I am willing to bet that when most entomologists are out for a walk spend most of their time looking at the ground or the vegetation between the ground and head height. Lepidopterists and odonatologists may be the exceptions that prove the rule, but most of us spend a lot of time looking for things lurking in dung, hiding under stones or bark, scurrying around in the undergrowth or making holes in leaves 🙂
Tell-tale signs for an entomologist that something is or has been enjoying a meal
I’m an entomologist, I’m trained to look out for signs of insect infestations; curled leaves as in the above picture tell me that almost certainly an aphid and her offspring have been at work, sticky leaves alert me to the fact that there are aphids above me in the canopy of a tree. Leaves with holes tell me that a beetle or caterpillar has been at work. Leaves spun together with a silk web tell me a similar story. Plants with their stems and leaves stripped right back inform me that sawfly, lepidoptera and beetle larvae have been at work. A fancy spiral of brown or white on a leaf tells me that a leafminer has been, or is at work. In some cases the insect may not be there when I see the damage, the curled leaves caused by an aphid or psyllid infestation remain there until leaf fall, the chances of finding a caterpillar feeding on the very obviously shot-holed leaves of a plant are slim. Like all sensible herbivores, the culprit will be in hiding closer to the stem, only sporadically popping out to feed. On the other hand it may have fallen victim to a visually acute predator (bird) that was attracted to the leaf by the tell-tale feeding signs, or been eaten by a predatory insect or have been parasitized by an ichneumonid wasp. Plants are a lot less passive than people think. By producing the equivalent of an immune response they cause the insects to move to different feeding sites to make more holes effectively advertising their presence to potential predators. Simultaneously, the plant sends out chemical signals telling insect predators and parasites that there is a meal or host available. An herbivore’s lot is not an easy one.
The Covid-19 crisis means that I have been working from home in a hamlet on the Staffordshire/Shropshire border. To keep myself reasonably sane and moderately physically healthy I have been treating myself to a lunchtime walk along the bridleways, footpaths and public roads within a 5 km radius of my house. As a result I have become much more familiar with the area. One of the things that has been very obvious, apparent even, is that some plants dominate the roadside verges, cow parsley Anthricus sylvestris being one that really stands
Cow parsley – very common and abundant, occurring in huge swathes around Forton and Sutton and in this case and in many other sites along my walks, backed by the equally apparent hawthorn (Crataegusus monogyna) hedge.
out from the crowd at this time of the year. Not only is it very apparent, but it provides a great source of nectar for the spring butterflies such as the Orange Tip and the assorted bumblebees, solitary bees and hoverflies, that despite the anthropogenic pressures put upon them, still manage to make an appearance. Nettles, as I particularly noticed when having to social distance myself from the sweaty joggers and cyclists taking advantage of the virtually deserted country lanes, also play a prominent role in the roadside plant community. Also very common, but showing a much patchier distribution and occurring in clumps, including in my garden, is the ribwort plantain, Plantago lanceolata, which is yet another so called weed*, that is perfect for pollinators.
Ribwort plantain – common but patchy and clumped – this clump in my garden where it is safe from forks and herbicides.
Although both the cow parsley and plantain were buzzing with pollinators, they were, and still are at time of writing, singularly devoid of herbivores, including my favourite aphids. Conversely, the odd scattered bird cherries (Prunus padus) and the solitary self-seeded wild cherry (Prunus avium) in my garden are proudly sporting the characteristic leaf rolls caused by the bird cherry aphid, Rhopaloisphum padi and the cherry black fly, Myzus cerasi respectively.
Note that both these trees were not growing near any of their relatives and were surrounded and overtopped by other plant species, so as far as humans are concerned not very apparent.
This got me to wondering why it was, that, the to me, and presumably other humans, the very obvious cow parsley and plantains, were not covered in plant feeding insects, while the less apparent cherries were heavily infested by their respective aphids. After all, according to Richard Root, large swathes of monocultures are likely to be easily found and colonised by pests. Plant apparency was first defined by the British born, American based ecologist Paul Feeny in the mid-1970s.
“The susceptibility of an individual plant to discovery by its enemies may be influenced not only by its size, growth form and persistence, but also by the relative abundance of its species within the overall community. To denote the interaction of abundance, persistence and other plant characteristics which influence likelihood of discovery, I now prefer to describe “bound to be found” plants by the more convenient term “apparent”, meaning “visible, plainly seen, conspicuous, palpable, obvious” (Shorter Oxford English Dictionary, 3rd, edition; Webster’s Concise English Dictionary). Plants which are “hard to find” by their enemies will be referred to as “unapparent”, the antonym of apparent (O.E.D. and Webster, loco cit.). The vulnerability of an individual plant to discovery by its enemies may then be referred to as its “apparency”, meaning “the quality of being apparent; visibility” (O.E.D. and Webster, loco cit.). Since animals, fungi and pathogens may use means other than vision to locate their host-plants, I shall consider apparency to mean “susceptibility to discovery” by whatever means enemies may employ” Feeny (1976).
So, even though cow parsley is highly visible and apparent to us humans, and their pollinators, because it is an annual and thus ephemeral within the landscape, it is not necessarily apparent to the herbivores that want to feed on it. Conversely, trees, such as bird cherry, although not necessarily apparent to us, are apparent to insect herbivores because they are large and long-lived. How does this affect the way in which plants avoid being found and eaten by insect herbivores?
Peter Price, another British born American based ecologist very neatly summarised Paul’s hypothesis as follows.
Long-lived trees which are bound to be found by herbivores, invest heavily in costly chemical defence with broad-spectrum efficacy. These quantitative defences are expensive but the cost is tolerable for a long-lived plant. Short-lived plants are less easily detected by herbivores, and their best defence is being hard to find in patchy and ephemeral sites. Low cost defences are effective against generalist herbviores should plants be found. Instead of tannins and other digestibility reducers found as defences in long-lived plants, short-lived plants have evolved with mustard oils (glucosinolates) in crucifers, for example, alkaloids in the potato family, furanocoumarins in the carrot family (Price, 2003).
All I can say is that the quantitative defences of the trees don’t seem to be doing as good a job as the less expensive ones of the cow parsley, plantains and nettles. As an aside, it turns out that although both cow parsley and plantain have a lot of medicinal uses, their chemistry does include some insecticides (Adler et al., 1995; Milovanovic et al., 1996). Cheap and cheerful seems to be the answer for an herbivore-free life in this case 🙂 Earlier I referred to cow parsley and plantains as being common. What does that mean? According to Wikipedia (where else would I go?),
“Common species and uncommon species are designations used in ecology to describe the population status of a species. Commonness is closely related to abundance. Abundance refers to the frequency with which a species is found in controlled samples; in contrast, species are defined as common or uncommon based on their overall presence in the environment. A species may be locally abundant without being common.
However, “common” and “uncommon” are also sometimes used to describe levels of abundance, with a common species being less abundant than an abundant species, while an uncommon species is more abundant than a rare species.”
In the UK we have a conservation designation, Sites of Special Scientific Interest, the criteria for selection which can be found here. To save you the trouble of reading the whole document, the way in which rarity and scarcity are defined is as follows.
Nationally Rare (15 or fewer UK hectad (10 km squares) records)
Nationally Scarce – Notable A (31-100 UK hectad records),
Nationally Scarce – Notable B (16-30 hectad records.
Local – (101-300 UK hectad records)
Okay, so what has all this to do with aphids and their pest status? As you all probably know by now I love aphids; as far as I am concerned, where insects are concerned, they are the bee’s knees**.
Unfortunately, aphids get a terrible press, most of it, in my opinion, undeserved.
Just a couple of examples of aphids getting a biblically bad press.
A few years ago, I wrote a short piece about the fact that only a minority of the so far 5600 or so aphids described, are pests, and many are very rare. The cover of this issue of New Scientist from 1977, which appeared a few months after I joined the group, very nicely sums up the question that we really ought to be asking. Here I have to confess that the article from our lab (McLean et al., 1977), made the case for aphids being pests, and it was the late Denis Owen who defended aphids (Owen, 1977).
Tony Dixon’s cereal aphid research group (of which I was proud to be a member) got more than just a mention in this issue.
Two plants that I have a particular interest in are sycamore and bird cherry, mainly because of their aphids, but in the case of the bird cherry, I love its flowers. Now, although both have very similar distributions and occurrences to cow parsley and ribwort plantain, ubiquitous, they are much easier
Distribution of cow parsley, ribwort plantain, and sycamore and bird cherry in the British Isles (Atlas of the British Flora)
to find aphids on than both cow parsley and plantain. On my daily walks during which I pass countless cow parsley and plantain plants, I have, so far, only found one cow parsley with aphids on and not a single plantain has shown any signs of aphid infestation . I have also, only found one nettle plant with Microlophium carnosum on it. Cow parsley has a number of aphid species that use it as a secondary host migrating there from willows or hawthorns. Plantains also serve as host plants to aphids, some such as Dysaphis plantaginea host alternate, others such as Aphis plantaginis, do not. The latter species, if present, is almost always ant attended (Novgorodova & Gavrilyuk, 2012), which, if you know what you are looking for, makes it easy to spot. I know what to look for and so far, have not found any! Nettles are also very common in the roadside verges, and they too have aphids that love them, Microlophium carnosum and Aphis urticata, the former a favourite prey of ants, the latter, farmed by the ants. So far this year I have only found one small colony of M. carnosum, and believe me, I have been looking.
So what about the trees? Sycamores are a common sight on my walks, occurring both as hedges and as solitary trees or sometime in small groups. Almost all the large trees have sycamore aphids, Drepanosiphum platanoidis feeding on their leaves, and many have dense colonies of the maple aphid, Periphyllus testudinaceus, some with ants in attendance. Bird cherry is not as common on my walks and where I have found it, they have been small trees or shrubs usually on their own, and surrounded by other woody plants. Without exception, all have been conspicuously infested by the bird-cherry oat aphid. To summarise, we have common plants that support aphids that are not regarded as rare, but find startlingly different levels of abundance of them here in Staffordshire, and in my experience, elsewhere. At the same time that I have been actively searching for aphids, six species of butterfly that the Woodland Trust lists as common, have been hard to miss. In order of sightings these are the Orange Tip, the Peacock, the Small Tortoiseshell, the Speckled Wood, the Holly Blue and the Brimstone, two of which, the Peacock and the Small Tortoiseshell, being nettle feeders as larvae. Despite the abundance of nettles in the hedgerows, So far I have only seen one small colony of Small Tortoiseshell larvae on the of nettles. I am, at this juncture, unable to resist mentioning that adults of the Holly Blue feed on aphid honeydew J Going back to my original point, the fact that I have seen more butterflies than aphids doesn’t necessarily mean that the aphids are less abundant, just less apparent.
There are at least 614 species of aphid in the UK (Bell et al., 2015). I am not sure how many I have seen, I stopped keeping a personal tick list many years ago, but I would guess that I have seen about half of them. I like aphids, I look for aphids, but there are many ‘common’ species that I have never seen. I have, however, seen some of the rare ones. Four that stand out in my memory are Monaphis antnenata, Stomapahis graffii, Myzocallis myricae and Maculolachnus submacula. The first feeds on the upper surface of birch leaves (Hopkins & Dixon, 1997) and was shown to me by the late Nigel Barlow, when he was on a sabbatical at Silwood Park. Stomaphis graffii which feeds under the bark of sycamores and maples and is ant attended, was shown to me by an MSc student, Andrew Johnson, also at Silwood Park. Myzocallis myricae, the bog myrtle aphid, only found on bog myrtle (Myrica gale) (Hopkins et al., 2002), I saw in the Highlands of Scotland, when Tony Dixon asked me to stop the car so he could go and look at a clump of bog myrtle he had spotted as we drove along between field sites. The giant rose aphid, Maculolachnus submacula, I saw in my garden in Norwich (84 Earlham Road) when I was a PhD student at the University of East Anglia. I only found it because I wondered why there was an ant nest reaching halfway up one of my roses. When I looked, I found that they were farming the aphids that were feeding on the lower stems.
It is important to remember that most aphids are host-specific, some feeding only on a single plant species, others being confined to a single genus with only a minority having a wide host range*** and considered pests (Dixon, 1998). Given this, it is obvious that aphids with rare host plants are also going to be rare (Hopkins et al., 2002). Many aphids are also very fussy about their niche, either feeding on a very particular part of a plant or having a very close association with a particular species of ant. Looking at the aphids that the two Bobs (Influential Points it seems that aphids that are rare are also ant-attended. Given, that many ant-attended aphids aren’t rare it would seem an interesting area to pursue. Perhaps it is the degree of ant-attendance, i.e. facultative versus obligate that is the key factor?
If you look at the list of species of insects that are regarded as endangered and worthy of conservation in the UK, the overwhelming impression is that unless they are big and pretty they don’t get a look in. Needless to say, despite their beauty and fascinating life styles, no aphids are included in the list L
We really should be conserving aphids, not squashing them. Many provide important nutrition for ants and other pollinators, honeydew. They are an important source of food for insects and birds (Cowie & Hinsley, 1988). Aphids also help plants grow by feeding mycorrhizae with their honeydew (Owen, 1980; Milcu et al., 2015). Finally, as aphids are so host specific using the presence of uncommon species in suction traps could help identify sites with rare plants.
Aphids, rare, useful and much maligned, time to rethink their role.
Adler, L.S., Schmitt, J. & Bowers, M.D. (1995) Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia, 101, 75-85.
Bell, J.R., Alderson, L., Izera, D., Kruger, T., Parker, S., Pickup, J., Shortall, C.R., Taylor, M.S., Verier, P. & Harrington, R. (2015) Long-term phenological trends, species accumulation rates, aphid traits and climate: five decades of change in migrating aphids. Journal of Animal Ecology, 84, 21-34.
Cowie, R.J. & Hinsley, S.A. (1988) Feeding ecology of great tits (Parus major) and blue tits (Parus caeruleus), breeding in suburban gardens. Journal of Animal Ecology, 57, 611-626.
Dixon, A.F.G. (1998) Aphid Ecology. Chapman & Hall, London.
Feeny, P. (1976) Plant apparency and chemical defence. Recent Advances in Phytochemistry, 10, 1-40.
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., Thacker, J.I.T., Dixon, A.F.G., Waring, P. & Telfer, M.G. (2002) Identifying rarity in aphids: the importance of host plant range. Biological Conservation, 105, 293-307.
McLean, I., Carter, N. & Watt, A. (1977) Pests out of Control. New Scientist, 76, 74-75.
Milcu, A., Bonkowski, H., Collins, C.M. & Crawley, M.J. (2015) Aphid honeydew-induced changes in soil biota can cascade up to tree crown architecture. Pedobiologia, 58, 119-127.
Milovanovic, M., Stefanovic, M., Djermanovic, V., & Milovanovic, J. (1996). Some chemical constituents of Anthriscus sylvestris. Journal of Herbs, Spices & Medicinal Plants, 4, 17–22. Eugenol – insecticide
Novgorodova, T.A. & Gavrilyuk, A.V. (2012). The degree of protection different ants (Hymenoptera: Formicidae) provide aphids (Hemiptera: Aphididae) against aphidophages European Journal of Entomology, 109, 187-196.
Owen, D.F. (1977) Are aphids really plant pests? New Scientist, 76, 76-77.
Owen, D.F. (1980) How plants may benefit from the animals that eat them. Oikos, 35, 230-235.
Price, P.W. (2003) Macroecological Theory on Macroecological Patterns, Cambridge University Press, Cambridge.
Thacker, J.I., Hopkins, G.W. & Dixon, A.F.G. (2006) Aphids and scale insects on threatened trees: co-extinction is a minor threat. Oryx, 40, 233-236.
Uusitalo, M. (2004) European Bird Cherry (Pruns padus L). A Biodiverse Wild Plant for Horticulture. MTT Agrifood Research Finland, Jokioinen.
*It never ceases to amaze me how many keen gardeners are determined to weed out all the native nectar bearing plants (wees) in their gardens and replace them with useless, gaudy, domesticated, infertile and non-native prima donnas and green deserts!
***Hugh Loxdale however, would argue that all insects are specialists and that so called polyphagous species are, in reality, cryptic specialist species (Loxdale, H.D., Lushai, G. & Harvey, J.A. (2011) The evolutionary improbablity of ‘generalism’ in nature, with special reference to insects. Biological Journal of the Linnean Society, 103, 1-18.)