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Potential exposure of a classical biological control agent of the soybean aphid, Aphis glycines, on non-target aphids in North America

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Abstract

In summer 2007, the Asian parasitoid Binodoxys communis (Hymenoptera: Braconidae) was released in North America for control of the exotic soybean aphid, Aphis glycines (Hemiptera: Aphididae). Despite its comparatively narrow host range, releases of B. communis may still constitute a risk to native aphid species. To estimate the risk of exposure of non-target aphids to B. communis, we merged assessments of temporal co-occurrence with projections of spatial overlap between B. communis and three native aphid species, and in-field measurements of the incidence of ecological filters that may protect these aphids from parasitism. Temporal co-occurrence was assessed between A. glycines and native aphids (Aphis asclepiadis, Aphis oestlundi, and Aphis monardae) at four different locations in Minnesota, USA. The degree of temporal overlap depended greatly on location and aphid species, ranging between 0 and 100%. All of the native aphids were tended by multiple species of ants, with overall ant-attendance ranging from 26.1 to 89.6%. During temporal overlap with A. glycines, 53 ± 11% of A. monardae colonies were partly found in flower heads of their host plant, with flowers acting as a physical refuge for this aphid. The extent of geographic overlap between B. communis and native aphids based upon Climex modeling was 17–28% for A. monardae, 13–22% for A. oestlundi, 46–55% for A. asclepiadis and 12–24% for the A. asclepiadis species complex. The estimated overall probability of potential exposure of B. communis on native aphids was relatively low (P = 0.115) for A. oestlundi and high (P = 0.550) for A. asclepiades. Physical and ant-mediated refuges considerably lowered probability of population-level impact on A. monardae, and could lead to substantial reduction of exposure for the other native aphids. These findings are used to make broader statements regarding the ecological safety of current B. communis releases and their potential impact on native aphid species in North America.

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References

  • Addicott JF (1981) Synonymy of Aphis heraclella Davis 1919 with Aphis helianthi Monell 1879 (Homoptera: Aphididae). Can Entomol 113:167–169

    Article  Google Scholar 

  • Allen CR, Johnson AR, Parris L (2006) A framework for spatial risk assessments: potential impacts of non-indigenous invasive species on native species. Ecol Soc 11:39

    Google Scholar 

  • Anderson RP, Martinez-Meyer E (2004) Modeling species’ geographic distributions for preliminary conservation assessments: an implementation with the spiny pocket mice (Heteromys) of Ecuador. Biol Conserv 116:167–179. doi:10.1016/S0006-3207(03)00187-3

    Article  Google Scholar 

  • Andow DA, Lane CP, Olson DM (1995) Use of Trichogramma in maize—estimating environmental risks. In: Hokkanen HMT, Lynch JM (eds) Biological control: benefits and risks. Press Syndicate of the University of Cambridge, Cambridge, pp 101–118

    Google Scholar 

  • Babendreier D, Schoch D, Kuske S, Dorn S, Bigler F (2003) Non-target habitat exploitation by Trichogramma brassicae (Hymenoptera: Trichogrammatidae): what are the risks for endemic butterflies. Agric For Entomol 5:199–208. doi:10.1046/j.1461-9563.2003.00180.x

    Article  Google Scholar 

  • Babendreier D, Bigler F, Kuhlmann U (2005) Methods used to assess non-target effects of invertebrate biological control agents of arthropod pests. Biocontrol 50:821–870. doi:10.1007/s10526-005-3633-3

    Article  Google Scholar 

  • Barlow ND, Barratt BIP, Ferguson CM, Barron MC (2004) Using models to estimate parasitoid impacts on non-target host abundance. Environ Entomol 33:941–948

    Google Scholar 

  • Barratt BIP, Ferguson CM, Evans AA, McNeil MR, Addison PJ (2000) Phenology of native weevils (Coleoptera: Curculionidae) in New Zealand pastures and parasitism by the introduced braconid, Microctonus aethiopiodes Loan (Hymenoptera: Braconidae). NZ J Zool 27:93–110

    Google Scholar 

  • Bigler F, Babendreier D, Kuhlmann U (eds) (2006) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI Publishing, Switzerland

    Google Scholar 

  • Bigler F, Kolliker-Ott UM (2006) Balancing environmental risks and benefits: a basic approach. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, Oxon, UK, pp 273–286

    Google Scholar 

  • Brodeur J, Rosenheim JA (2000) Intraguild interactions in aphid parasitoids. Entomol Exp Appl 97:93–108. doi:10.1023/A:1004013232410

    Article  Google Scholar 

  • Bryne MJ, Currin S, Hill MP (2002) The influence of climate on the establishment and success of the biocontrol agent Gratiana spadicea, released on Solanum sisymbriifolium in South Africa. Biol Control 24:128–134. doi:10.1016/S1049-9644(02)00021-X

    Article  Google Scholar 

  • Chacon J, Landis DA, Heimpel GE. Potential for biotic interference of a classical biological control agent of the soybean aphid. Biol Control (in press)

  • Cook EF (1984) Aphis (Homoptera: Aphididae) recorded from Compositae in North America, with a key to the species east of the Rocky Mountains and comments on synonymy and re-descriptions of some little known forms. Ann Entomol Soc Am 77:442–449

    Google Scholar 

  • Crawley MJ (1986) The population biology of invaders. Philos T Roy Soc B 314:711–731. doi:10.1098/rstb.1986.0082

    Article  Google Scholar 

  • Doutt RL, Annecke DP, Tremblay E (1976) Biology and host relationships of parasitoids. In: Huffaker CB, Messenger PS (eds) Theory and practice of biological control. Academic Press, New York, pp 143–168

    Google Scholar 

  • Drake JM, Lodge DM (2006) Forecasting potential distributions of non-indigenous species with a genetic algorithm. Fisheries 31:9–16. doi:10.1577/1548-8446(2006)31[9:FPDONS]2.0.CO;2

    Article  Google Scholar 

  • Dunlop EA, Wilson JC, Mackey AP (2006) The potential geographic distribution of the invasive weed Senna obtusifolia in Australia. Weed Res 46:404–413. doi:10.1111/j.1365-3180.2006.00524.x

    Article  Google Scholar 

  • Dzialowski AR, Lennon JT, Smith VH (2007) Food web structure provides biotic resistance against plankton invasion attempts. Biol Invasions 9:257–267. doi:10.1007/s10530-006-9030-8

    Article  Google Scholar 

  • Essig EO (1917) Aphididae of California. Calif Pub 1:301–346

    Google Scholar 

  • Fiaboe KKM, Fonseca RL, de Moraes GJ, Ogol CKPO, Knapp M (2006) Identification of priority areas in South America for exploration of natural enemies for classical biological control of Tetranychus evansi (Acari: Tetranychidae) in Africa. Biol Control 38:373–379. doi:10.1016/j.biocontrol.2006.05.011

    Article  Google Scholar 

  • Follett PA, Duan JJ (eds) (2000) Non-target effects of biological control. Kluwer Academic Publishers, Norwell

    Google Scholar 

  • Follett PA, Duan J, Messing RH, Jones VP (2000) Parasitoid drift after biological control introductions: re-examining Pandora’s box. Am Entomol 46:82–94

    Google Scholar 

  • Gillette CP, Palmer MA (1932) The Aphididae of Colorado. Ann Entomol Soc Am 2:369–496

    Google Scholar 

  • Goolsby JA, DeBarro PJ, Kirk AA, Sutherst RW, Cañas L, Ciomperlik MA, Ellsworth PC, Gould JR, Hartley DM, Hoelmer KA, Naranjo SE, Rose M, Roltsch WJ, Ruiz RA, Pickett CH, Vacek DC (2005) Post-release evaluation of biological control of Bemisia tabaci biotype “B” in the USA and the development of predictive tools to guide introduction for other countries. Biol Control 32:70–77. doi:10.1016/j.biocontrol.2004.07.012

    Article  Google Scholar 

  • Hart AJ, Bale JS, Tullett AG, Worland MR, Walters KFA (2002) Effects of temperature on the establishment potential in the UK of the non-native glasshouse biocontrol agent Macrolophus caliginosus. Physiol Entomol 27:112–123. doi:10.1046/j.1365-3032.2002.00276.x

    Article  Google Scholar 

  • Heimpel GE, Ragsdale DW, Venette RC, Hopper KR, O’Neil RJ, Rutledge CE, Wu Z (2004) Prospects for importation biological control of the soybean aphid: anticipating potential costs and benefits. Ann Entomol Soc Am 97:249–258. doi:10.1603/0013-8746(2004)097[0249:PFIBCO]2.0.CO;2

    Article  Google Scholar 

  • Heraty J, Hawks D (1998) Hexamethyldisilazane—a chemical alternative for drying insects. Entomol News 109:369–374

    Google Scholar 

  • 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. doi:10.1016/j.biocontrol.2005.05.001

    Article  Google Scholar 

  • Hopper KR (2001) Research needs concerning non-target impacts of biological control introductions. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating the indirect ecological effects of biological control. CABI Publishing, Wallingford, pp 39–56

    Google Scholar 

  • Hubner G (2000) Differential interactions between an aphid endohyperparasitoid and three honeydew collecting ant species: a field study of Alloxysta brevis (Thomson) (Hymenoptera: Alloxystidae). J Insect Behav 13:771–784. doi:10.1023/A:1007856330094

    Article  Google Scholar 

  • Jewel JJ, O’Dowd DJ, Bergelson J et al (1999) Deliberate introductions of species: research needs—benefits can be reaped, but risks are high. Bioscience 49:619–630. doi:10.2307/1313438

    Article  Google Scholar 

  • Kaneko S (2003) Different impacts of two species of aphid-attending ants with different aggressiveness on the number of emerging adults of the aphid’s primary parasitoid and hyperparastioids. Ecol Res 18:199–212. doi:10.1046/j.1440-1703.2003.00547.x

    Article  Google Scholar 

  • Kimberling DN (2004) Lessons from history: predicting successes and risks of intentional introductions for arthropod biological control. Biol Invasions 6:301–318. doi:10.1023/B:BINV.0000034599.09281.58

    Article  Google Scholar 

  • Kuske S, Babendreier D, Edwards PJ, Turlings TCJ, Bigler F (2004) Parasitism of non-target Lepidoptera by mass-released Trichogramma brassicae and its implication for the larval parasitoid Lydella thomposoni. Biocontrol 49:1–19. doi:10.1023/B:BICO.0000009379.13685.47

    Article  Google Scholar 

  • Levine JM, D’Antonio CM (1999) Elton revisited: a review of evidence linking diversity and invasibility. Oikos 87:15–26. doi:10.2307/3546992

    Article  Google Scholar 

  • Liepert C, Dettner K (1996) Role of cuticular hydrocarbons of aphid parasitoids in their relationship to aphid attending ants. J Chem Ecol 22:695–707. doi:10.1007/BF02033579

    Article  CAS  Google Scholar 

  • Louda SM, Pemberton RW, Johnson MT, Follett PA (2003) Nontarget effects—the Achilles’ heel of biological control? Retrospective analysis to reduce risk associated with biocontrol introductions. Annu Rev Entomol 48:365–396. doi:10.1146/annurev.ento.48.060402.102800

    Article  PubMed  CAS  Google Scholar 

  • Messing RH, Wright MG (2006) Biological control of invasive species: solution or pollution? Front Ecol Evol 4:132–140. doi:10.1890/1540-9295(2006)004[0132:BCOISS]2.0.CO;2

    Article  Google Scholar 

  • Messing R, Roitberg B, Brodeur J (2006) Measuring and predicting indirect impacts of biological control: competition, displacement and secondary interactions. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control. CABI Publishing, Wallingford, pp 64–77

    Google Scholar 

  • Miller TE, Kneitel JM, Burns JH (2002) Effects of community structure on invasion success and rate. Ecology 83:898–905

    Article  Google Scholar 

  • Mortimer DL, Tissot AN (1965) A preliminary list of Texas aphids. Fla Entomol 48:255–264. doi:10.2307/3493778

    Article  Google Scholar 

  • Murdoch WW, Chesson J, Chesson PL (1985) Biological control theory and practice. Am Nat 125:344–366. doi:10.1086/284347

    Article  Google Scholar 

  • NAPIS (2006) National Agricultural Pest Information System. http://ceris.purdue.edu Cited 12 March 2007

  • Nechols JR, Kauffman WC, Schaefer PW (1992) Significance of host specificity in classical biological control. In: Kauffmann WC, Nechols JE (eds) Selection criteria and ecological consequences of importing natural enemies. Thomas Say Publications in Entomology, Lanham, pp 41–52

    Google Scholar 

  • New M, Hulme M, Jones P (1999) Representing twentieth century space-time climate variability. Part I: development of a 1961–90 mean monthly terrestrial climatology. J Clim 12:829–856. doi:10.1175/1520-0442(1999)012<0829:RTCSTC>2.0.CO;2

    Google Scholar 

  • Palmer MA (1952) Aphids of the Rocky Mountain region. The Thomas Say Foundation, vol 5. The A.B. Hirschfeld Press, Denver

    Google Scholar 

  • Pearson DE, Callaway RM (2005) Indirect nontarget effects of host-specific biological control agents: implications for biological control. Biol Control 35:288–298. doi:10.1016/j.biocontrol.2005.05.011

    Article  Google Scholar 

  • Pemberton RW (2000) Predictable risk to native plants in weed biological control. Oecologia 125:489–494. doi:10.1007/s004420000477

    Article  Google Scholar 

  • Peterson AT (2001) Predicting species geographic distribution based on ecological niche modeling. Bioscience 51:363–371. doi:10.1641/0006-3568(2001)051[0363:PSIUEN]2.0.CO;2

    Article  Google Scholar 

  • Phillips SJ, Dudik M, Schapire RE (2004) A maximum entropy approach to species distribution modeling. In: Proceedings of the 21st international conference of machine learning, Banff, July 2004

  • PLANTS Database (2007) USDA, Natural Resource Conservation Service. http://plants.usda.gov. Cited 13 Dec 2007

  • Ragsdale DW, McCornack BP, Venette RC, Potter BD, MacRae IV, Hodgson EW, O’Neal ME, Johnson KD, O’Neil RJ, DiFonzo CD, Hunt TE, Glogoza PA, Cullen EM (2007) Economic threshold for soybean aphid (Hemiptera: Aphididae). J Econ Entomol 100:1258–1267. doi:10.1603/0022-0493(2007)100[1258:ETFSAH]2.0.CO;2

    Article  PubMed  CAS  Google Scholar 

  • Ragsdale DW, Voegtlin DJ, O’Neil RJ (2004) Soybean aphid biology in North America. Ann Entomol Soc Am 97:204–208. doi:10.1603/0013-8746(2004)097[0204:SABINA]2.0.CO;2

    Article  Google Scholar 

  • Rand TA, Louda SA (2006) Spillover of agriculturally subsidized predators as a potential threat to native insect herbivores in fragmented landscapes. Conserv Biol 20:1720–1729. doi:10.1111/j.1523-1739.2006.00507.x

    Article  PubMed  Google Scholar 

  • Rand TA, Tylianakis JM, Tscharntke T (2006) Spillover edge effects: the dispersal of agriculturally subsidized insect natural enemies into adjacent natural habitats. Ecol Lett 9:603–614. doi:10.1111/j.1461-0248.2006.00911.x

    Article  PubMed  Google Scholar 

  • Renault CK, Buffa LM, Delfino MA (2005) An aphid-ant interaction: effects on different trophic levels. Ecol Res 20:71–74. doi:10.1007/s11284-004-0015-8

    Article  Google Scholar 

  • Rojanavongse V, Robinson AG (1977) Aphids of manitoba. Can Entomol 109:649–661

    Google Scholar 

  • Schoener TW, Spiller DA (1995) Effects of predators and area on invasions: an experiment with spiders. Science 267:1811–1813. doi:10.1126/science.267.5205.1811

    Article  PubMed  CAS  Google Scholar 

  • Schreiner IH, Nafus DM (1992) Changes in a moth community mediated by biological control of the dominant species. Environ Entomol 21:664–668

    Google Scholar 

  • Secord D, Kareiva P (1996) Perils and pitfalls in the host specificity paradigm. Bioscience 46:448–453. doi:10.2307/1312879

    Article  Google Scholar 

  • Simberloff D, Stiling P (1996) How risky is biological control. Ecology 77:1965–1974. doi:10.2307/2265693

    Article  Google Scholar 

  • Stary P (1966) Aphid parasites (Hymenoptera: Aphididae) and their relationship to aphid attending ants, with respect to biological control. Insect Soc 13:185–202. doi:10.1007/BF02223024

    Article  Google Scholar 

  • Stockman AK, Beamer DA, Bond JE (2006) An evaluation of a GARP model as an approach to predicting the spatial distribution of non-vagile invertebrate species. Divers Distrib 12:81–89. doi:10.1111/j.1366-9516.2006.00225.x

    Article  Google Scholar 

  • Stockwell DRB, Peters DP (1999) The GARP modeling system: problems and solutions to automated spatial prediction. Int J Geogr Inf Sci 13:143–158. doi:10.1080/136588199241391

    Article  Google Scholar 

  • Stockwell DRB, Peterson AT (2002) Effects of sample size on accuracy of species distribution models. Ecol Modell 148:1–13. doi:10.1016/S0304-3800(01)00388-X

    Article  Google Scholar 

  • Strong DR, Pemberton RW (2001) Food webs, risk of natural enemies and reform of biological control. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects in biological control. CAB International, Wallingford, pp 57–79

    Google Scholar 

  • Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc B 274:151–164

    Article  PubMed  Google Scholar 

  • Sutherst RW, Maywald GF, Bottomley W, Bourne A (2004) CLIMEX v 2. user’s guide. CSIRO Publishing, Collingwood

    Google Scholar 

  • US EPA (1998) Guidelines for ecological risk assessment. Science Advisory Board, Washington, D.C., USA

    Google Scholar 

  • Van Driesche RG, Reardon R (eds) (2004) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. U.S. Department of Agriculture Forest Health Technology Enterprise Team, Morgantown

    Google Scholar 

  • van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM (2006) Assessing risk of releasing exotic biological control agents of arthropod pests. Annu Rev Entomol 51:609–634. doi:10.1146/annurev.ento.51.110104.151129

    Article  PubMed  CAS  Google Scholar 

  • Venette RC, Ragsdale DW (2004) Assessing the invasion by soybean aphid (Homoptera: Aphididae): where will it end? Ann Entomol Soc Am 97:219–226. doi:10.1603/0013-8746(2004)097[0219:ATIBSA]2.0.CO;2

    Article  Google Scholar 

  • Völkl W, Novak H (1997) Foraging behaviour and resource utilization of the aphid parasitoid, Pauesia pini (Hymenoptera: Aphidiidae) on spruce: influence of host species and ant attendance. Eur J Entomol 94:211–220

    Google Scholar 

  • Wajnberg E, Scott JK, Quimby PC (eds) (2001) Evaluating indirect effects of biological control. CAB International, Wallingford

    Google Scholar 

  • Williams TA (1910) The Aphididae of Nebraska. The University of Nebraska, University Studies 10

  • Willis AJ, Memmott J (2005) The potential for indirect effects between a weed, one of its biocontrol agents and native herbivores: a food web approach. Biol Control 35:299–306. doi:10.1016/j.biocontrol.2005.07.013

    Article  Google Scholar 

  • Wright MG, Hoffmann MP, Kuhar TP, Gardner J, Pitcher SA (2005) Evaluating risks of biological control introductions: a probabilistic risk-assessment approach. Biol Control 35:338–347. doi:10.1016/j.biocontrol.2005.02.002

    Article  Google Scholar 

  • Wyckhuys KAG, Heimpel GE (2007) Response of the soybean aphid parasitoid Binodoxys communis (Gahan) (Hymenoptera: Braconidae) to olfactory cues from target and non-target host-plant complexes. Entomol Exp Appl 123:149–158. doi:10.1111/j.1570-7458.2007.00532.x

    Article  Google Scholar 

  • Wyckhuys KAG, Hopper KR, Wu K, Straub C, Gratton G, Heimpel GE (2007a) Predicting potential ecological impact of soybean aphid biological control introductions. Biocontrol News Inf 28(2):30N–34N

    Google Scholar 

  • Wyckhuys KAG, Koch RL, Heimpel GE (2007b) Physical and ant-mediated refuges from parasitism: implications for non-target effects in biological control. Biol Control 40:306–313. doi:10.1016/j.biocontrol.2006.11.010

    Article  Google Scholar 

  • Wyckhuys KAG, Stone L, Desneux N et al. (2008a) Parasitism of the soybean aphid Aphis glycines by Binodoxys communis: the role of aphid defensive behavior and parasitoid reproductive performance. Bull Entomol Res (in press)

  • Wyckhuys KAG, Strange-George JE, Kulhanek CA, Wäckers FL, Heimpel GE (2008b) Comparing floral nectar and aphid honeydew diets on longevity, carbohydrate profiles and nutrient levels of Binodoxys communis, a parasitoid of the soybean aphid. J Insect Physiol 54:481–491

    Article  PubMed  CAS  Google Scholar 

  • Yu DS, van Achterberg K, Horstmann K (2005) World Ichneumonoidea. CD-ROM Taxapad

  • Zoebelein G (1956) Der Honingtau als Nahrung der Insekten. Z Angew Entomol 38:369–416

    Google Scholar 

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Acknowledgements

This paper is dedicated to Robert J. O’Neil, a pioneer in the field of biological control and source of inspiration to many, who passed away in Feb. 2008. We would like to thank Norbert Brotz and Jeremy Chacon for help with field research. We are grateful to Susana Acheampong, Nicolas Desneux and Wang LiMin for providing unpublished data. This work benefited greatly from technical assistance by Robert Venette (US Forest Service). The help of David Voegtlin and James C. Trager in identifying the respective aphid and ant species was invaluable. We are also grateful to Bob Djupstrom, Ellen Fuge and the Minnesota DNR, Scientific and Natural Areas Program for their granting permission to conduct research in Minnesota prairie sites. Lastly, we would like to thank Jeffrey Corney and John Haarstad at the Cedar Creek Natural History Area for their assistance in selecting appropriate field sites. This work was funded in part by the multi-state USDA-RAMP project, in part by the North Central Soybean Research Council, and in part by the Minnesota Agricultural Experiment Station.

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  1. Horticulture Research Center (CIAA), Universidad Jorge Tadeo Lozano, Carretera Central del Norte, 3 kms adelante de la Caro, A.A. 140196, Chia (Cundinamarca), Colombia

    Kris A. G. Wyckhuys

  2. Plant Protection Division, Minnesota Department of Agriculture, St. Paul, MN, USA

    Robert L. Koch

  3. Systematic Entomology Laboratory, Smithsonian Institution, Washington, DC, USA

    Robert R. Kula

  4. Department of Entomology, University of Minnesota, St. Paul, MN, USA

    George E. Heimpel

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Wyckhuys, K.A.G., Koch, R.L., Kula, R.R. et al. Potential exposure of a classical biological control agent of the soybean aphid, Aphis glycines, on non-target aphids in North America. Biol Invasions 11, 857–871 (2009). https://doi.org/10.1007/s10530-008-9299-x

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