Ant semiochemicals limit apterous aphid dispersal

Some organisms can manipulate the nervous systems of others or alter their physiology in order to obtain benefit. Ants are known to limit alate aphid dispersal by physically removing wings and also through chemical manipulation of the alate developmental pathway. This results in reduced dispersal and higher local densities of aphids, which benefit ants in terms of increased honeydew and prey availability. Here, we show that the walking movement of mutualistic apterous aphids is also reduced by ant semiochemicals. Aphids walk slower and their dispersal from an unsuitable patch is hampered by ants. If aphid walking dispersal has evolved as a means of natural enemy escape, then ant chemicals may act as a signal indicating protection; hence, reduced dispersal could be adaptive for aphids. If, however, dispersal is primarily a means to reduce competition or to maintain persistent metapopulations, then manipulation by ants could be detrimental. Such manipulation strategies, common in host–parasite and predator–prey interactions, may be more common in mutualism than expected.

[1]  C. Detrain,et al.  Collective exploration and area marking in the ant Lasius niger , 2002, Insectes Sociaux.

[2]  D. Macintosh,et al.  Evidence that insect herbivores are deterred by ant pheromones , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[3]  A. D. Lees.  The production of the apterous and alate forms in the aphid Megoura viciae Buckton, with special reference to the rôle of crowding , 1967 .

[4]  M. Way.  Mutualism Between Ants and Honeydew-Producing Homoptera , 1963 .

[5]  P. Kindlmann,et al.  Timing of dispersal: effect of ants on aphids , 2007, Oecologia.

[6]  David W. Williams,et al.  SPATIAL SYNCHRONY IN FOREST INSECT OUTBREAKS: ROLES OF REGIONAL STOCHASTICITY AND DISPERSAL , 2002 .

[7]  H. Kunkel.  Die Kotabgabe der Aphiden (Aphidina, Hemiptna) unter Einfluß von Ameisen , 1973 .

[8]  G. Mashanov,et al.  Automatic detection of single fluorophores in live cells. , 2007, Biophysical journal.

[9]  S. Leather,et al.  Ant‐mediated dispersal of the black willow aphid Pterocomma salicis L.; does the ant Lasius niger L. judge aphid‐host quality? , 2002 .

[10]  A. Dixon,et al.  Ant attendance in aphids: why different degrees of myrmecophily? , 1999 .

[11]  J. Deneubourg,et al.  Trail laying behaviour during food recruitment in the antLasius niger (L.) , 1992, Insectes Sociaux.

[12]  Relation between diet and polyethism in Formica colonies , 1987 .

[13]  E. Lombaert,et al.  Dispersal strategies of phytophagous insects at a local scale: adaptive potential of aphids in an agricultural environment , 2006, BMC Evolutionary Biology.

[14]  W. Völkl,et al.  Dispersal in the aphid parasitoid, Lysiphlebus cardui (Marshall) (Hym., Aphidiidae) , 1997 .

[15]  H. L. Nixon,et al.  Effects of the Ant, Lasius Niger L., on the Feeding and Excretion of the Bean Aphid, Aphis Fabae Scop , 1958 .

[16]  J. Deneubourg,et al.  Marking as a decision factor in the choice of a new resting site in Lasius niger , 2004, Insectes Sociaux.

[17]  R. Buckley.  INTERACTIONS INVOLVING PLANTS, HOMOPTERA, AND ANTS , 1987 .

[18]  T. Mittler,et al.  A CHEMICAL INFLUENCE OF ANTS ON WING DEVELOPMENT IN APHIDS , 1975 .

[19]  A. Honěk,et al.  The effect of parasitism by Aphelinus abdominalis and drought on the walking movement of aphids , 1998 .

[20]  A. Dixon,et al.  ECOLOGY AND EVOLUTION OF APHID-ANT INTERACTIONS , 2005 .

[21]  J. Hardie,et al.  The role of nutrition, crowding and interspecific interactions in the development of winged aphids , 2001 .

[22]  R. Matthews,et al.  Ants. , 1898, Science.

[23]  S. El‐Ziady.  FURTHER EFFECTS OF LASIUS NIGER L. OX APHIS FABAE SCOPOLI , 2009 .

[24]  R. Rosengren.  The interaction between red wood ants, Cinara aphids, and pines. A ghost of mutualism past? , 1991 .

[25]  O. Sutherland.  The role of crowding in the production of winged forms by two strains of the pea aphid, Acyrthosiphon pisum , 1969 .

[26]  Bruce Johnson.  WING POLYMORPHISM IN APHIDS II. INTERACTION BETWEEN APHIDS , 1965 .

[27]  Ross Ihaka,et al.  Gentleman R: R: A language for data analysis and graphics , 1996 .

[28]  C. Hodgson.  Dispersal of apterous aphids (Homoptera: Aphididae) from their host plant and its significance , 1991 .

[29]  S. Friedman,et al.  Crowding as the primary factor in the production of the agamic alate form of Therioaphis maculata (Homoptera: Aphididae) , 1967 .