Can parasites halt the invader? Mermithid nematodes parasitizing the yellow-legged Asian hornet in France

PeerJ

Volumn 2015, Issue 5, 2015, Pages

  Villemant, Claire ^a   Zuccon, Dario ^b   Rome, Quentin ^a   Muller, Franck ^a   Poinar, George O ^c   Justine, Jean Lou ^a  

^a Sorbonne Universités   (France)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

Asian hornet; Biological control; France; Hymenoptera; Invasive species; Nematodes

Indexed keywords

CYTOCHROME C OXIDASE; GENOMIC DNA;

ARTICLE; DNA EXTRACTION; FRANCE; FREEZE THAWING; GENE SEQUENCE; GENETIC ANALYSIS; GEOGRAPHICAL VARIATION (SPECIES); MERMITHOIDEA; MORPHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; OVERLAPPING GENE; PARASITE IDENTIFICATION; PARASITE SURVIVAL; POLYMERASE CHAIN REACTION; PUPA; SPECIES IDENTIFICATION; VESPA;

APOIDEA; CONOPIDAE; HYMENOPTERA; MERMITHIDA; NEMATODA; PHEROMERMIS; PHEROMERMIS VESPARUM; VESPA VELUTINA; VESPIDAE;

EID: 84930655402     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.947     Document Type: Article

References (61)

1. Arca M, Mougel F, Guillemaud T, Dupas S, Rome Q, Perrard A, Muller F, Fossoud A, Capdevielle-Dulac C, Torres-Leguizamon M, Chen X-X, Tan J, Jung C, Villemant C, Arnold G, Silvain J-F. 2015. Reconstructing the invasion and the demographic history of the yellow-legged hornet, Vespa velutina, in Europe. Biological Invasions Epub ahead of print Mar 24 2015 DOI 10.1007/s10530-015-0880-9.
2. Arca M, Papachristoforou A, Mougel F, Rortais A, Monceau K, Bonnard O, Tardy P, Thiéry D, Silvain J-F, Arnold G. 2014. Defensive behaviour of Apis mellifera against Vespa velutina in France: testing whether European honeybees can develop an effective collective defence against a new predator. Behavioural Processes 106:122-129 DOI 10.1016/j.beproc.2014.05.002.
3. Archer ME. 2012. Vespine wasps of the world. Behaviour, Ecology and Taxonomy of the Vespinae. Manchester: Siri Scientific Press.
4. Baker GL, Capinera JL. 1997. Nematodes and nematomorphs as control agents of grasshoppers and locusts. Memoirs of the Entomological Society of Canada 129:157-211 DOI 10.4039/entm129171157-1.
5. Barbet-Massin M, Rome Q, Muller F, Perrard A, Villemant C, Jiguet F. 2013. Climate change increases the risk of invasion by the Yellow-legged hornet. Biological Conservation 157:4-10 DOI 10.1016/j.biocon.2012.09.015.
6. Barlow ND, Beggs JR, Barron MC. 2002. Dynamics of common wasps in New Zealand beech forests: a model with density dependence and weather. Journal of Animal Ecology 71:663-671 DOI 10.1046/j.1365-2656.2002.00630.x.
7. Beggs JR, Rees JS, Toft RJ, Dennis TE, Barlow ND. 2008. Evaluating the impact of a biological control parasitoid on invasive Vespula wasps in a natural forest ecosystem. Biological Control 44:399-407 DOI 10.1016/j.biocontrol.2007.10.016.
8. Beggs JR, Brockerhoff EG, Corley JC, Kenis M, Masciocchi M, Muller F, Rome Q, Villemant C. 2011. Ecological effects and management of invasive alien Vespidae. BioControl 56:505-526 DOI 10.1007/s10526-011-9389-z.
9. Blackith RE, Stevenson JH. 1958. Autumnal populations of wasps nests. Insectes Sociaux 5:347-352 DOI 10.1007/BF02226851.
10. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ. 2004. Is invasion success explained by the enemy release hypothesis? Ecology Letters 7:721-733 DOI 10.1111/j.1461-0248.2004.00616.x.
11. Cross MA, Collins C, Campbell N, Watts PC, Chubb JC, Cunningham CO, Hatfield EMC, MacKenzie K. 2006. Levels of intra-host and temporal sequence variation in a large CO1 sub-units from Anisakis simplex sensu stricto (Rudolphi 1809) (Nematoda: Anisakisdae): implications for fisheries management. Marine Biology 151:695-702 DOI 10.1007/s00227-006-0509-8.
12. Darrouzet E, Gévar J, Dupont S. 2014. A scientific note about a parasitoid that can parasitize the yellow-legged hornet, Vespa velutina nigrithorax, in Europe. Apidologie 46:130-132 DOI 10.1007/s13592-014-0297-y.
13. Dayrat B, Tillier A, Lecointre G, Tillier S. 2001. First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Phylogenetics and Evolution 19:225-235 DOI 10.1006/mpev.2001.0926.
14. Demichelis S, Manino A, Minuto G, Mariotti M, Porporato M. 2014. Social wasp trapping in north west Italy: comparison of different bait-traps and first detection of Vespa velutina. Bulletin of Insectology 67:307-317.
15. Donovan BJ, Havron A, Leathwick DM, Ishay JS. 2002. Release of Sphecophaga orientalis Donovan (Hymenoptera: Ichneumonidae: Cryptinae) in New Zealand as a possible 'new association' biocontrol agent for the adventice social wasps Vespula germanica (F.) and Vespula vulgaris (L.) (Hymenoptera: Vespidae: Vespinae). New Zealand Entomologist 25:17-25 DOI 10.1080/00779962.2002.9722090.
16. Dunn AM. 2009. Parasites and biological invasions. In: Webster JP, ed. Natural history of host-parasite interactions, Advances in parasitology. Waltham: Academic Press, 161-184 (Chapter 7).
17. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3:294-299.
18. Fox-Wilson G. 1946. Factors affecting populations of social wasps, Vespula species, in England (Hymenoptera). In: Proceedings of the royal entomological society of London. Series A, general entomology. Hoboken: Wiley Online Library, 17-27.
19. Gambino P, Pierluisi GJ, Poinar GOJ. 1992. Field test of the nematode Steinernema feltiae (Nematoda: Steinernematidae) against yellowjacket colonies (Hym.: Vespidae). Entomophaga 37:107-114 DOI 10.1007/BF02372979.
20. Gillespie S. 2010. Factors affecting parasite prevalence among wild bumblebees. Ecological Entomology 35:737-747 DOI 10.1111/j.1365-2311.2010.01234.x.
21. Girardoz S, Kenis M, Quicke DLJ. 2006. Recruitment of native parasitoids by an exotic leaf miner, Cameraria ohridella: host-parasitoid synchronization and influence of the environment. Agricultural and Forest Entomology 8:49-56 DOI 10.1111/j.1461-9555.2006.00281.x.
22. Giribet G, Carranza S, Baguna J, Ruitort M, Ribera C. 1996. First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution 13:76-84 DOI 10.1093/oxfordjournals.molbev.a025573.
23. Gouge DH. 2005. Application for social insect control. In: Grewal PS, Ehlers RU, Shapiro-Ilan DI, eds. Nematods as biocontrol agents. Wallingford: CABI Publishing, 317-329.
24. Harris RJ, Beggs J. 1995. Variation in the quality of Vespula vulgaris (L.) queens (Hymenoptera: Vespidae) and its significance in wasp population dynamics. New Zealand Journal of Zoology 22:131-142 DOI 10.1080/03014223.1995.9518030.
25. Holt RD, Lawton JH. 1993. Apparent competition and enemy-free space in insect host-parasitoid communities. American Naturalist 142:623-645 DOI 10.1086/285561.
26. Holway DA, Suarez AV, Case TJ. 1998. Loss of intraspecific aggression in the success of a widespread invasive social insect. Science 282:949-952 DOI 10.1126/science.282.5390.949.
27. INPN. 2015. Vespa velutina Lepeletier, 1836. Available at http://inpn.mnhn.fr/espece/cd nom/433589 (accessed 19 February 2015).
28. Janet C. 1903. Observations sur les gûepes. Paris: C. Naud.
29. Kaiser H. 1987. Biologie, Okologie und Entwicklung des europaischen Wespen-Parasitoiden Pheromermis vesparum n. sp. (Mermithidae, Nematoda). In: Zoologische Jahrbucher. Abteilung fur Systematik, Okologie und Geographie der Tiere. Jena: G. Fischer.
30. Kenis M, Auger-Rozenberg M-A, Roques A, Timms L, Péré C, Cock MJW, Settele J, Augustin S, Lopez-Vaamonde C. 2009. Ecological effects of invasive alien insects. In: Langor DW, Sweeney J, eds. Ecological impacts of non-native invertebrates and fungi on terrestrial ecosystems. Amsterdam: Springer, 21-45.
31. Lacey LA, Frutos R, Kaya HK, Vail P. 2001. Insect pathogens as biological control agents: do they have a future? Biological Control 21:230-248 DOI 10.1006/bcon.2001.0938.
32. Lee KA, Klasing KC. 2004. A role for immunology in invasion biology. Trends in Ecology Evolution 19:523-529 DOI 10.1016/j.tree.2004.07.012.
33. Martin S. 1991. A simulation model for colony development of the hornet Vespa simillima (Hymenoptera, Vespidae). Japanese Journal of Entomology 59:105-124.
34. Martin SJ. 2004. A simulation model of biological control of social wasps (Vespinae) using mermithid nematodes. New Zealand Journal of Zoology 31:241-248 DOI 10.1080/03014223.2004.9518376.
35. Matsuura M, Yamane S. 1990. Biology of the vespine wasps. Berlin: Springer-Verlag.
36. Moller H, Clapperton BK, Alspach PA, Tilley JAV. 1991. Comparative seasonality of Vespula germanica (F.) and Vespula vulgaris (L.) colonies (Hymenoptera: Vespidae) in urban Nelson, New Zealand. New Zealand Journal of Zoology 18:111-120 DOI 10.1080/03014223.1991.10757957.
37. Molloy DP, Vinikour WS, Anderson RV. 1999. New North American records of aquatic insects as paratenic hosts of Pheromermis (Nematoda: Mermithidae). Journal of Invertebrate Pathology 74:89-95 DOI 10.1006/jipa.1999.4860.
38. Monceau K, Arca M, Lepretre L, Mougel F, Bonnard O, Silvain J-F, Maher N, Arnold G, Thiéry D. 2013. Native prey and invasive predator patterns of foraging activity: the case of the yellow-legged hornet predation at European Honeybee Hives. PLoS ONE 8:e66492 DOI 10.1371/journal.pone.0066492.
39. Péré C, Bell R, Turlings TCJ, Kenis M. 2011. Does the invasive horse-chestnut leaf mining moth, Cameraria ohridella, affect the native beech leaf mining weevil, Orchestes fagi, through apparent competition? Biodiversity and Conservation 20:3003-3016 DOI 10.1007/s10531-011-0134-9.
40. Perrard A, Haxaire J, Rortais A, Villemant C. 2009. Observations on the colony activity of the Asian Hornet Vespa velutina Lepeletier 1836 (hymenoptera: Vespidae: Vespinae) in France. Annales de la Société Entomologique de France 45:119-127 DOI 10.1080/00379271.2009.10697595.
41. Poinar GO. 1976. Presence of mermithidae (Nematoda) in invertebrate paratenic hosts. The Journal of Parasitology 62:843-844 DOI 10.2307/3278981.
42. Poinar Jr GO. 1979. Nematodes for biological control of insects. Boca Raton: CRC Press, Inc.
43. Poinar GOJ. 1981. Distribution of Pheromermis pachysoma (Mermithidae) determined by paratenic invertebrate hosts. Journal of Nematology 13:421-426.
44. Poinar GO, Lane RS, Thomas GM. 1976. Biology and redescription of Pheromermis pachysoma (V. Linstow) N. Gen., N. Comb. (Nematoda: Mermithidae), a parasite of yellowjackets (Hymenoptera: Vespidae). Nematologica 22:360-370 DOI 10.1163/187529276X00652.
45. Prenter J, MacNeil C, Dick JTA, Dunn AM. 2004. Roles of parasites in animal invasions. Trends in Ecology & Evolution 19:385-390 DOI 10.1016/j.tree.2004.05.002.
46. Rasplus J-Y, Villemant C, Paiva MR, Delvare G, Roques A. 2010. Hymenoptera. Chapter 12. In: Roques A, ed. Arthropod invasions in Europe. BioRisk, 669-776.
47. Rome Q, Dambrine L, Onate C, Muller F, Villemant C, Garcí{dotless}a Pérez AL, Maia M, Carvalho Esteves P, Bruneau E. 2013. Spread of the invasive hornet Vespa velutina Lepeletier, 1836, in Europe in 2012 (Hym., Vespidae). Bulletin de la Société entomologique de France 118:21-22.
48. Rome Q, Muller FJ, Touret-Alby A, Darrouzet E, Perrard A, Villemant C. 2015. Caste differentiation and seasonal changes in Vespa velutina (Hym.: Vespidae) colonies in its introduced range. Journal of Applied Entomology DOI 10.1111/jen.12210.
49. Rortais A, Villemant C, Gargominy O, Rome Q, Haxaire J, Papachristoforou A, Arnold G. 2010. A new enemy of honeybees in Europe: The Asian hornet Vespa velutina. In: Settele J, ed. Atlas of biodiversity risks - from Europe to the globe, from stories to maps. Sofia: Pensoft, 181.
50. Rose EAF, Harris RJ, Glare TR. 1999. Possible pathogens of social wasps (Hymenoptera: Vespidae) and their potential as biological control agents. New Zealand Journal of Zoology 26:179-190 DOI 10.1080/03014223.1999.9518188.
51. Roy HE, Handley L-JL, Schönrogge K, Poland RL, Purse BV. 2011. Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? BioControl 56:451-468 DOI 10.1007/s10526-011-9349-7.
52. Schmid-Hempel P, Müller C, Schmid-Hempel R, Shykoff JA. 1990. Frequency and ecological correlates of parasitism by conopid flies (Conopidae, Diptera) in populations of bumblebees. Insectes Sociaux 37:14-30 DOI 10.1007/BF02223812.
53. Schmid-Hempel P. 2001. On the evolutionary ecology of host-parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88:147-158 DOI 10.1007/s001140100222.
54. Spradbery JP. 1973. Wasps: an account of the biology and natural history of solitary and social wasps with particular reference to those of the British Isles. London: Sidgwick & Jackson.
55. Spradbery JP. 1991. An orphaned colony of the European wasp Vespula germanica (F.) (Hymenoptera: Vespidae) in Australia resulting from repeated usurpation. New Zealand Journal of Zoology 18:101-103 DOI 10.1080/03014223.1991.10757955.
56. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690 DOI 10.1093/bioinformatics/btl446.
57. Sumpter DJT, Martin SJ. 2004. The dynamics of virus epidemics in Varroa-infested honey bee colonies. Journal of Animal Ecology 73:51-63 DOI 10.1111/j.1365-2656.2004.00776.x.
58. Toft RJ, Harris RJ. 2004. Can Trapping control Asia paper wasp (Polistes chinensis antennalis) populations? New Zealand Journal of Ecology 28:279-282.
59. Torchin ME, Mitchell CE. 2004. Parasites, pathogens, and invasions by plants and animals. Frontiers in Ecology and the Environment 2:183-190 DOI 10.1890/1540-9295(2004)002[0183:PPAIBP]2.0.CO;2.
60. Villemant C, Barbet-Massin M, Perrard A, Muller F, Gargominy O, Jiguet F, Rome Q. 2011. Predicting the invasion risk by the alien bee-hawking yellow-legged hornet Vespa velutina nigrithorax across Europe and other continents with niche models. Biological Conservation 144:2142-2150 DOI 10.1016/j.biocon.2011.04.009.
61. Villemant C, Rome Q, Muller F, Arca M, Maher N, Darrouzet E. 2008. Etude de la biologie du comportement et de l'impact de Vespa velutina sur les abeilles en vue d'un controle spécifique. Programme Communautaire pour l'Apiculture, CE no. 797/2007-2010, rapport intermédiaire 2007-2008. Available at http://inpn.mnhn.fr/docs/Vespa velutina/Villemant%202008 Vespa% 20velutina%20en%20France.pdf.