The impacts of Harmonia axyridis cues on foraging behavior of Aphidius gifuensis to Myzus persicae

다국어 초록 (Multilingual Abstract)

This study investigated the effect of adult associated cues of the multicolored Asian ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae) on the foraging behavior of the aphid parasitoid, Aphidius gifuensis Ashmead (Hymenoptera: Aphididae) with three assays: 1) whole aphid leaf-disc with H. axyridis tracks; 2) aphid leaf-disc with only half contaminated with H. axyridis tracks; 3) aphid leaf-discs without H. axyridis tracks. Foraging behavior of A. gifuensis was recorded using the Observer® XT 11 and EthoVsion® XT 12. In addition, functional responses of A. gifuensis in patches with or without H. axyridis cues were also tested. Aphidius gifuensis females preferred oviposition in arenas where no adult tracks of H. axyridis were present. However, no significant dif ference between functional responses of A. gifuensis foraging in plants with and without H. axyridis cues was detected. Our study suggests that H. axyridis associated cues could influence the foraging behavior and activity of A. gifuensis under laboratory conditions. On the other hand, the foraging efficiency of A. gifuensis was not significantly affected by H. axyridis walking tracks in a single plant system. Aphidius gifuensis might exhibit flexible behavioral responses to predator associated cues. The risk of intraguild interactions and the possibility of mitigating such risks for parasitoids are important components for ultimately determining the compatibility of biological control agents.

참고문헌 (Reference)

1 Bates, D, "lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-13"

2 Fox, J, "car: Companion to applied regression. R package version 2.1-5"

3 Ryan J. Wasserman, "Using functional responses to quantify interaction effects among predators" Wiley 30 (30): 1988-1998, 2016

4 R L. Koch, "The multicolored Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts" Oxford University Press (OUP) 3 (3): 1-16, 2003

5 Pan, M. Z., "The influence of feeding and host deprivation on egg load and reproduction of an aphid parasitoid, Aphidius gifuensis(Hymenoptera : Braconidae)" 52 (52): 255-263, 2017

6 Yoshitaka Nakashima, "The Role of Semiochemicals in the Avoidance of the Seven-Spot Ladybird, Coccinella septempunctata, by the Aphid Parasitoid, Aphidius ervi" Springer Science and Business Media LLC 30 (30): 1103-1116, 2004

7 M. E. Solomon, "The Natural Control of Animal Populations" JSTOR 18 (18): 1-, 1949

8 G A Polis, "The Ecology and Evolution of Intraguild Predation: Potential Competitors That Eat Each Other" Annual Reviews 20 (20): 297-330, 1989

9 HELEN E. ROY, "Ten years of invasion:Harmonia axyridis(Pallas) (Coleoptera: Coccinellidae) in Britain" Wiley 40 (40): 336-348, 2015

10 Heather D. Vance-Chalcraft, "THE INFLUENCE OF INTRAGUILD PREDATION ON PREY SUPPRESSION AND PREY RELEASE: A META-ANALYSIS" Wiley 88 (88): 2689-2696, 2007

11 Ming-Zhen Pan, "Suitability of three aphid species for Aphidius gifuensis (Hymenoptera: Braconidae): Parasitoid performance varies with hosts of origin" Elsevier BV 69 : 90-96, 2014

12 Eric W. Riddick, "Spotlight on the positive effects of the ladybird Harmonia axyridis on agriculture" Springer Science and Business Media LLC 62 (62): 319-330, 2017

13 Achim Zeileis, "Regression Models for Count Data inR" Foundation for Open Access Statistic 27 (27): 1-25, 2008

14 David Rogers, "Random Search and Insect Population Models" JSTOR 41 (41): 369-383, 1972

15 R Development Core Team, "R: a language and environment for statistical computing. Version 3.6.1"

16 R.G. Colfer, "Predation on immature parasitoids and its impact on aphid suppression" Springer Science and Business Media LLC 126 (126): 292-304, 2001

17 W.W. Murdoch, "Predation and Population Stability" Elsevier 9 : 1-131, 1975

18 Taylor, R.J., "Predation" Chapman and Hall 1984

19 Zdeněk RŮŽIČKA, "Persistence of deterrent larval tracks in Coccinella septempunctata, Cycloneda limbifer and Semiadalia undecimnotata (Coleoptera: Coccinellidae)" Biology Centre, AS CR 99 (99): 471-475, 2002

20 Einat Bilu, "Parasitized Aphids Are Inferior Prey for a Coccinellid Predator: Implications for Intraguild Predation" Oxford University Press (OUP) 38 (38): 153-158, 2009

21 Wu, S. L., "Parasitic selectivity of aphidius gifuensis on different ages of myzus persicae and development of their offsprings" 46 (46): 84-88, 2017

22 Toshinori Okuyama, "On selection of functional response models: Holling’s models and more" Springer Science and Business Media LLC 58 (58): 293-298, 2013

23 F.L. Wackers, "Olfactory and Visual Learning and Their Combined Influence on Host Site Location by the Parasitoid Microplitis croceipes (Cresson)" Elsevier BV 4 (4): 105-112, 1994

24 Deborah L. Finke, "Niche Partitioning Increases Resource Exploitation by Diverse Communities" American Association for the Advancement of Science (AAAS) 321 (321): 1488-1490, 2008

25 David J. Perović, "Managing biological control services through multi-trophic trait interactions: review and guidelines for implementation at local and landscape scales" Wiley 93 (93): 306-321, 2018

26 Shaun A. Langley, "Learning by the parasitoid wasp, Aphidius ervi (Hymenoptera: Braconidae), alters individual fixed preferences for pea aphid color morphs" Springer Science and Business Media LLC 150 (150): 172-179, 2006

27 Gary A. Polis, "Intraguild predation: The dynamics of complex trophic interactions" Elsevier BV 7 (7): 151-154, 1992

28 Matthew Meisner, "Intraguild predation on the parasitoid Aphidius ervi by the generalist predator Harmonia axyridis: the threat and its avoidance" Wiley 138 (138): 193-201, 2011

29 Judith K. Pell, "Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives" Springer Science and Business Media LLC 53 (53): 147-168, 2008

30 Xing-Lin Yu, "Intraguild predation between Harmonia axyridis and Aphidius gifuensis: effects of starvation period, plant dimension and extraguild prey density" Springer Science and Business Media LLC 64 (64): 55-64, 2019

31 Jacques Brodeur, "Intraguild interactions in aphid parasitoids" Wiley 97 (97): 93-108, 2000

32 J.A. Rosenheim, "Intraguild Predation Among Biological-Control Agents: Theory and Evidence" Elsevier BV 5 (5): 303-335, 1995

33 Daniel R. Latham, "Host instar preference and functional response of Aphidius transcaspicus, a parasitoid of mealy aphids (Hyalopterus species)" Springer Science and Business Media LLC 57 (57): 603-610, 2012

34 Yi Feng, "Host Plants Affect the Foraging Success of Two Parasitoids that Attack Light Brown Apple Moth Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae)" Public Library of Science (PLoS) 10 (10): e0124773-, 2015

35 Douglas A. Landis, "Habitat Management to Conserve Natural Enemies of Arthropod Pests in Agriculture" Annual Reviews 45 (45): 175-201, 2000

36 William E. Snyder, "GENERALIST PREDATORS DISRUPT BIOLOGICAL CONTROL BY A SPECIALIST PARASITOID" Wiley 82 (82): 705-716, 2001

37 Bhupendra KUMAR, "Functional response and predatory interactions in conspecific and heterospecific combinations of two congeneric species (Coleoptera: Coccinellidae)" Biology Centre, AS CR 111 (111): 257-265, 2014

38 P. J. Lester, "Functional and numerical responses do not always indicate the most effective predator for biological control: an analysis of two predators in a two-prey system" Wiley 39 (39): 455-468, 2002

39 Peter A. Abrams, "Functional Responses of Optimal Foragers" University of Chicago Press 120 (120): 382-390, 1982

40 Robert J. O'Neil, "Functional Response and Search Strategy of Podisus maculiventris (Heteroptera: Pentatomidae) Attacking Colorado Potato Beetle (Coleoptera: Chrysomelidae)" Oxford University Press (OUP) 26 (26): 1183-1190, 1997

41 Pritchard, D, "Frair:Functional response analysis in R. R Package Version 0.4"

42 Polis, G. A., "Food Webs" Chapman & Hall 1996

43 Wang, S. Y., "Feeding and parasitic functional responses of the parasitoid Aphelinus asychis Walker to green preach aphid Myzus persicae(Sulzer)" 43 (43): 267-274, 2016

44 Raki Almohamad, "Encounters with aphid predators or their residues impede searching and oviposition by the aphid parasitoidAphidius ervi(Hymenoptera: Aphidiinae)" Wiley 21 (21): 181-188, 2014

45 Hironori YASUDA, "Effects of conspecific and heterospecific larval tracks on the oviposition behaviour of the predatory ladybird, Harmonia axyridis (Coleoptera: Coccinellidae)" Biology Centre, AS CR 97 (97): 551-553, 2000

46 Agarwala, B. K., "Effects of conspecific and heterospecific competitors on feeding and oviposition of a predatory ladybird : a laboratory study" 106 (106): 219-226, 2003

47 Bradley J. Cardinale, "Effects of biodiversity on the functioning of trophic groups and ecosystems" Springer Science and Business Media LLC 443 (443): 989-992, 2006

48 Taylor, A. J., "Effect of aphid predators on oviposition behavior of aphid parasitoids" 11 (11): 297-302, 1998

49 Antonio Biondi, "Ecology, Worldwide Spread, and Management of the Invasive South American Tomato Pinworm, Tuta absoluta: Past, Present, and Future" Annual Reviews 63 (63): 239-258, 2018

50 Juliano, S., "Design and analysis of ecological experiments" Oxford University Press 178-196, 2001

51 William E. Snyder, "Coccinellids in diverse communities: Which niche fits?" Elsevier BV 51 (51): 323-335, 2009

52 Yoshitaka Nakashima, "Chemically Mediated Intraguild Predator Avoidance by Aphid Parasitoids: Interspecific Variability in Sensitivity to Semiochemical Trails of Ladybird Predators" Springer Science and Business Media LLC 32 (32): 1989-1998, 2006

53 Bradley J. Cardinale, "Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem" Wiley 6 (6): 857-865, 2003

54 Yoshitaka Nakashima, "Avoidance of ladybird trails by an aphid parasitoid Aphidius ervi : active period and effects of prior oviposition experience" Wiley 109 (109): 163-166, 2003

55 Robert D. Holt, "A Theoretical Framework for Intraguild Predation" University of Chicago Press 149 (149): 745-764, 1997

56 Ulrich Halekoh, "A Kenward-Roger Approximation and Parametric Bootstrap Methods for Tests in Linear Mixed Models - TheRPackagepbkrtest" Foundation for Open Access Statistic 59 (59): 1-30, 2014