Skip to main content

Host Behavioural Manipulation of Spiders by Ichneumonid Wasps

  • Chapter
  • First Online:
Behaviour and Ecology of Spiders

Abstract

Modified webs constructed by spiders parasitized by Ichneumonid wasps were first mentioned in literature in 1771. These initial observations were restricted to the description of the cocoon web spun by an unidentified spider species presenting a cocoon attached. Only in the year 2000 was the subject intensively studied in another host/parasitoid system. The interaction between Leucauge argyra (Tetragnathidae) and Hymenoepimecis argyraphaga (Ichneumonidae) was carefully described by W. G. Eberhard in Costa Rica. Web modifications, in this case, are even more extensive than those previously recorded. Cocoon webs spun by L. argyra are composed of just a few strong lines. Spirals are absent, and the cocoon remains suspended attached to the hub of the structure. From these studies up to now, several other cases have been described in the Neotropics. The initial doubt about the generality of host manipulation involving the Polysphincta genus-group was solved, but many questions arise from the subsequent studies. We still know almost nothing about the mechanisms involved in manipulation, for example. Recent studies suggest that it involves the injection of some substance by the parasitoid onto its host because the removal of the attached larva leads to a restoration of the original web patterns. Another interesting aspect is the investigation of how the structure of normal webs affects the design of cocoon webs. Finally, it is important to demonstrate that specific alterations in normal webs result in benefits to the manipulative wasp. The objectives of this chapter are to present an overview of recent discoveries involving these interactions, a brief historical summary of the researching efforts in the Neotropical region, and perspectives for future studies.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fish 10:131–165

    Article  Google Scholar 

  • Barnard CJ, Behnke JM (1990) Parasitism and host behaviour. Taylor and Francis, London

    Google Scholar 

  • Barrantes G, Eberhard WG, Weng J (2008) Seasonal patterns of parasitism of the tropical spiders Theridion evexum (Araneae, Theridiidae) and Allocyclosa bifurca (Araneae, Araneidae) by the wasps Zatypota petronae and Polysphincta gutfreundi (Hymenoptera, Ichneumonidae). Rev Biol Trop 56:749–754

    PubMed  Google Scholar 

  • Berdoy M, Webster JP, Macdonald DW (2000) Fatal attraction in rats infected with Toxoplasma gondii. Proc R Soc Lond B 267:1591–1594

    Article  CAS  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 

  • Bovee J, Leech R (2014) Araneus gemmoides (Araneae, Araneidae) death by a parasitoid (Hymenoptera Ichneumonidae). Bull Entomol Soc Can 46:86–90

    Google Scholar 

  • Cram ER (1931) Developmental stages of some nematodes of the Spiruroidea parasitic in poultry and game birds. USDA Technical Bulletin, Beltsville

    Google Scholar 

  • De Geer C (1771) Memoires pour servir à l’histoire des insects. French Grefing and Hesselberg, Stockholm, Sweden.

    Google Scholar 

  • Dubois J, Rollard C, Villemant C, Gauld ID (2002) The phylogenetic position of parasitoids of spiders within Pimplinae (Hymenoptera, Ichneumonidae). In: Samu F, Szinetár CS (eds) Proceedings of the 20th European Colloquium of Arachnology, Budapest

    Google Scholar 

  • Eberhard WG (2000a) The natural history and behavior of Hymenoepimecis argyraphaga (Hymenoptera: Ichneumonidae) a parasitoid of Plesiometa argyra (Araneae, Tetragnathidae). J Hymenopt Res 9:220–240

    Google Scholar 

  • Eberhard WG (2000b) Spider manipulation by a wasp larva. Nature 406:255–256

    Article  CAS  PubMed  Google Scholar 

  • Eberhard WG (2001) Under the influence: webs and building behavior of Plesiometa argyra (Araneae, Tetragnathidae) when parasitized by Hymenoepimecis argyraphaga (Hymenoptera, Ichneumonidae). J Arachnol 29:354–366

    Article  Google Scholar 

  • Eberhard WG (2010a) Recovery of spiders from the effects of parasitic wasps: implications for fine-tuned mechanisms of manipulation. Anim Behav 79:375–383

    Article  Google Scholar 

  • Eberhard WG (2010b) New types of behavioral manipulation of host spiders by a parasitoid wasp. Psyche. https://doi.org/10.1155/2010/950614

  • Eberhard WG (2013) The polysphinctine wasps Acrotaphus tibialis, Euga ca. gutfreund, and Hymenoepimecis tedfordi (Hymenoptera, Ichneumonidae, Pimplinae) induce their host spiders to build modified webs. Ann Entomol Soc Am 106:652–660

    Article  Google Scholar 

  • Fincke OM, Higgins L, Rojas E (1990) Parasitism of Nephila clavipes (Araneae, Tetragnathidae) by an ichneumonid (Hymenoptera, Polysphinctini) in Panama. J Arachnol 18:321–329

    Google Scholar 

  • Fritz RS (1982) Selection for host behavior modification by parasitoids. Evolution 36:283–288

    Article  PubMed  Google Scholar 

  • Gauld ID (2000) The re-definition of pimpline genus Hymenoepimecis (Hymenoptera: Ichneumonidae) with a description of a plesiomorphic new Costa Rican species. J Hymenopt Res 9:213–219

    Google Scholar 

  • Gauld ID, Dubois J (2006) Phylogeny of the Polysphincta group of genera (Hymenoptera: Ichneumonidae; Pimplinae): a taxonomic revision of spider ectoparasitoids. Syst Entomol 31:529–564

    Article  Google Scholar 

  • Godfray HCJ (1994) Parasitoids: behavioural and evolutionary ecology. Princeton University Press, Princeton

    Google Scholar 

  • Gonzaga MO, Sobczak JF (2007) Parasitoid-induced mortality of Araneus omnicolor (Araneae, Araneidae) by Hymenoepimecis sp. (Hymenoptera, Ichneumonidae) in southeastern Brazil. Naturwissenschaften 93:223–227

    Article  Google Scholar 

  • Gonzaga MO, Sobczak JF (2011) Behavioral manipulation of the orb-weaver spider Argiope argentata (Araneae: Araneidae) by Acrotaphus chedelae (Hymenoptera: Ichneumonidae). Entomol Sci 14:220–223

    Article  Google Scholar 

  • Gonzaga MO, Sobczak JF, Penteado-Dias AM, Eberhard WG (2010) Modification of Nephila clavipes (Araneae, Nephilidae) webs induced by the parasitoids Hymenoepimecis bicolor and H. robertsae (Hymenoptera Ichneumonidae). Ethol Ecol Evol 22:151–165

    Article  Google Scholar 

  • Gonzaga MO, Cardoso JFC, Vasconcellos-Neto J (2015a) Do parasitoids explain differential abundance of two syntopic orb-weaver spiders (Araneae: Araneidae)? Acta Oecol 69:113–120

    Article  Google Scholar 

  • Gonzaga MO, Moura RR, Pêgo PT, Bang DL, Meira FA (2015b) Changes to web architecture of Leucauge volupis (Araneae: Tetragnathidae) induced by the parasitoid Hymenoepimecis jordanensis (Hymenoptera: Ichneumonidae). Behaviour 152:181–193

    Article  Google Scholar 

  • Gonzaga MO, Loffredo AP, Penteado-Dias AM, Cardoso JCF (2016) Host behavior modification of Achaearanea tingo (Araneae: Theridiidae) induced by the parasitoid wasp Zatypota alborhombarta (Hymenoptera: Ichneumonidae). Entomol Sci 19:133–137

    Article  Google Scholar 

  • Grosman AH, Janssen A, Brito EF, Cordeiro EG, Colares F, Fonseca JO, Lima ER, Pallini A, Sabelis MW (2008) Parasitoid increases survival of its pupae by inducing hosts to fight predators. PLoS One 3(6):e2276

    Article  PubMed  PubMed Central  Google Scholar 

  • Hafer N (2016) Conflicts over host manipulation between different parasites and pathogens: investigating the ecological and medical consequences. BioEssays 38:1027–1037

    Article  PubMed  PubMed Central  Google Scholar 

  • Hafer N, Milinski M (2016) Inter- and intraspecific conflicts between parasites over host manipulation. Proc R Soc Lond B 283:20152870

    Article  Google Scholar 

  • Hansen EK, Poulin R (2005) Impact of a microphallid trematode on the behaviour and survival of its isopod intermediate host: phylogenetic inheritance? Parasitol Res 97:242–246

    Article  PubMed  Google Scholar 

  • Holmes JC, Bethel WM (1972) Modification of intermediate host behaviour by parasites. In: Canning EU, Wright CA (eds) Behavioural aspects of parasite transmission. Academic Press, London, pp 123–149

    Google Scholar 

  • Hughes DP, Brodeur J, Thomas F (2012) Host manipulation by parasites. Oxford University Press, Oxford

    Book  Google Scholar 

  • Kloss TG, Gonzaga MO, Rouxinol JAM, Sperber CF (2016a) Host behavioural manipulation of two orb-weaver spiders by parasitoid wasps. Anim Behav 111:289–296

    Article  Google Scholar 

  • Kloss TG, Gonzaga MO, Rouxinol JAM, Sperber CF (2016b) Attack behavior of two wasp species of the Polysphincta genus group (Hymenoptera, Ichneumonidae) on their orb-weaver spider hosts (Araneae, Araneidae). J Insect Behav 29:315–324

    Article  Google Scholar 

  • Kloss TG, Gonzaga MO, Oliveira LL, Sperber CF (2017) Proximate mechanism of behavioral manipulation of an orb-weaver spider host by a parasitoid wasp. PLoS One 12(2):e0171336

    Article  PubMed  PubMed Central  Google Scholar 

  • Korenko S, Pekár S (2011) A parasitoid wasp induces overwintering behaviour in its spider host. PLoS One 6(9):e24628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korenko S, Michalkova V, Zwakhals K et al (2011) Host specificity and temporal and seasonal shifts in host preference of a web-spider parasitoid Zatypota percontatoria. J Insect Sci 11:1–12

    Article  Google Scholar 

  • Korenko S, Isaia M, Satrapová J, Pekár S (2014) Parasitoid genus-specific manipulation of orb-web host spiders (Araneae, Araneidae). Ecol Entomol 39:30–38

    Article  Google Scholar 

  • Korenko S, Korenková B, Satrapová J et al (2015a) Modification of Tetragnatha montana (Araneae, Tetragnathidae) web architecture induced by larva of the parasitoid Acrodactyla quadrisculpta (Hymenoptera, Ichneumonidae, Polysphincta genus-group). Zool Stud 54:40

    Article  Google Scholar 

  • Korenko S, Satrapová J, Zwakhals K (2015b) Manipulation of araneid spider web architecture by the polysphinctine parasitoid Zatypota picticollis (Hymenoptera: Ichneumonidae: Pimplinae). Entomol Sci 18:383–388

    Article  Google Scholar 

  • Lafferty KD, Shaw JC (2013) Comparing mechanisms of host manipulation across host and parasite taxa. J Exp Biol 216:56–66

    Article  PubMed  Google Scholar 

  • Matsumoto R (2009) “Veils” against predators: modified web structure of a host spider induced by an ichneumonid parasitoid, Brachyzapus nikkoensis (Uchida) (Hymenoptera). J Insect Behav 22:39–48

    Article  Google Scholar 

  • Matsumoto R (2016) Molecular phylogeny and systematics of the Polysphincta group of genera (Hymenoptera, Ichneumonidae, Pimplinae). Syst Entomol 41:854–864

    Article  Google Scholar 

  • Matsumoto R, Konishi K (2007) Life histories of two ichneumonid parasitoids of Cyclosa octotuberculata (Araneae): Reclinervellus tuberculatus (Uchida) and its new sympatric congener (Hymenoptera: Ichneumonidae: Pimplinae). Entomol Sci 10:67–278

    Article  Google Scholar 

  • McLachlan A (1999) Parasites promote mating success: the case of a midge and a mite. Anim Behav 57:1199–1205

    Article  CAS  PubMed  Google Scholar 

  • Moore J (1984) Altered behavioral responses in intermediate hosts — an Acanthoceptalan parasite strategy. Am Nat 123:572–577

    Article  Google Scholar 

  • Moore J (2002) Parasites and the behavior of animals. Oxford University Press, Oxford

    Google Scholar 

  • Nielsen E (1923) Contributions to the life history of the Pimpline spider parasites (Polysphincta, Zaglyptus, Tromatobia) (Hym. Ichneum.) Entomol Medd 14:137–205

    Google Scholar 

  • Pádua DG, Salvatierra L, Sobczak JF, Oliveira ML (2016) Parasitism of Hymenoepimecis manauara Pádua and Oliveira (Hymenoptera: Ichneumonidae: Pimplinae) on Leucauge henryi Mello-Leitão (Araneae: Tetragnathidae) in Brazilian Amazonian. Biodivers Data J. https://doi.org/10.3897/BDJ.4.e11219

  • Pallacio E, Sääksjärvi IE, Vahtera V (2007) Lamnatibia, a new genus of the Polysphincta group of genera from Colombia (Hymenoptera: Ichneumonidae; Pimplinae). Zootaxa 1431:55–63

    Article  Google Scholar 

  • Poulin R (2000) Manipulation of host behaviour by parasites: a weakening paradigm? Proc R Soc Lond B 267:787–792

    Article  CAS  Google Scholar 

  • Shaw JC, Korzan WJ, Carpenter RE, Kuris AM, Lafferty KD, Summers CH, Øverli Ø (2009) Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis. Proc R Soc Lond B 276:1137–1146

    Article  CAS  Google Scholar 

  • Sobczak JF (2013) Estudos biológicos e ecológicos da interação entre Nephila clavipes (Araneae, Nephilidae) e o parasitoide Hymenoepimecis bicolor (Hymenoptera, Ichneumonidae, Pimplinae). PhD Thesis, Universidade Federal de São Carlos

    Google Scholar 

  • Sobczak JF, Loffredo APS, Penteado-Dias AM, Gonzaga MO (2009) Two new species of Hymenoepimecis (Hymenoptera: Ichneumonidae: Pimplinae) with notes on their spider hosts and behaviour manipulation. J Nat Hist 43:2691–2699

    Article  Google Scholar 

  • Sobczak JF, Loffredo APS, Carmago LF, Penteado-Dias AM (2012a) Hymenoepimecis neotropica (Brues and Richardson) (Hymenoptera, Ichneumonidae, Pimplinae) parasitoid of Araneus omnicolor (Keyserling) (Araneae, Araneidae): first host record and new occurrence to Brazil. Rev Bras Entomol 56:390–392

    Article  Google Scholar 

  • Sobczak JF, Loffredo APS, Penteado-Dias AM (2012b) Parasitism on Araneus venatrix (Koch, 1838) (Araneae: Araneidae) by Hymenoepimecis silvanae Loffredo and Penteado-Dias, 2009 (Ichneumonidae, Pimplinae) with description of male of the wasp. Braz J Biol 72:221–223

    Article  CAS  PubMed  Google Scholar 

  • Sobczak JF, Sobczak JCMSM, Messas YF, Souza HS, Vasconcellos-Neto J (2014) A new record of a host-parasitoid interaction: Hymenoepimecis veranii Lofredo and Penteado-Dias, 2009 (Hymenoptera: Ichneumonidae) parasitizing Araneus orgaos Levi, 1991 (Araneae: Araneidae). J Insect Behav 27:753–758

    Article  Google Scholar 

  • Soghigian J, Valsdottir LR, Livdahl TP (2017) A parasite’s modification of host behavior reduces predation on its host. Ecol Evol 7:1453–1461

    Article  PubMed  PubMed Central  Google Scholar 

  • Takasuka K, Matsumoto R (2011a) Lying on the dorsum: unique host-attacking behaviour of Zatypota albicoxa (Hymenoptera, Ichneumonidae). J Ethol 29:203–207

    Article  Google Scholar 

  • Takasuka K, Matsumoto R (2011b) Infanticide by a solitary koinobiont ichneumonid ectoparasitoid of spiders. Naturwissenschaften 98:529–536

    Article  CAS  PubMed  Google Scholar 

  • Takasuka K, Matsumoto R, Ohbayashi N (2009) Oviposition behavior of Zatypota albicoxa (Hymenoptera, Ichenumonidae), an ectoparasitoid of Achaearanea tepidariorum (Araneae, Theridiidae). Entomol Sci 12:232–237

    Article  Google Scholar 

  • Takasuka K, Yasui T, Ishigami T, Nakata K, Matsumoto R, Ikeda K, Maeto K (2015) Host manipulation by an ichneumonid spider-ectoparasitoid that takes advantage of preprogrammed web-building behaviours for its cocoon protection. J Exp Biol 218:2326–2332

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Van Dobben WH (1952) The food of the cormorant in the Netherlands. Ardea 40:1–63

    Google Scholar 

  • Vinson SB (1975) Biochemical coevolution between parasitoids and their host. In: Price PW (ed) Evolutionary strategies of parasitic insects and mites. Plenum Press, New York, pp 14–48

    Chapter  Google Scholar 

  • Weng JL, Barrantes G (2007) Natural history and larval behavior of the parasitoid Zatypota petronae (Hymenoptera: Ichneumonidae). J Hymenopt Res 16:326–335

    Google Scholar 

  • Wesolowska W, Wesolowski T (2014) Do Leucochloridium sporocysts manipulate the behaviour of their snail hosts? J Zool 292:151–155

    Article  Google Scholar 

  • Wickler W (1976) Evolution-oriented ethology, kin selection, and altruistic parasites. Z Tierpsychol 42:206–214

    Article  CAS  PubMed  Google Scholar 

  • Witt PN (1971) Drugs alter web-building of spiders: a review and evaluation. Behav Sci 16:98–113

    Article  CAS  PubMed  Google Scholar 

  • Yanoviak SP, Kaspary M, Dudley R, Poinar G Jr (2008) Parasite-induced fruit mimicry in a tropical canopy ant. Am Nat 171:536–544

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marcelo O. Gonzaga .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Gonzaga, M.O., Kloss, T.G., Sobczak, J.F. (2017). Host Behavioural Manipulation of Spiders by Ichneumonid Wasps. In: Viera, C., Gonzaga, M. (eds) Behaviour and Ecology of Spiders. Springer, Cham. https://doi.org/10.1007/978-3-319-65717-2_16

Download citation

Publish with us

Policies and ethics