Tinker, Tailor, Soldier Aphid!

As a follow-up to my earlier article about biting aphids https://simonleather.wordpress.com/2013/01/25/not-all-aphids-are-vegans/, I thought it would be fun to draw people’s attention to a little-known aspect of aphid biology and ecology and yet another reason for why I love aphids so much.  Tree leaves are only really good food sources for aphids in spring and autumn, when the levels of soluble nitrogen are at their highest levels in the phloem sap (Dixon, 1973).

To get around this, a number of aphid species modify the leaf tissues by forming galls.  The galls, which are induced by chemicals in the saliva of the aphid, contain cells which are higher in nitrogen than the surrounding tissues and ensure that the nutritional quality of the leaves remains high throughout the year.

Those tree-feeding aphids, such as the sycamore aphid, Drepanosiphum platanoidis, which are unable to form galls, enter summer aestivation (reduce their metabolic rates) as an adaptation to the low nitrogen levels found in summer leaves.  Amongst aphids, the Pemphigine aphids are renowned for their gall forming activities, many of which are formed along the leaf petiole.  The position of the gall along the petiole is very important, the closer the gall is to the base of a leaf, the better the quality of the food that the gall inhabitants experience.  There is thus a premium to be gained by either being first to form a gall, or, if in second place, to usurp the aphid stem mother that got there first and push her further up the leaf petiole.   We thus see two strategies.  In the first strategy, newly emerged first instar nymphs, (such as Pemphigus betae) fight each other  for the best position on the petiole (Whitham, 1979). These fights are serious affairs, and incredibly, can last for up to two days.

In the second strategy, as seen in a related species, Epipemphigus niisimae, where a gall has already been formed by an earlier arrival, the first instar nymphs fight to gain possession of this premium dwelling place.  These fights are even more vicious and protracted and can actually result in the death of the loser (Aoki & Makino, 1982).

As a further development, a number of gall-forming aphids, such as Ceratoglypnia styracicola and Hamamelistes cristafolaie, have a specially adapted nymphal morph, with thicker and broader front legs, whose function is to defend gall usurpation by other aphid stem mothers, so-called soldier aphids (Akimoto et al, 1996; Aoki & Kurosu, 2010).  These stay outside the gall and repel possible invaders.  It should thus not come as a surprise to find that in some species, the soldiers don’t just fight other aphids, but actually defend their siblings against predators, even being able to kill lacewing larvae (Kutsukake et al., 2004).

Truly a force to be reckoned with and of course why I love aphids so much.

Akimoto, S., Ozaki, K. &Matsumoto, Y. (1996). Production of first-instar defenders by the Hormaphidid gall-forming aphid Hamamelsites cristafoliae living anholocyclically on Betula maximowicziana. Japanese Journal of Entomology 64, 879-888.

Aoki, S. &Makino, S. (1982). Gall usurpation and lethal fighting among fundatrices of the aphid Epipemphigus niisimae. Kontyu 50, 365-376.

Aoki, S. & Kurosu, U. (2010) A review of the biology of Cerataphidini (Hemiptera, Aphididae, Hormaphidinae), focusing mainly on their life cycles, gall formation, and soldiers. Psyche, 2010, http://connection.ebscohost.com/c/articles/60639059/

Dixon, A.F.G. (1973)  Biologyof Aphids, Edward Arnold, London

Kutsukake, M., Shibao, H., Nikoh, N., Morioka M., Tamura, T., Hoshino, T., Ohgiya, S, & Fukatsu, T. (2004) Venomous protease of aphid soldier for colony defense,  Proceedings of the National Academy of Sciences USA, 101,11338-11343. http://www.pnas.org/content/101/31/11338.full.pdf+html

Whitham, T. G. (1979). Territorial behaviour of Pemphigus gall aphids. Nature 279, 324-325.

http://www.nature.com/nature/journal/v279/n5711/abs/279324a0.html