If I were to misquote Jane Austen and state “It is a truth universally acknowledged, that aphids are found on the underside of leaves” most people who know what aphids are would agree without quibbling. If natural enemies could speak, they would probably agree as this quote from an early paper by my former boss, Hugh Evans puts it “since most aphids are found on the lower surfaces of leaves anthocorids must be wasting time in searching the upper leaf surface” (Evans, 1976). The only enemies that regularly search the upper surface of leaves are parasitoids, which use aphid honeydew as a host-findng cue (e.g. Volkl, 1994), which is where it falls if the leaves above them are infested with aphids. We know that not all aphids feed on leaves, many using roots, flowers, stems and even tree trunks as their preferred feeding sites, but do all leaf-feeding aphids behave in the same way?
A few species of leaf-dwelling aphid buck the trend and live on the upper surface of leaves. Dogma has it that most leaf-feeding aphids prefer the underside because there are more stomata there and this makes access to the phloem easier.
Aphis grossulariae on the underside of a gooseberry leaf, – only revealed because I turned the leaf over.
Look, however, at a neat experiment that Graham Hopkins and Tony Dixon did (Hopkins & Dixon, 2000). They showed that the birch aphid Euceraphis betulae, which is normally found on the lower surface of leaves, will, if the leaves are held so that the upper surface faces the ground, move from the now facing upward lower surface to the now facing downward upper surface. The answer can’t all be to do with the stomata. That said, in grasses and other monocotyledonous plants, there are more stomata on the upper surface of the leaves andmMany grass-feeding aphids do seem to have a predilection for the upper surface. The green spruce aphid, Elatobium abietinum, another aphid that has a very strong preference for feeding through stomata, is found mainly on the upper surface of spruce needles which are where the stomata are more prevalent (Parry, 1971).
Utamophoraphora humboltdi feeding on the upper surface of Poa annua outside my office.
The Green Spruce Aphid, Elatobium abietinum feeding on the upper surface of spruce needles (Albrecht (2017)
It is possible, however, that the preference for the upper surface of grasses is not entirely due to the relative abundance of stomata there. The grass aphid, Sipha kurdjumovi for example, although most commonly found feeding on the upper surface of grass and cereal leaves, prefers to settle on a concave ridged surface (Dixon & Shearer, 1974), a characteristic of the upper surface of many grasses Lewton-Brain, 1904). Another advantage to living on the upper surface of grass leaves is that when grasses want to conserve water they roll inwards along the mid-vein, which has the added benefit of hiding the aphids and protecting them from their natural enemies.
Mainly, however, if you are an aphid, you feed where the stomata are plentiful, hence the tendency for aphids living on monocotyledonous plants to feed mainly on the upper surface of leaves, instead of the lower surface. Conversely, a leaf-feeding aphid on a dicotyledonous host plant would be expected to feed on the lower surface of the leaves, where there are more stomata. It also makes sense for those aphids to be underneath the leaf, as there is less chance of them being knocked off by the rain or being dislodged by leaves brushing against each other in the wind.
There are, however, two tree-dwelling aphids in the UK that live on the upper side of the leaves of their woody hosts, the very rare Monaphis antennata on birch (Hopkins & Dixon, 1997) and the less rare large walnut aphid, Panaphis juglandis on walnut (Heie, 1982). So what makes these aphids so contrary? According to Graham Hopkins and Tony Dixon (Hopkins & Dixon, 1997), M. antennata is taking advantage of enemy-free space and to compensate for living on top of the leaf is cryptic to avoid detection by enterprising predators, and has a flattened and contoured body shape to avoid accidental dislodgement.
When it comes to P. juglandis things are bit more conjectural. Interestingly, despite being a pest in some parts of the world (e.g. Wani & Ahmad, 2014) we don’t know much about it. It is also hard to understand why it has adopted the upper side of the leaf as its habitat. One very obvious downside
Panaphis juglandis – prominently lined up along the mid-vein of the upper surface of a walnut leaf and displaying their possible unpalatability by their conspicuous yellow and black colouration. From Influential Points https://influentialpoints.com/Images/Panaphis_juglandis_nymphs_on-vein_c2013-07-06_18-35-17ew.jpg
is that by so doing it has opened Itself up to competition from the other common walnut aphid, Chromaphis juglandicola, the honeydew of which falls from the leaves like acid rain on to P. juglandis and prevents them living on the same trees (Olson, 1974; Wani & Ahmad, 2014). In the absence of C. juglandicola it is, however, very successful with a number of life history traits that presumably ensure its survival, although no one has quantified this. First, it is striped yellow and black, a clear warning sign. Bob Dransfield and Bob Brightwell who run that fantastic site, Influential Points, suggest that perhaps P. juglandis sequesters juglone from its walnut host as a defence against predators. It therefore makes sense to advertise it by being conspicuously coloured. Second, they also, point out that the way in which the nymphs line up along the mid-vein might act as a form of masquerade mimicry or disruptive camouflage, by looking from certain angles like a blemish caused by a fungal disease or injury. Neither of these suggestions answer the question as to why it lives on the upper side of leaves. For M. antennata, escape from natural enemies and competition are cited as the reason why it lives where it does. Neither seem to explain P. juglandis, as it is not, at least according to Olson (1974), safe from predation and parasitism, although there is some indication that it might be ant-attended (Fremlin, 2016), nor is it able to share its host plant with the other walnut specialist, Chromaphis juglandicola. On the other hand, unlike M. antennata, it is most definitely not a rarity.
As they used to say when I was young, “answers on a postcard please”. In the meantime, until someone has the time and inclination to delve into this intriguing conundrum, I guess we should add it to Ole Heie’s list of unsolved aphid mysteries 🙂
Albrecht, A. (2017) Illustrated identification guide to the Nordic aphids feeding on conifers (Pinophyta) (Insecta, Hemiptera, Sternorhyncha, Aphidomorpha). European Journal of Taxonomy, 338, 1-160.
Dixon, A.F.G. & Shearer, J.W. (1974) Factors determining the distribution of the aphid, Sipha kurdjumovi on grasses. Entomologia experimentalis et applicata, 17, 439-444.
Evans, H.F. (1976) The searching behaviour of Anthocoris confusus (Reuter) in relation to prey density and plant surface topography. Ecological Entomology, 1, 163-169.
Fremlin, M. (2016) The large walnut aphid (Panaphis juglandis Goeze) – A few observations. Nature in North-East Essex, 2016, 68-76.
Heie, O.E. (1982) Fauna Entomologia Scandinavia, Vol. 11. The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. II. The family Drepanosiphidae. Scandinavian Science Press, Klampenbourg, Denmark.
Heie, O.E. (2009) Aphid mysteries not yet solved/Hemiptera:Aphidomorpha./. Monograph Aphids and Other Hemipterous Insects, 15, 31-48.
Hopkins, G.W. & Dixon, A.F.G. (1997) Enemy-free space and the feeding niche of an aphid. Ecological Entomology, 22, 271-274.
Hopkins, G.W. & Dixon, A.F.G. (2000) Feeding site location in birch aphids (Sternorrhyncha: Aphididae): the simplicity and reliability of cues. European Journal of Entomology, 97, 279-280.
Lewton-Brain, L. (1904). VII. On the anatomy of the leaves of British grasses. Transactions of the Linnaean Society of London, Botany, Series 2, 6, 312-359.
Olson, W.H. (1974) Dusky-veined walnut aphid studies. California Agriculture, 28, 18-19.
Parry, W.H. (1971) Differences in the probing behaviour of Elatobium abietinum feeding on Sitka and Norway spruces. Annals of Applied Biology, 69, 177-185.
Volkl, W. (1994) Searching at different spatial scales: the foraging behaviour of the aphid parasitoid Aphidius rosae in rose bushes. Oecologia, 100, 177-183.
Wani, S.A. & Ahmad, S.T. (2014). Competition and niche-partitioning in two species of walnut aphids. International Journal of Scientific Research and Reviews 3, 120 – 125.
Willmer, C. & Fricker W (1996) Stomata, Springer, Berlin.