Previous exposures to cues from conspecifics and ladybird beetles prime antipredator responses in pea aphids Acyrthosiphon pisum (Hemiptera: Aphididae)

Applied Entomology and Zoology - Tập 54 - Trang 277-283 - 2019
Kazuhiko Tamai1, Yasuyuki Choh1
1Laboratory of Applied Entomology, Department of Horticulture, Chiba University, Chiba,, Japan

Tóm tắt

When prey encounter predators, they exhibit antipredator responses to reduce their risk of predation. Delayed responses can be fatal. Because prey can assess the risk of predation using predation-related cues, previous exposures to these cues could affect subsequent antipredator responses. We tested this possibility using the pea aphid Acyrthosiphon pisum Harris (Hemiptera: Aphididae) and its predator the Asian ladybird beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Aphids disperse from their host plants after sensing predators. We investigated whether previous exposures to cues from conspecifics and ladybird beetles affected the dispersal rates of aphids encountering predators. The cues contained visual, chemical, and vibrational information from aphids and ladybird beetles. Aphids that had previously been exposed to these cues increased dispersal rates and, consequently, suffered less predation than unexposed aphids. To clarify how aphids increased their dispersal rate, we examined their feeding times. Aphids that had been exposed to cues reduced feeding times compared with unexposed conspecifics. Therefore, we further tested whether the predator-induced dispersal of non-feeding aphids was greater than that of feeding conspecifics and found correlated differences. Previous exposures to cues from conspecifics and predators may allow prey to tune their antipredator responses to predation risk prior to further predator encounters.

Tài liệu tham khảo

Ayon RE, Putman BJ, Clark RW (2017) Recent encounters with rattlesnakes enhance ground squirrel responsiveness to predator cues. Behav Ecol Sociobiol 71:149. https://doi.org/10.1007/s00265-017-2378-1 Barbour MA, Clark RW (2012) Ground squirrel tail-flag displays alter both predatory strike and ambush site selection behaviours of rattlesnakes. Proc R Soc B Biol Sci 279:3827–3833 Basile BM, Hampton RR (2012) Monkeys show recognition without priming in a classification task. Behav Process 93:50–61 Braendle C, Weisser WW (2001) Variation in escape behavior of red and green clones of the pea aphid. J Insect Behav 14:497–509 Brown GE, Ferrari MCO, Malka PH, Oligny MA, Romano M, Chivers DP (2011) Growth rate and retention of learned predator cues by juvenile rainbow trout: Faster-growing fish forget sooner. Behav Ecol Sociobiol 65:1267–1276 Choh Y, Takabayashi J, Sabelis MW, Janssen A (2014) Witnessing predation can affect strength of counterattack in phytoseiids with ontogenetic predator-prey role reversal. Anim Behav 93:9–13 De Brujin PJA, Egas M, Janssen A, Sabelis MW (2006) Pheromone-induced priming of a defensive response in Western flower thrips. J Chem Ecol 32:1599–1603 Dielenberg RA, McGregor IS (2001) Defensive behavior in rats towards predatory odors: a review. Neurosci Biobehav Rev 25:597–609 Dill LM, Fraser AHG, Roitberg BD (1990) The economics of escape behaviour in the pea aphid, Acyrthosiphon pisum. Oecologia 83:473–478 Dixon AFG, Agarwala BK (1999) Ladybird-induced life-history changes in aphids. Proc R Soc B Biol Sci 266:1549–1553 Ferrari MCO, Lysak KR, Chivers DP (2010) Turbidity as an ecological constraint on learned predator recognition and generalization in a prey fish. Anim Behav 79:515–519 Ferrari MCO, Vrtělová J, Brown GE, Chivers DP (2012) Understanding the role of uncertainty on learning and retention of predator information. Anim Cogn 15:807–813 Folkers E, Drain P, Quinn WG (1993) Radish, a Drosophila mutant deficient in consolidated memory. Proc Natl Acad Sci USA 60:8123–8127 Goodale E, Kotagama SW (2008) Response to conspecific and heterospecific alarm calls in mixed-species bird flocks of a Sri Lankan rainforest. Behav Ecol 19:887–894 Griffin AS, Evans CS, Blumstein DT (2001) Learning specificity in acquired predator recognition. Anim Behav 62:577–589 Gross P (1993) Insect behavioral and morphological defenses against parasitoids. Annu Rev Entomol 38:251–273 Hardie J, Holyoak M, Taylor NJ, Griffiths DC (1992) The combination of electronic monitoring and video-assisted observations of plant penetration by aphids and behavioural effects of polygodial. Entomol Exp Appl 62:233–239 Harrison KV, Preisser EL (2016) Dropping behavior in the pea aphid (Hemiptera: Aphididae): how does environmental context affect antipredator responses? J Insect Sci 16:1–5 Hatano E, Kunert G, Weisser WW (2010) Aphid wing induction and ecological costs of alarm pheromone emission under field conditions. PLoS One 5:e11188. https://doi.org/10.1371/journal.pone.0011188 Hermann SL, Thaler JS (2014) Prey perception of predation risk: volatile chemical cues mediate non-consumptive effects of a predator on a herbivorous insect. Oecologia 176:669–676 Hughes NK, Korpimäki E, Banks PB (2010) The predation risks of interspecific eavesdropping: weasel-vole interactions. Oikos 119:1210–1216 Kelley JL, Magurran AE (2003) Learned predator recognition and antipredator responses in fishes. Fish Fish 4:216–226 Kotler B, Blaustein L, Brown J (1992) Predator facilitation: the combined effect of snakes and owls on the foraging behavior of gerbils. Ann Zool Fennici 29:199–206 Kouamé KL, Mackauer M (1992) Influence of starvation on development and reproduction in apterous virginoparae of the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae). Can Entomol 124:87–95 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 Leavesley AJ, Magrath RD (2005) Communicating about danger: urgency alarm calling in a bird. Anim Behav 70:365–373 Lima SL (1998) Nonlethal effects in the ecology of predator-prey interactions: what are the ecological effects of anti-predator decision-making? Bioscience 48:25–34 Losey JE, Denno RF (1998) The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecol Entomol 23:53–61 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 Margulies C, Tully T, Dubnau J (2005) Deconstructing memory in Drosophila. Curr Biol 15:700–713. https://doi.org/10.1016/j.cub.2005.08.024 Matsumoto Y, Mizunami M (2002) Temporal determinants of long-term retention of olfactory memory in the cricket Gryllus bimaculatus. J Exp Biol 205:1429–1437 McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of enriched metacommunities. Nature 395:794–798 Menzel R (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53–62 Mondor EB, Roitberg BD (2004) Inclusive fitness benefits of scent-marking predators. Proc R Soc B Biol Sci 271:S341–S343 Nault LR, Edwards LJ, Styer WE (1973) Aphid alarm pheromones: secretion and reception. Environ Entomol 2:101–105 Nelson EH (2007) Predator avoidance behavior in the pea aphid: costs, frequency, and population consequences. Oecologia 151:22–32 Němec M, Syrová M, Dokoupilová L, Veselý P, Šmilauer P, Landová E, Lišková S, Fuchs R (2015) Surface texture and priming play important roles in predator recognition by the red-backed shrike in field experiments. Anim Cogn 18:259–268 Oku K, Yano S, Osakabe M, Takafuji A (2003) Spider mites assess predation risk by using the odor of injured conspecifics. J Chem Ecol 29:2609–2613 Pestana 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 Podjasek JO, Bosnjak LM, Brooker DJ, Mondor EB (2005) Alarm pheromone induces a transgenerational wing polyphenism in the pea aphid, Acyrthosiphon pisum. Can J Zool 83:1138–1141 Relyea RA (2003) How prey respond to combined predators: a review and an empirical test. Ecology 84:1827–1839 Roitberg BD, Myers JH (1978) Adaptation of alarm pheromone responses of the pea aphid Acyrthosiphon pisum (Harris). Can J Zool 56:103–108 R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation, Vienna. http://www.R-project.org Schmitt MH, Stears K, Shrader AM (2016) Zebra reduce predation risk in mixed-species herds by eavesdropping on cues from giraffe. Behav Ecol 27:1073–1077 Stephenson JF (2016) Keeping eyes peeled: guppies exposed to chemical alarm cue are more responsive to ambiguous visual cues. Behav Ecol Sociobiol 70:575–584 Suraci JP, Clinchy M, Dill LM, Roberts D, Zanette LY (2016) Fear of large carnivores causes a trophic cascade. Nat Commun 7:1–7. https://doi.org/10.1038/ncomms10698 Tamai K, Choh Y (2018) 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 Tollrian R (1995) Predator-induced morphological defenses: costs, life history shifts, and maternal effects in Daphnia pulex. Ecology 76:1691–1705 Vandermoten S, Mescher MC, Francis F, Haubruge E, Verheggen FJ (2012) Aphid alarm pheromone: an overview of current knowledge on biosynthesis and functions. Insect Biochem Mol Biol 42:155–163 Weisser WW, Braendle C, Minoretti N (1999) Predator-induced morphological shift in the pea aphid. Proc R Soc B Biol Sci 266:1175–1181 Wisenden BD, Chivers DP, Smith RJF (1997) Learned recognition of predation risk by Enallagma damselfly larvae (Odonata, Zygoptera) on the basis of chemical cues. J Chem Ecol 23:137–151 Witz BW (1990) Antipredator mechanisms in arthropods: a twenty year literature survey. Fla Entomol 73:71–99