Abstract
Parasitoid wasps may act as hyperparasites and sometimes regulate the populations of their hosts by a top-down dynamic. Nasonia vitripennis (Walker, 1836) is a generalist gregarious parasitoid that parasitizes several host flies, including the blowfly Protocalliphora Hough, 1899 (Diptera, Calliphoridae), which in turn parasitizes bird nestlings. Nonetheless, the ecological factors underlying N. vitripennis prevalence and parasitoidism intensity on its hosts in natural populations are poorly understood. We have studied the prevalence of N. vitripennis in Protocalliphora azurea (Fallén, 1817) puparia parasitizing wild populations of pied flycatcher (Ficedula hypoleuca) and blue tit (Cyanistes caeruleus) birds in two Mediterranean areas in central and southern Spain. We found some evidence that the prevalence of N. vitripennis was higher in moist habitats in southern Spain. A host-dependent effect was found, since the greater the number of P. azurea puparia, the greater the probability and rate of parasitoidism by the wasp. Our results also suggest that N. vitripennis parasitizes more P. azurea puparia in blue tit nests than in pied flycatcher nests as a consequence of a higher load of these flies in the former. Based on the high prevalence of N. vitripennis in P. azurea puparia in nature, we propose that this wasp may regulate blowfly populations, with possible positive effects on the reproduction of both bird species.
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Aung KSD, Takagi M, Myint YY et al (2011) Effect of host density on the progeny production of the egg parasitoids Ooencyrtus nezarae (Ishii) (Hymenoptera: Encyrtidae). J Fac Agric Kyushu Univ 56:71–74
Bennett GF, Whitworth TL (1991) Studies on the life history of some species of Protocalliphora (Diptera: Calliphoridae). Can J Zool 69:2048–2058. https://doi.org/10.1139/z91-286
Camacho C, Canal D, Potti J (2015) Testing the matching habitat choice hypothesis in nature: phenotype-environment correlation and fitness in a songbird population. Evol Ecol 29:873–886. https://doi.org/10.1007/s10682-015-9793-4
Cook N, Parker DJ, Turner F et al (2018) Genome-wide disruption of DNA methylation by 5-aza-2’-deoxycytidine in the parasitoid wasp. bioRxiv:437202. https://doi.org/10.1101/437202
Daoust SP, Savage J, Whitworth TL et al (2012) Diversity and abundance of ectoparasitic blow flies Protocalliphora (Diptera: Calliphoridae) and their Nasonia (Hymenoptera: Pteromalidae) parasitoids in tree swallow nests within agricultural lands of southern Québec, Canada. Ann Entomol Soc Am 105:471–478. https://doi.org/10.1603/AN11155
De Lange ES, Farnier K, Degen T et al (2018) Parasitic wasps can reduce mortality of teosinte plants infested with fall armyworm: support for a defensive function of herbivore-induced plant volatiles. Front Ecol Evol 6:55. https://doi.org/10.3389/fevo.2018.00055
Desjardins CA, Perfectti F, Bartos JD, Enders LS, Werren JH (2010) The genetic basis of interspecies host preference differences in the model parasitoid Nasonia. Heredity 104:270–277. https://doi.org/10.1038/hdy.2009.145
Draber-Monko A (1995) Protocalliphora azurea (Fall.) (Diptera, Calliphoridae) and other insects found in nests of sparrows, Passer domesticus (L.) and Passer montanus (L.) in the vicinity of Warsaw. Int Stud Sparrows 22:3–10
Edwards RL (1954) The effect of diet on egg maturation and resorption in Mormoniella vitripennis (Hymenoptera, Pteromalidae). Q J Microsc Sci 95:459–468
Floate KD, Skovgård H (2004) Winter survival of nuisance fly parasitoids (Hymenoptera: Pteromalidae) in Canada and Denmark. Bull Entomol Res 94:331–340. https://doi.org/10.1079/BER2003308
Foottit R, Adler PH (eds) (2017) Insect biodiversity: science and society, 2nd edn. New Jersey, John Wiley & Sons, Inc, Hoboken
Frederickx C, Dekeirsschieter J, Verheggen FJ, Haubruge E (2014) Depth and type of substrate influence the ability of Nasonia vitripennis to locate a host. J Insect Sci 14:58. https://doi.org/10.1093/jis/14.1.58
Godfray HCJ (2010) Nasonia: a jewel among wasps. Heredity 104:235–236. https://doi.org/10.1038/hdy.2010.3
Gold CS, Dahlsten DL (1989) Prevalence, habitat selection and biology of Protocalliphora (Diptera: Calliphoridae) found in nests of mountain and chestnut-backed chickadees in California. Hilgardia 57:1–19. https://doi.org/10.3733/hilg.v57n02p019
Grillenberger BK, Koevoets T, Burton-Chellew MN, Sykes EM, Shuker DM, van de Zande L, Bijlsma R, Gadau J, Beukeboom LW (2008) Genetic structure of natural Nasonia vitripennis populations: validating assumptions of sex-ratio theory. Mol Ecol 17:2854–2864. https://doi.org/10.1111/j.1365-294X.2008.03800.x
Grillenberger BK, Van De Zande L, Bijlsma R et al (2009) Reproductive strategies under multiparasitism in natural populations of the parasitoid wasp Nasonia (Hymenoptera). J Evol Biol 22:460–470. https://doi.org/10.1111/j.1420-9101.2008.01677.x
Hannam K (2006) Ectoparasitic blow flies (Protocalliphora sp.) and nestling eastern bluebirds (Sialia sialis): direct effects and compensatory strategies. Can J Zool 84:921–930. https://doi.org/10.1139/z06-079
Hawkins BA (1992) Parasitoid-host food webs and donor control. Oikos 65:159–162. https://doi.org/10.2307/3544898
Heads PA, Lawton JH (1983) Studies on the natural enemy complex of the holly leaf-miner: the effects of scale on the detection of aggregative responses and the implications for biological control. Oikos 40:267. https://doi.org/10.2307/3544591
Hochberg ME, Ives AR (eds) (2000) Parasitoid population biology. Princeton University Press, Princeton, New Jersey
Hurtrez-Boussès S, Perret P, Renaud F, Blondel J (1997) High blowfly parasitic loads affect breeding success in a Mediterranean population of blue tits. Oecologia 112:514–517. https://doi.org/10.1007/s004420050339
Johnson LS, Albrecht DJ (1993) Effects of haematophagous ectoparasites on nestling house wrens, Troglodytes aedon: who pays the cost of parasitism? Oikos 66:255. https://doi.org/10.2307/3544812
Kaufman PE, Long SJ, Rutz DA, Waldron JK (2001) Parasitism rates of Muscidifurax raptorellus and Nasonia vitripennis (Hymenoptera: Pteromalidae) after individual and paired releases in New York poultry facilities. J Econ Entomol 94:593–598. https://doi.org/10.1603/0022-0493-94.2.593
Lynch JA, Brent AE, Leaf DS, Pultz MA, Desplan C (2006) Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature 439:728–732. https://doi.org/10.1038/nature04445
Marchiori CH (2004) Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) parasitóide de dípteros muscóides coletado em Itumbiara, Goiás. Arq Bras Med Veterinária E Zootec 56:422–424. https://doi.org/10.1590/S0102-09352004000300024
Marchiori CH, Leles AS, Carvalho SAD, Rodrigues RF (2007) Parasitóides de dípteros muscóides coletados no matadouro Alvorada em Itumbiara, sul de Goiás, Brasil. Rev Bras Parasitol Veterinária 16:235–237. https://doi.org/10.1590/S1984-29612007000400010
May RM (1978) Host-parasitoid systems in patchy environments: a phenomenological model. J Anim Ecol 47:833–844
May RM, Hassell MP, Anderson RM, Tonkyn DW (1981) Density dependence in host-parasitoid models. J Anim Ecol 50:855–865. https://doi.org/10.2307/4142
Merino S, Potti J (1995) Mites and blowflies decrease growth and survival in nestling pied flycatchers. Oikos 73:95. https://doi.org/10.2307/3545730
Miller CK, Fair JM (1997) Effects of blow fly (Protocalliphora spatulata: Diptera: Calliphoridae) parasitism on the growth of nestling savannah sparrows in Alaska. Can J Zool 75:641–644. https://doi.org/10.1139/z97-080
Møller AP (1989) Parasites, predators and nest boxes: facts and artefacts in nest box studies of birds? Oikos 56:421–423. https://doi.org/10.2307/3565628
Moreno-Rueda G (2003) Selección de cajas-nido por aves insectívoras en Sierra Nevada. Zool Baetica 13(14):131–138
Morgan PB (1980) Sustained releases of Spalangia endius walker (Hymenoptera: Pteromalidae) for the control of Musca domestica (L.) and Stomoxys calcitrans (L.) (Diptera: Muscidae). J Kans Entomol Soc 53:367–372
Niehuis O, Gibson JD, Rosenberg MS, Pannebakker BA, Koevoets T, Judson AK, Desjardins CA, Kennedy K, Duggan D, Beukeboom LW, van de Zande L, Shuker DM, Werren JH, Gadau J (2010) Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia. PLoS ONE 5:e8597. https://doi.org/10.1371/journal.pone.0008597
Oliva A (2008) Parasitoid wasps (Hymenoptera) from puparia of sarcosaprophagous flies (Diptera: Calliphoridae; Sarcophagidae) in Buenos Aires, Argentina. Rev Soc Entomológica Argent 67:139–141
Oliveira DCSG, Raychoudhury R, Lavrov DV, Werren JH (2008) Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Mol Biol Evol 25:2167–2180. https://doi.org/10.1093/molbev/msn159
Peters RS (2010) Host range and offspring quantities in natural populations of Nasonia vitripennis (Walker, 1836) (Hymenoptera: Chalcidoidea: Pteromalidae). J Hymenopt Res 19:128–138
Peters RS (2011) Two ways of finding a host: a specialist and a generalist parasitoid species (Hymenoptera: Chalcidoidea: Pteromalidae). Eur J Entomol 108:565–573. https://doi.org/10.14411/eje.2011.073
Peters RS, Abraham R (2010) The food web of parasitoid wasps and their non-phytophagous fly hosts in birds’ nests (Hymenoptera: Chalcidoidea, and Diptera: Cyclorrhapha). J Nat Hist 44:625–638. https://doi.org/10.1080/00222930903437317
Potti J (2008) Blowfly infestation at the nestling stage affects egg size in the pied flycatcher Ficedula hypoleuca. Acta Ornithol 43:76–82. https://doi.org/10.3161/000164508X345356
Potti J, Montalvo S (1990) Ocupación de áreas con nidales por el papamoscas cerrojillo (Ficedula hypoleuca). Ardeola 37:75–84
Poulin R (2011) The many roads to parasitism. In: Advances in Parasitology, 1st edn. Elsevier, London, pp 1–40
Poulin R, Randhawa HS (2015) Evolution of parasitism along convergent lines: from ecology to genomics. Parasitology 142:S6–S15. https://doi.org/10.1017/S0031182013001674
Puchala P (2004) Detrimental effects of larval blow flies (Protocalliphora azurea) on nestlings and breeding success of tree sparrows (Passer montanus). Can J Zool 82:1285–1290. https://doi.org/10.1139/z04-111
Quicke DLJ (1997) Parasitic wasps, 1st edn. Chapman & Hall, London, New York
Rivers DB (2004) Evaluation of host responses to envenomation as a means to assess ectoparasitic pteromalid wasp’s potential for controlling manure-breeding flies. Biol Control 30:181–192. https://doi.org/10.1016/j.biocontrol.2004.01.004
Rivers DB, Denlinger DL (1995) Fecundity and development of the ectoparasitic wasp Nasonia vitripennis are dependent on host quality. Entomol Exp Appl 76:15–24. https://doi.org/10.1111/j.1570-7458.1995.tb01942.x
Rodrigues-Guimarães R, Guimarães RR, de Carvalho RW et al (2006) Registro de Aphaereta laeviuscula (Spinola) (Hymenoptera: Braconidae) e Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) como parasitóide de Cochliomyia hominivorax (Coquerel) (Diptera: Calliphoridae), no estado do Rio de Janeiro. Neotrop Entomol 35:402–407. https://doi.org/10.1590/S1519-566X2006000300017
Rózsa L, Reiczigel J, Majoros G (2000) Quantifying parasites in samples of hosts. J Parasitol 86:228–232. https://doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2
Rutz DA, Axtell RC (1981) House fly (Musca domestica) control in broiler-breeder poultry houses by pupal parasites (Hymenoptera: Pteromalidae): indigenous parasite species and releases of Muscidifurax raptor. Environ Entomol 10:343–345. https://doi.org/10.1093/ee/10.3.343
Rutz DA, Scoles GA (1989) Occurrence and seasonal abundance of parasitoids attacking muscoid flies (Diptera: Muscidae) in caged-layer poultry facilities in New York. Environ Entomol 18:51–55. https://doi.org/10.1093/ee/18.1.51
Simon A, Thomas D, Blondel J, Perret P, Lambrechts MM (2004) Physiological ecology of Mediterranean blue tits (Parus caeruleus L.): effects of ectoparasites (Protocalliphora spp.) and food abundance on metabolic capacity of nestlings. Physiol Biochem Zool 77:492–501. https://doi.org/10.1086/383512
Simon A, Thomas DW, Speakman JR et al (2005) Impact of ectoparasitic blowfly larvae (Protocalliphora spp.) on the behavior and energetics of nestling blue tits. J Field Ornithol 76:402–410. https://doi.org/10.1648/0273-8570-76.4.402
Skovgård H, Jespersen JB (1999) Activity and relative abundance of hymenopterous parasitoids that attack puparia of Musca domestica and Stomoxys calcitrans (Diptera: Muscidae) on confined pig and cattle farms in Denmark. Bull Entomol Res 89:263–269. https://doi.org/10.1017/S0007485399000383
Skovgård H, Jespersen JB (2000) Seasonal and spatial activity of hymenopterous pupal parasitoids (Pteromalidae and Ichneumonidae) of the house fly (Diptera: Muscidae) on Danish pig and cattle farms. Environ Entomol 29:630–637. https://doi.org/10.1603/0046-225X-29.3.630
Skovgård H, Nachman G (2004) Biological control of house flies Musca domestica and stable flies Stomoxys calcitrans (Diptera: Muscidae) by means of inundative releases of Spalangia cameroni (Hymenoptera: Pteromalidae). Bull Entomol Res 94:555–567
Sorribas J, Rodríguez R, Garcia-Mari F (2010) Parasitoid competitive displacement and coexistence in citrus agroecosystems: linking species distribution with climate. Ecol Appl 20:1101–1113. https://doi.org/10.1890/09-1662.1
StatSoft Inc (2007) STATISTICA (data analysis software system). StatSoft, Inc.
Stiling PD (1987) The frequency of density dependence in insect host-parasitoid systems. Ecology 68:844–856
Streby HM, Peterson SM, Kapfer PM (2009) Fledging success is a poor indicator of the effects of bird blow flies on ovenbird survival. The Condor 111:193–197. https://doi.org/10.1525/cond.2009.080095
Sullivan DJ (2009) Hyperparasitism. In: Encyclopedia of Insects, 2nd edition. Academic Press / Elsevier Science, pp 486–488
Sullivan DJ, Völkl W (1999) Hyperparasitism: multitrophic ecology and behavior. Annu Rev Entomol 44:291–315. https://doi.org/10.1146/annurev.ento.44.1.291
Thomas K, Shutler D (2001) Ectoparasites, nestling growth, parental feeding rates, and begging intensity of tree swallows. Can J Zool 79:346–353. https://doi.org/10.1139/z00-206
Werren JH (1983) Sex ratio evolution under local mate competition in a parasitic wasp. Evolution 37:116. https://doi.org/10.2307/2408180
Werren JH, Loehlin DW (2009, 2009) The parasitoid wasp Nasonia: an emerging model system with haploid male genetics. Cold Spring Harb Protoc:pdb.emo134-pdb.emo134. https://doi.org/10.1101/pdb.emo134
Whiting AR (1967) The biology of the parasitic wasp Mormoniella vitripennis [= Nasonia brevicornis] (Walker). Q Rev Biol 42:333–406 https://www.jstor.org/stable/2818420
Whitworth TL, Bennett GF (1992) Pathogenicity of larval Protocalliphora (Diptera: Calliphoridae) parasitizing nestling birds. Can J Zool 70:2184–2191. https://doi.org/10.1139/z92-295
Wylie HG (1958) Factors that affect host finding by Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae). Can Entomol 90:597–608. doi. https://doi.org/10.4039/Ent90597-10
Wylie HG (1967) Some effects of host size on Nasonia vitripennis and Muscidifurax raptor (Hymenoptera: Pteromalidae). Can Entomol 99:742–748. https://doi.org/10.4039/Ent99742-7
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems: data exploration. Methods Ecol Evol 1:3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x
Acknowledgements
The study was supported by projects of Plan Nacional of the Spanish Ministerio de Economía y Competitividad (CGL2014-55969-P and CGL2017-84938-P), both financed with FEDER (E.U.) funds. We are grateful to Abelardo Requena Blanco, Nicola Bernardo, Mar Comas, Maribel P. Moreno, José Luis Ros Santaella, and Eliana Pintus for their collaboration in various aspects of fieldwork and also to David Nesbitt for his help improving the English. Comments by two anonymous referees improved the typescript.
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Garrido-Bautista, J., Moreno-Rueda, G., Baz, A. et al. Variation in parasitoidism of Protocalliphora azurea (Diptera: Calliphoridae) by Nasonia vitripennis (Hymenoptera: Pteromalidae) in Spain. Parasitol Res 119, 559–566 (2020). https://doi.org/10.1007/s00436-019-06553-x
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DOI: https://doi.org/10.1007/s00436-019-06553-x