Climate and seasonal effects on phenology and biological control of giant whitefly Aleurodicus dugesii (Hemiptera: Aleyrodidae) with parasitoids in southern California, USA

Abstract

The invasive giant whitefly Aleurodicus dugesii Cockerell (Hemiptera: Aleyrodidae), a pest of many important crops and ornamentals, has established throughout southern California, USA. The parasitoids Encarsia noyesi Hayat (Hymenoptera: Aphelinidae), Idioporous affinis LaSalle and Polaszek (Hymenoptera: Pteromalidae), and Entedononecremnus krauteri Zolnerowich and Rose (Hymenoptera: Eulophidae) were introduced as part of a classical biological control program against giant whitefly. Populations of giant whitefly can still reach high numbers, however, despite biological control efforts. Seasonal variation in giant whitefly population densities and parasitoids' species-specific parasitism rates across three climates types in southern California were examined by repeated censuses during 2015–2016 in order to identify potential underlying factors influencing giant whitefly population dynamics. Giant whitefly population densities did not vary between southern California climate types, but varied seasonally, with the highest observed population densities in the spring. Parasitism rates of all three parasitoids also varied seasonally, with total parasitism reaching a peak in late summer and declining until the start of spring. Only I. affinis parasitism rates varied between climate types. Parasitism rates of I. affinis were the highest of the three parasitoid species observed, followed by E. noyesi and E. krauteri. Potential explanations for these findings and their impact on giant whitefly control are discussed.

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References

  1. Amarasekare P (2007) Species coexistence in communities with intraguild predation: the roles of trade-offs and temporal variation. Ecology 88:2720–2728

    PubMed  Article  Google Scholar 

  2. Baffoe K, Dalin P, Nordlander PG, Stenberg JA (2012) Importance of temperature for the performance and biocontrol efficiency of the parasitoid Perilitus brevicollis (Hymenoptera: braconidae) on Salix. BioControl 57:611–618

    Article  Google Scholar 

  3. Bellows TS Jr., Kabashima JN, Robb KL. (2002). Giant Whitefly. University of California Agriculture and Natural Resources Publication 7400.

  4. Blumberg D (1991) Seasonal variations in the encapsulation of eggs of the encyrtid parasitoid Metaphycus stanleyi by the pyriform scale, Protopulvinaria pyriformis. Entomol Exp et Appl 58:231–237

    Article  Google Scholar 

  5. Blumberg D, DeBach P (1981) Effects of temperature and host age upon the encapsulation of Metaphycus stanleyi and Metaphycus helvolus eggs by brown soft scale Coccus hesperidium. J Invertebr Pathol 37:73–79

    Article  Google Scholar 

  6. Boughton AJ, Mendez MA, Francis AW, Smith TR, Osborne LS, Mannion CM (2015) Host stage suitability and impact of Encarsia noyesi (Hymenoptera: Aphelinidae) on the invasive rugose spiraling whitefly, Aleurodicus rugioperculatus (Hemiptera: Aleyrodidae), in Florida. Biol Control 88:61–67

    Article  Google Scholar 

  7. Bourchier RS, Smith SM (1996) Influence of environmental conditions and parasitoid quality on field performance of Trichogramma minutum. Entomol Exp Appl 80:461–468

    Article  Google Scholar 

  8. Briggs CJ, Latto J (1996) The window of vulnerability and its effect on relative parasitoid abundance. Ecol Entomol 21:128–140

    Article  Google Scholar 

  9. Campbell A, Frazer BD, Gilbert N, Gutierrez AP, Mackauer M (1974) Temperature requirements of some aphids and their parasites. J Appl Ecol 11:431–438

    Article  Google Scholar 

  10. Cherry RH (1979) Temperature tolerance of three whitefly species found in Florida. Environ Entomol 8:1150–1152

    Article  Google Scholar 

  11. Cock MJW, Murphy ST, Kairo MTK, Thompson E, Murphy RJ, Francis AW (2016) Trends in the classical biological control of insect pests by insects: an update of the BIOCAT database. BioControl 61:349–363

    CAS  Article  Google Scholar 

  12. Crozier L (2004) Warmer winters drive butterfly range expansion by increasing survivorship. Ecology 85:231–241

    Article  Google Scholar 

  13. Cui X, Wan F, Xie M, Liu T (2008) Effects of heat shock on survival and reproduction of two whitefly species, Trialeurodes vaporariorum and Bemisia tabaci biotype B. J insect Sci 8:24

    PubMed Central  Article  Google Scholar 

  14. Curnutte LB, Simmons AM, Abd-Rabou S (2014) Climate change and Bemisia tabaci (Hemiptera: Aleyrodidae): impacts of temperature and carbon dioxide on life history. Ann Entomol Soc Am 107:933–943

    Article  Google Scholar 

  15. DeBach P, Fisher TW, Landi J (1955) Some effects of meteorological factors on all stages of Aphytis lingnanensis, a parasite of the California red scale. Ecology 36:743–753

    Article  Google Scholar 

  16. DeBach P, Hagen KS (1964) Manipulation of entomophagous species. In: DeBach P (ed) Biological control of insect pests and weeds. Chapman and Hall, London, pp 429–458

    Google Scholar 

  17. DeBach P, Hendrickson RM, Rose M (1978) Competitive displacement: extinction of the yellow scale, Aonidiella citrina (Coq.) (Homoptera: Diaspididae), by its ecological homologue, the California red scale, Aonidiella aurantii (Mask.) in southern California. Hilgardia 46:1–35

    Article  Google Scholar 

  18. Ehler LE, Hall RW (1982) Evidence for competitive exclusion of introduced natural enemies in biological control. Environ Entomol 11:1–4

    Article  Google Scholar 

  19. Evans GA. (2008). The whiteflies (Hemiptera: Aleyrodidae) of the world and their host plants and natural enemies. https://keys.lucidcentral.org/keys/v3/whitefly/PDF_PwP%20ETC/world-whitefly-catalog-Evans.pdf. Accessed June 2020

  20. Fellowes MDE, Kraaijeveld AR, Godfray HCJ (1999) Cross-resistance following artificial selection for increased defense against parasitoids in Drosophila melanogaster. Evolution 53:966–972

    CAS  PubMed  Article  Google Scholar 

  21. Godfray HCJ, Hassell MP, Holt RD (1994) The population dynamic consequences of phenological asynchrony between parasitoids and their hosts. J Anim Ecol 63:1–10

    Article  Google Scholar 

  22. Hågvar EB (1991) Ecological problems in the establishment of introduced predators and parasites for biological control. Acta Entomol Bohemoslov 88:1–11

    Google Scholar 

  23. Hance T, van Baaren J, Vernon P, Boivin G (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Ann Rev Entomol 52:107–126

    CAS  Article  Google Scholar 

  24. Hassell MP (2000) The spatial and temporal dynamics of host–parasitoid interactions. Oxford University Press, Oxford

    Google Scholar 

  25. Hodges G. (2004). Giant whitefly, Aleurodicus dugesii Cockerell, in Florida. Pest Alert, Division of Plant Industry, Florida Department of Agricultural and Consumer Services. https://www.freshfromflorida.com/content/download/68178/1612763/Pest_Alert_-_Aleurodicus_ dugesii,_Giant_whitefly.pdf. Accessed March 2019

  26. Hoelmer KA, Kirk AA (2005) Selecting arthropod biological control agents against arthropod pests: can the science be improved to decrease the risk of releasing ineffective agents? Biol Control 34:255–264

    Article  Google Scholar 

  27. Jalali SK, Venkatesan T, Murthy KS, Biswas SR, Lalitha Y (2005) Influence of temperature and host density on functional response of Telenomus remus Nixon, an egg parasitoid of Spodoptera litura Fabricius. Entomon 30:193–199

    Google Scholar 

  28. Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    PubMed  Article  Google Scholar 

  29. Karban R (1998) Caterpillar basking behavior and nonlethal parasitism by tachinid flies. J Insect Behav 11:713–723

    Article  Google Scholar 

  30. Karl TR, Trenbeth KE (2003) Modern global climate change. Science 302:1719–1723

    CAS  PubMed  Article  Google Scholar 

  31. Kenward MG, Roger JH (2009) An improved approximation to the precision of fixed effects from restricted maximum likelihood. Comput Stat Data Anal 53:2583–2595

    Article  Google Scholar 

  32. Kiritani K (2006) Predicting impacts of global warming on population dynamics and distribution of arthropods in Japan. Popul Ecol 48:5–12

    Article  Google Scholar 

  33. Lebrun EG, Plowes RM, Gilbert LE (2009) Indirect competition facilitates widespread displacement of one naturalized parasitoid of imported fire ants by another. Ecology 90:1184–1194

    CAS  PubMed  Article  Google Scholar 

  34. Mason PG, Hopper KR (1997) Temperature dependence in locomotion of the parasitoid Aphelinus asychis (Hymenoptera: Aphelinidae) from geographical regions with different climates. Environ Entomol 26:1416–1423

    Article  Google Scholar 

  35. Naranjo SE, Ellsworth PC, Frisvold GB (2015) Economic value of biological control in integrated pest management of managed plant systems. Annu Rev Entomol 60:621–645

    CAS  PubMed  Article  Google Scholar 

  36. Price PW (1987) The role of natural enemies in insect populations. In: Barbosa P, Schultz JC (eds) Insect outbreaks. Academic Press, San Diego, pp 287–312

    Google Scholar 

  37. Rochat J, Gutierrez AP (2001) Weather-mediated regulation of olive scale by two parasitoids. J Anim Ecol 70:476–490

    Article  Google Scholar 

  38. Romo CM, Tylianakis JM (2013) Elevated temperature and drought interact to reduce parasitoid effectiveness in suppressing hosts. PLoS ONE 8(3):e58136

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. SAS Institute Inc (2011) SAS/STAT User’s Guide. Version 9.4, SAS Institute, Inc., Cary, NC

  40. Schoeller EN, Redak RA (2018a) Host stage preferences of Encarsia noyesi, Idioporus affinis, and Entedononecremnus krauteri: parasitoids of the giant whitefly Aleurodicus dugesii (Hemiptera: Aleyrodidae). Environ Entomol 47:1493–1500

    PubMed  Google Scholar 

  41. Schoeller EN, Redak RA (2018b) Temperature-dependent development and survival of giant whitefly Aleurodicus dugesii (Hemiptera: Aleyrodidae) under constant temperatures. Environ Entomol 47:1586–1595

    PubMed  Google Scholar 

  42. Simberloff D (2012) Risks of biological control for conservation purposes. BioControl 57:263–276

    Article  Google Scholar 

  43. Sorribas J, Rodriguez R, Garcia-Marí F (2010) Parasitoid competitive displacement and coexistence in citrus agroecosystems: linking species distribution with climate. Ecol Appl 20:1101–1113

    PubMed  Article  Google Scholar 

  44. Stiling P (1990) Calculating the establishment rates of parasitoids in classical biological control. Am Entomol 36:225–230

    Article  Google Scholar 

  45. Stiling P (1993) Why do natural enemies fail in classical biological control programs? Am Entomol 39:31–37

    Article  Google Scholar 

  46. Thomson LJ, Macfadyen S, Hoffmann AA (2010) Predicting the effects of climate change on natural enemies of agricultural pests. Biol Control 52:296–306

    Article  Google Scholar 

  47. Turnbull AL, Chant PA (1961) The practice and theory of biological control of insects in Canada. Can J Zool 89:697–753

    Article  Google Scholar 

  48. van Baaren J, Outreman Y, Boivin G (2005) Effect of low temperature exposure on oviposition behavior and patch exploitation strategy in parasitic wasps. Anim Behav 70:153–163

    Article  Google Scholar 

  49. van Nouhuys S, Lei G (2004) Parasitoid-host metapopulation dynamics: the causes and consequences of phenological asynchrony. J Anim Ecol 73:526–535

    Article  Google Scholar 

  50. Voigt W, Perner J, Davis AJ, Eggers T, Schumacher J, Bährmann R, Fabian B, Heinrich W, Köhler G, Lichter D, Marstaller R, Sander FW (2003) Trophic levels are differentially sensitive to climate. Ecology 84:2444–2453

    Article  Google Scholar 

  51. Wetherington MT, Jennings DE, Shrewsbury PM, Duan JJ (2017) Climate variation alters the synchrony of host–parasitoid interactions. Ecol Evol 7:8578–8587

    PubMed  PubMed Central  Article  Google Scholar 

  52. Wu GM, Barrette M, Boivin G, Brodeur J, Giraldeau LA, Hance T (2011) Temperature influences the handling efficiency of an aphid parasitoid through body size-mediated effects. Environ Entomol 40:737–742

    PubMed  Article  Google Scholar 

  53. Zolnerowich G, Rose M (1996) A new species of Entedononecremnus (Hymenoptera: Chalcidoidea: Eulophidae) parasitic on the giant whitefly, Aleurodicus dugesii Cockerell (Homoptera: Aleyrodidae). P Entomol Soc Wash 98:369–373

    Google Scholar 

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Acknowledgements

We are grateful the property owners who allowed us access to collect insects throughout the year. Funding for this research was provided by the United States Department of Agriculture (NIFA 2016-67011-25164), Robert and Peggy van den Bosch Memorial Scholarship, and California Association of Nurseries and Garden Centers.

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Correspondence to Erich N. Schoeller.

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Schoeller, E.N., Redak, R.A. Climate and seasonal effects on phenology and biological control of giant whitefly Aleurodicus dugesii (Hemiptera: Aleyrodidae) with parasitoids in southern California, USA. BioControl (2020). https://doi.org/10.1007/s10526-020-10029-8

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Keywords

  • Parasitoids
  • Whitefly
  • Phenology
  • Biological control