Behav Ecol 16:656–660

    Article  Google Scholar 

  • Biron DG, Ponton F, Marché L, Galeotti N, Renault L, Demey-Thomas E, Poncet J, Brown SP, Jouin P, Thomas F (2006) ‘Suicide’ of crickets harbouring hairworms: a proteomics investigation. Insect Mol Biol 15:731–742

    Article  PubMed  Google Scholar 

  • Blair D (1983) Larval horsehair worms (Nematomorpha) from the tissues of native freshwater fish in New Zealand. N Z J Zool 10:341–344

    Article  Google Scholar 

  • Blaxter M, Koutsovoulos G (2015) The evolution of parasitism in Nematoda. Parasitology 142:S26–S39

    Article  PubMed  Google Scholar 

  • Bolek MG (2000) Records of horsehair worms Paragordius varius, Chordodes morgani and Gordius robustus (Nematomorpha) from Indiana. J Freshw Ecol 15:421–423. https://doi.org/10.1080/02705060.2000.9663760

    Article  Google Scholar 

  • Bolek MG, Rogers E, Szmygiel C, Shannon RP, Doerfert-Schrader WE, Schmidt-Rhaesa A, Hanelt B (2013a) Survival of larval and cyst stages of gordiids (Nematomorpha) after exposure to freezing. J Parasitol 99:397–402. https://doi.org/10.1645/12-62.1

    Article  PubMed  Google Scholar 

  • Bolek MG, Szmygiel C, Kubat A, Schmidt-Rhaesa A, Hanelt B (2013b) Novel techniques for biodiversity studies of gordiids and description of a new species of Chordodes (Gordiida, Nematomorpha) from Kenya. Africa Zootaxa 3717:23–38. https://doi.org/10.11646/zootaxa.3717.1.2

    Article  PubMed  Google Scholar 

  • Bolek MG, Schmidt-Rhaesa A, De Villalobos LC, Hanelt B (2015) Phylum Nematomorpha. In: Thorp, J. & Rogers, D.C. (eds.), Thorp and Covich’s freshwater invertebrates. Vol. I. Ecology and General Biology. 4th Edition. Academic Press, Boston, pp 303–326

  • Brivio MF, de Eguileor M, Grimaldi A, Vigetti D, Valvassori R, Lanzavecchia G (2000) Structural and biochemical analysis of the parasite Gordius villoti (Nematomorpha, Gordiacea) cuticle. Tissue Cell 32:366–376

    Article  CAS  PubMed  Google Scholar 

  • Cantor AB, Shuster JJ (1992) Parametric versus non-parametric methods for estimating cure rates based on censored survival data. Stat Med 11:931–937. https://doi.org/10.1002/sim.4780110710

    Article  CAS  PubMed  Google Scholar 

  • Carvalho JCM (1942) Studies on some Gordiacea of North and South America. J Parasitol 28:213–222

    Article  Google Scholar 

  • Chiu MC, Huang CH, Wu WJ, Shiao SF (2015) Morphological allometry and intersexuality in horsehair-worm-infected mantids, Hierodula formosana (Mantodea: Mantidae). Parasitol. 142:1130–1142. https://doi.org/10.1017/S0031182015000360

    Article  Google Scholar 

  • Chiu MC, Huang CH, Wu WJ, Lin ZH, Chen HW, Shiao F (2020) A new millipede-parasitizing horsehair worm, Gordius chiashanus sp. nov., at medium altitudes in Taiwan (Nematomorpha, Gordiida). ZooKeys 941:25–48. https://doi.org/10.3897/zookeys.941.49100

    Article  PubMed  PubMed Central  Google Scholar 

  • Combes C (2001) Parasitism: the ecology and evolution of intimate interactions. University of Chicago Press, 728 pp

  • Cotton S, Small J, Pomiankowski A (2006) Sexual selection and condition-dependent mate preferences. Curr Biol 16:R755–R765

    Article  CAS  PubMed  Google Scholar 

  • Crowley J, Breslow N (1984) Statistical analysis of survival data. Annu Rev Public Health 5:385–411

    Article  CAS  PubMed  Google Scholar 

  • Dorier A (1930) Classe des Gordiacés. In: Traité de Zoologie Grassé Vol. 4(3) P.P. ed Paris Masson et Cie pp 1201–1222

  • Eggleston P, Gaston KJ (1990) “Parasitoid” species and assemblages: convenient definitions or misleading compromises? Oikos 59:417–421

    Article  Google Scholar 

  • Feldman RM (1998) Parasitic castration of the crab, Tumidocarcinus giganteus Glaessner, from the Miocene of New Zealand: coevolution within the Crustacea. J Paleontol 72:493–498. https://doi.org/10.1017/S0022336000024264

    Article  Google Scholar 

  • Hanelt B (2009) An anomaly against a current paradigm-extremely low rates of individual fecundity variability of the Gordian worm (Nematomorpha: Gordiida). Parasitology 136:211–218. https://doi.org/10.1017/S0031182008005337

    Article  CAS  PubMed  Google Scholar 

  • Hanelt B, Bolek MG, Schmidt-Rhaesa A (2012) Going solo: discovery of the first parthenogenetic gordiid (Nematomorpha: Gordiida). PLoS ONE 7:1–8 e34472. https://doi.org/10.1371/journal.pone.0034472

  • Hanelt B, Janovy JJ (2004) Untying a Gordian knot: the domestication and laboratory maintenance of a Gordian worm, Paragordius varius (Nematomorpha: Gordiida). J Nat Hist 38:939–950. https://doi.org/10.1080/0022293021000058718

    Article  Google Scholar 

  • Hanelt B, Thomas F, Schmidt-Rhaesa A (2005) Biology of the phylum Nematomorpha. Adv Parasitol 59:243–309

    Article  CAS  PubMed  Google Scholar 

  • Hanelt B, Schmidt-Rhaesa A, Bolek MG (2015) Cryptic species of hairworm parasites revealed by molecular data and crowdsourcing of specimen collections. Molecular Phylogenetics and Evolution 82:211–218

  • Harvey JA, Jervis MA, Gols R, Jiang N, Vet LEM (1999) Development of the parasitoid, Cotesia rubecula (Hymenoptera: Braconidae) in Pieris rapae and Pieris brassicae (Leipidoptera: Pieridae): evidence for host regulation. J Insect Physiol 45:173–182

    Article  CAS  PubMed  Google Scholar 

  • Hurd H (1990) Parasite induced modulation of insect reproduction. Adv Invert Reprod 5:163–169

    Google Scholar 

  • Hurd H (2001) Host fecundity reduction: a strategy for damage limitation? Trends Parasitol 17:363–368

    Article  CAS  PubMed  Google Scholar 

  • Hurd H (2009) Evolutionary drivers of parasite-induced changes in insect life-history traits: from theory to underlying mechanisms. Adv Parasitol 68:85–110

    Article  PubMed  Google Scholar 

  • Hurd H, Arme C (1984) Tenebrio molitor (Coleoptera): effects of metacestodes of Hymenolepis diminuta (Cestoda) on haemolymph amino acids. Parasitology 89:245–251

    Article  CAS  Google Scholar 

  • Jolivet P (1945) De l´hydrotrophisme positif de Steropus madidus, Fabr. (Col., Pterostichidae). Misc Entomol 41:102–106

    Google Scholar 

  • Jolivet P (1948) Introduction a l´etude des Gordiacés, vers parasites d´insectes. Misc Entomol 45:83–90

    Google Scholar 

  • Kumar P, Ballal CR (1992) The effect of parasitism by Hyposoter didymator (Hym.: Ichneumonidae) on food consumption and utilization by Spodoptera litura (Lep: Noctuidae). Entomophaga 37(1992):197–203

    Article  Google Scholar 

  • Lease HM, Wolf BO (2011) Lipid content of terrestrial arthropods in relation to body size, phylogeny, ontogeny and sex. Physiol Entomol 36:29–38

    Article  CAS  Google Scholar 

  • Libersat F, Delago A, Gal R (2009) Manipulation of host behavior by parasitic insects and insect parasites. Annu Rev Entomol 54:189–207

    Article  CAS  PubMed  Google Scholar 

  • Linstow OV (1891) Weitere Beobachtungen an Gordius tolosanus and Mermis. Arch fürMikrosk Anat 37:239–249

    Article  Google Scholar 

  • Looney C, Hanelt B, Zack RS (2012) New records of Nematomorph parasites (Nematomorpha: Gordiida) of ground beetles (Coleoptera: Carabidae) and camel crickets (Orthoptera: Rhaphidophoridae) in Washington state. J Parasitol 98:554–559. https://doi.org/10.1645/GE-2929.1

    Article  PubMed  Google Scholar 

  • McCook HC (1884) Note on the intelligence of a cricket parasitised by a Gordius. Proc Acad Nat Sci Philadelphia 1884:293–294

    Google Scholar 

  • Müller GW (1920) Beobachtungen an Gordius. Zool Anz 51:225–229

    Google Scholar 

  • Nijhout HF (1979) Stretch-induced moulting in Oncopeltus fasciatus. J Insect Physiol 25:277–281. https://doi.org/10.1016/0022-1910(79)90055-6

    Article  Google Scholar 

  • Philonenko P, Postovalov S (2015) A new two-sample test for choosing between log-rank and Wilcoxon tests with right-censored data. J Stat Comput 85:2761–2770. https://doi.org/10.1080/00949655.2014.941533

    Article  Google Scholar 

  • Poinar G, Brockerhoff AM (2001) Nectonema zealandica n. sp. (Nematomorpha: Nectonematoidea) parasitizing the purple rock crab Hemigrapsus edwardsi (Brachyura: Decapoda) in New Zealand, with notes on the prevalence of infection and host defense reactions. Syst Parasitol 50:149–157

    Article  PubMed  Google Scholar 

  • Ponton F, Lalubin F, Fromont C, Wilson K, Behm C, Simpson SJ (2011) Host use altered macronutrient intake to circumvent parasite-induced reduction in fecundity. Int J Parasitol 41:43–50. https://doi.org/10.1016/j.ijpara.2010.06.007

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (1995) Hairworms (Nematomorpha: Gordioidea) infecting New Zealand short-horned grasshoppers (Orthoptera: Acrididae). J Parasitol 81:121–122

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press 332 pp

  • Sanchez MI, Ponton F, Schmidt-Rhaesa A, Hughes DP, Misse D, Thomas F (2008) Two steps to suicide in crickets harbouring hairworms. Anim Behav 76:1621–1624

    Article  Google Scholar 

  • Sato T, Arizono M, Sone R, Harada Y (2008) Parasite-mediated allochthonous input: do hairworms enhance subsidized predation of stream salmonids on crickets? Can J Zool 86:231–235. https://doi.org/10.1139/Z07-135

    Article  Google Scholar 

  • Schmidt-Rhaesa A (2013) Nematomorpha. In: Schmidt-Rhaesa A (ed) Handbook of Zoology. Gastrotricha, Cycloneuralia and Gnathifera. Nematomorpha, Priapulida, Kinorhyncha and Loricifera, vol 1. De Gruyter, Berlin, pp 29–145

    Google Scholar 

  • Schmidt-Rhaesa A, Biron DG, Joly C, Thomas F (2005) Host-parasite relations and seasonal occurrence of Paragordius tricuspidatus and Spinochordodes tellinii (Nematomorpha) in Southern France. Zool Anz – A Journal of Comparative Zoology 244:51–57. https://doi.org/10.1016/j.jcz.2005.04.002

    Article  Google Scholar 

  • Smith CL, Smilowitz Z (1976) Growth and development of Pieris rapae larvae parasitized by Apanteles glomeratus. Entomol Exp Appl 19:189–195

    Article  Google Scholar 

  • Studier EH, Lavoie KH, Chandler CM (1991) Biology of cave crickets, Hadenoecus subterraneus, and camel crickets, Ceuthophilus stygius (Insecta: Orthoptera): parasitism by hairworms (Nematomorpha). J Helminthol Soc Wash 58:248–250

    Google Scholar 

  • Szmygiel C, Schmidt-Rhaesa A, Hanelt B, Bolek MG (2014) Comparative descriptions of non-adult stages of four genera of Gordiids (Phylum: Nematomorpha). Zootaxa 3768:101–118

    Article  PubMed  Google Scholar 

  • Tanner VM (1939) Notes on the Gordiacea of Utah. Great Basin Nat 1:2

    Google Scholar 

  • Thomas F, Schmidt-Rhaesa A, Martin G, Manu C, Durand P, Renaud F (2002) Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? J Evol Biol 15:356–361. https://doi.org/10.1046/j.1420-9101.2002.00410.x

    Article  Google Scholar 

  • Thomas F, Adamo S, Moore J (2005) Parasitic manipulation: where are we and where should we go? Behav. Processes 68:185–199

    Google Scholar 

  • Thorne G (1940) The hairworm, Gordius robustus Leidy, as a parasite of the Mormon cricket, Anabrus simplex Haldeman. J Wash Acad Sci 30:219–231

    Google Scholar 

  • Townsend JI (1970) Records of Gordian worms (Nematomorpha) from New Zealand Carabidae. N Z Entomol 4:98–99

    Article  Google Scholar 

  • Von Linstow O (1891) Ueber die Entwicklungsgeschichte von Gordius tolosanus Duj. Centralbl Bacteriol Parasitenkd 9:760–762

    Google Scholar 

  • Weinersmith KL, Liu SM, Forbes AA, Egan SP (2017) Tales from the crypt: a parasitoid manipulates the behaviour of its parasite host. Proc R Soc B 284:1–8. https://doi.org/10.1098/rspb.2016.2365

    Article  Google Scholar 

  • Woodring JP, Clifford CW, Beckman BR (1979) Food utilization and metabolic efficiency in larval and adult house crickets. J Insect Physiol 25:903–912

    Article  Google Scholar 

Download references

Acknowledgements

We thank the undergraduate students who assisted us in the laboratory including Adrian Horner, Madison Young, Amanda Keck, Diana Soriano, Kenzie Hull, Mia Milliner, and Gabriel Crow. We also thank two anonymous reviewers for their constructive comments which contributed to the improvement of this manuscript.

Funding

Partial support for this work was provided by the Oklahoma State Women’s Faculty Council Student Research Award to Christina Anaya.

Author information

Author notes

  1. Christina Anaya

    Present address: Department of Integrative Biology, Oklahoma State University, 501 Life Sciences West, Stillwater, OK, 74078, USA

Authors and Affiliations

  1. Department of Integrative Biology, Oklahoma State University, 501 Life Sciences West, Stillwater, OK, 74078, USA

    Matthew G. Bolek

  2. School of Biological Sciences, University of Nebraska Lincoln, Lincoln, NE, 68588, USA

    Christina Anaya

Authors
  1. Christina Anaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew G. Bolek
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CA designed, implemented, collected data, and wrote the manuscript. MGB edited drafts.

Corresponding author

Correspondence to Christina Anaya.

Ethics declarations

Not applicable

Conflict of interest

The authors declare no competing interests.

Additional information

Section Editor: Elizabeth Marie Warburton

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Anaya, C., Bolek, M.G. Is there life after parasitism? Survival, longevity, and oogenesis in Acheta domesticus (Orthoptera: Gryllidae) infected with the hairworm, Paragordius varius (Phylum: Nematomorpha). Parasitol Res 120, 2333–2342 (2021). https://doi.org/10.1007/s00436-021-07173-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-021-07173-0

Keywords

Search

Navigation