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Antipredator response of pea aphids Acyrthosiphon pisum (Hemiptera: Aphididae): effects of predation risks from an alternative patch on a current patch

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Abstract

To escape from predators, herbivorous prey could leave their current patch and relocate to an alternative patch. However, when other predators are present on the new patch, prey are again exposed to predation risk. Thus, patch leaving might be affected by the other predators. We studied patch leaving of pea aphids Acyrthosiphon pisum Harris (Hemiptera: Aphididae) in response to ladybird larvae Harmonia axyridis Pallas (Coleoptera: Coccinellidae) on broad bean Vicia faba L. shoots that were offered as patches for aphids. We tested whether shoot leaving was affected by the presence of predators on alternative shoots under laboratory conditions. Odors from alternative shoots were evaluated as possible cues used by aphids to assess predation risk on the shoots. We exposed aphids to odors from alternative shoots with conspecifics plus either adult or larval ladybirds or larval green lacewings Mallada desjardinsi Navas (Neuroptera: Chrysopidae). Shoot leaving was reduced only when adult ladybirds were present on the alternative shoots compared with controls (i.e., no predators on the alternative shoots). Odors of both adult ladybirds and of conspecifics being attacked by ladybird larvae were required for reduced leaving. Hence, predation risks on current and alternative patches might affect the antipredator responses of aphids.

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References

  • Agarwala BK, Yasuda H, Kajita Y (2003) Effect of conspecific and heterospecific feces on foraging and oviposition of two predatory ladybirds: role of fecal cues in predator avoidance. J Chem Ecol 29:357–376

    CAS  PubMed  Google Scholar 

  • Braendle C, Weisser WW (2001) Variation in escape behavior of red and green clones of the pea aphid. J Insect Behav 14:497–509

    Google Scholar 

  • Canard M (2001) Natural food and feeding habits of lacewings. In: McEwen P, New TR, Whittington AE (eds) Lacewings in the crop environment. Cambridge University Press, Cambridge, pp 116–129

    Google Scholar 

  • Choh Y, Takabayashi J (2007) Predator avoidance in phytophagous mites: response to present danger depends on alternative host quality. Oecologia 151:262–267

    PubMed  Google Scholar 

  • Choh Y, Takabayashi J (2010) Predator avoidance by phytophagous mites is affected by the presence of herbivores in a neighboring patch. J Chem Ecol 36:614–619

    CAS  PubMed  Google Scholar 

  • Clegg JM, Barlow CA (1982) Escape behaviour of the pea aphid Acyrthosiphon pisum (Harris) in response to alarm pheromone and vibration. Can J Zool 60:2245–2252

    Google Scholar 

  • Dielenberg RA, McGregor IS (2001) Defensive behavior in rats towards predatory odors: a review. Neurosci Biobehav Rev 25:597–609

    CAS  PubMed  Google Scholar 

  • Dill LM, Fraser AHG, Roitberg BD (1990) The economics of escape behaviour in the pea aphid, Acyrthosiphon pisum. Oecologia 83:473–478

    PubMed  Google Scholar 

  • Du YJ, Poppy GM, Powell W, Pickett JA, Wadhams LJ, Woodcock CM (1998) Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J Chem Ecol 24:1355–1368

    CAS  Google Scholar 

  • Frazer BD (1988) Coccinellidae. In: Minks AK, Harrewijn WH (eds) Aphids: their biology, natural enemies and control, volume B. Elsevier, Amsterdam, pp 231–248

  • Gish M, Dafni A, Inbar M (2012) Young aphids avoid erroneous dropping when evading mammalian herbivores by combining input from two sensory modalities. PLoS One 7:e32706

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gnanvossou D, Hanna R, Dicke M (2003) Infochemical-mediated intraguild interactions among three predatory mites on cassava plants. Oecologia 135:84–90

    PubMed  Google Scholar 

  • Gross P (1993) Insect behavioral and morphological defenses against parasitoids. Annu Rev Entomol 38:251–273

    Google Scholar 

  • Hatano E, Kunert G, Weisser WW (2010) Aphid wing induction and ecological costs of alarm pheromone emission under field conditions. PLoS One 5:e11188

    PubMed  PubMed Central  Google Scholar 

  • Hodek I, Evans EW (2012) Food relationships. In: Hodek I, van Emden HF, Honek A (eds) Ecology and behaviour of the ladybird beetles (Coccinellidae). Blackwell, Hoboken, pp 141–168

  • Ito Y (1989) The evolutionary biology of sterile soldiers in aphids. Trends Ecol Evol 4:69–73

    CAS  PubMed  Google Scholar 

  • Janssen A, Bruin J, Jacobs G, Schraag R, Sabelis MW (1997) Predators use volatiles to avoid prey patches with conspecifics. J Anim Ecol 66:223–232

    Google Scholar 

  • Keiser CN, Mondor EB (2015) Cues of predation risk Induce instar- and genotype-specific changes in pea aphid colony spatial structure. Ethology 121:144–151

    Google Scholar 

  • Kotler BP, Brown JS, Slotow RH, Goodfriend WL, Strauss M (1993) The influence of snakes on the foraging behaviour of gerbils. Oikos 67:309–316

    Google Scholar 

  • Kunert G, Otto S, Röse USR, Gershenzon J, Weisser WW (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecol Lett 8:596–603

    Google Scholar 

  • Kusch RC, Mirza RS, Chivers DP (2004) Making sense of predator scents: investigating the sophistication of predator assessment abilities of fathead minnows. Behav Ecol Sociobiol 55:551–555

    Google Scholar 

  • Lima SL (1998) Nonlethal effects in the ecology of predator–prey interactions. Bioscience 48:25–34

    Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Google Scholar 

  • Loose CJ, Dawidowicz P (1994) Trade-offs in diel vertical migration by zooplankton: the costs of predator avoidance. Ecology 75:2255–2263

    Google Scholar 

  • Losey JE, Denno RF (1998) The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecol Entomol 23:53–61

    Google Scholar 

  • Loxdale HD, Lushai G (2007) Population genetic issues: the unfolding story using molecular markers. In: van Emden HF, Harington R (eds) Aphids as crop pests. CAB International, Wallingford, pp 31–68

    Google Scholar 

  • Luca RM, Gerlai R (2012) In search of optimal fear inducing stimuli: differential behavioral responses to computer animated images in zebrafish. Behav Brain Res 226:66–76

    PubMed  Google Scholar 

  • Matsumoto T, Itioka T, Nshida T (2002) Fitness cost of parasitoid avoidance behavior in the arrowhead scale, Unaspis yanonensis Kuwana. Entomol Exp Appl 105:83–88

    Google Scholar 

  • Miller LR, Gutzke WHN (1999) The role of the vomeronasal organ of crotalines (Reptilia: Serpentes: Viperidae) in predator detection. Anim Behav 58:53–57

    CAS  PubMed  Google Scholar 

  • Mondor EB, Roitberg BD (2004) Inclusive fitness benefits of scent-marking predators. Proc R Soc B Biol Sci 271:S341–S343

    Google Scholar 

  • Montgomery ME, Nault LR (1977) Comparative response of aphids to the alarm pheromone, (E)-β-farnesene. Entomol Exp Appl 22:236–242

    CAS  Google Scholar 

  • Muratori FB, Rouyar A, Hance T (2014) Clonal variation in aggregation and defensive behavior in pea aphids. Behav Ecol 25:901–908

    Google Scholar 

  • Nault LR, Edwards LJ, Styer WE (1973) Aphid alarm pheromones: secretion and reception. Environ Entomol 2:101–105

    CAS  Google Scholar 

  • Nelson EH (2007) Predator avoidance behavior in the pea aphid: costs, frequency, and population consequences. Oecologia 151:22–32

    PubMed  Google Scholar 

  • Nelson EH, Matthews SE, Rosenheim JA (2004) Predators reduce prey population growth by inducing changes in prey behavior. Ecology 85:1853–1858

    Google Scholar 

  • New TR (1988) Neuroptera. In: Minks AK, Harrewijn WH (eds) Aphids: their biology, natural enemies and control, volume B. Elsevier, Amsterdam, pp 249–258

  • Pestena JLT, Baird DJ, Soares AMVM (2013) Predator threat assessment in Daphnia magna: the role of kairomones versus conspecific alarm cues. Mar Freshw Res 64:679–686

    Google Scholar 

  • R Development Core Team (2015) R (version 3.3.2), a language and environment for statistical computing. R Foundation, Vienna. http://www.R-project.org

  • Relyea RA (2003) How prey respond to combined predators: a review and an empirical test. Ecology 84:1827–1839

    Google Scholar 

  • Roitberg BD, Myers JH (1979) Behavioural and physiological adaptations of pea aphids (Homoptera: Aphididae) to high ground temperatures and predator disturbance. Can Entomol 111:515–519

    Google Scholar 

  • Schoeppner NM, Relyea RA (2005) Damage, digestion, and defence: the roles of alarm cues and kairomones for inducing prey defences. Ecol Lett 8:505–512

    PubMed  Google Scholar 

  • Stamp NE, Bowers MD (1988) Direct and indirect effects of predator wasps (Polistes sp.: Vespidae) on gregarious caterpillars (Hemileuca lucina: Saturniidae). Oecologia 75:619–624

    CAS  PubMed  Google Scholar 

  • Thaker M, Vanak AT, Owen CR, Ogden MB, Niemann SM, Slotow R (2011) Minimizing predation risk in a landscape of multiple predators: effects on the spatial distribution of African ungulates. Ecology 92:398–407

    PubMed  Google Scholar 

  • Tollrian R (1995) Predator-induced morphological defenses: costs, life history shifts, and maternal effects in Daphnia pulex. Ecology 76:1691–1705

    Google Scholar 

  • Vadas RL, Elner RW (2003) Responses to predation cues and food in two species of sympatric, tropical sea urchins. Mar Ecol (Berl) 24:101–121

    Google Scholar 

  • Verheggen FJ, Haubruge E, Moraes CMD, Mescher MC (2009) Social enviroment influences aphid production of alarm pheromone. Behav Ecol 20:283–288

    Google Scholar 

  • Weisser WW, Braendle C, Minoretti N (1999) Predator-induced morphological shift in the pea aphid. Proc R Soc B Biol Sci 266:1175–1181

    Google Scholar 

  • Witz BW (1989) Antipredator mechanisms in arthropods: a twenty year literature survey. Fla Entomol 73:71–99

    Google Scholar 

Download references

Acknowledgements

We thank Masashi Nomura and Kiyoshi Nakamuta for their valuable comments and Masayuki Hayashi and Haruka Kakuta for help with the experiments. This study was supported by the Japan Society for the Promotion of Science (Basic Research C; grant number 23570018 to YC).

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  1. Laboratory of Applied Entomology, Department of Horticulture, Chiba University, Matsudo 648, Chiba, 271-8510, Japan

    Kazuhiko Tamai & Yasuyuki Choh

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  1. Kazuhiko Tamai
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  2. Yasuyuki Choh
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Correspondence to Yasuyuki Choh.

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Tamai, K., Choh, Y. Antipredator response of pea aphids Acyrthosiphon pisum (Hemiptera: Aphididae): effects of predation risks from an alternative patch on a current patch. Appl Entomol Zool 53, 267–274 (2018). https://doi.org/10.1007/s13355-018-0554-z

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  • DOI: https://doi.org/10.1007/s13355-018-0554-z

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