Not all aphids get eaten – “bottom-up” wins this time

In the lecture that I introduce aphids to our entomology MSc students I show them two quotes that illustrate the prodigious reproductive potential of these fantastic animals.

“In a season the potential descendants of one female aphid contain more substance than 500 million stout men “– Thomas Henry Huxley (1858) and “In a year aphids could form a layer 149 km deep over the surface of the earth.  Thank God for limited resources and natural enemies” – Richard Harrington (1994).

I was a little discomfited whilst researching this article to find that both Huxley and I had been short-changed, although the original quote does hint at the mortality factors that an aphid clone faces during its life.

The original words and the morphed ‘quote’

 

Both these quotes acknowledge the contribution that both bottom-up and top-down factors have on aphid populations.  For those not familiar with the ecological jargon, ecologists have at times over the last 40 years or so, got quite territorial* about whether herbivorous insect populations are regulated by top-down e.g. predators or bottom-up e.g. host plant quality, factors (e.g. Hunter & Price, 1992).  Who is in charge of an aphid clone’s destiny, natural enemies or the food plant?

Aphids are the favourite food of several insect species; ladybirds (but not all species), lacewing larvae, hoverfly larvae, and also the larvae of some Cecidomyiid flies (Aphidoletes spp.), and Chamaemyiid flies (e.g. Leucopis glyphinivora).  They are also attacked by other Hemipteran species, such as Anthocoris nemorum.   Those insects that make a living almost solely from aphids, are termed aphidophagous and every three years you can, if you feel like it, attend an international conference devoted to the subject 🙂

As well as these specialist predators, aphids are also preyed upon by more generalist predators, such as carabid and staphylinid beetles, harvestmen and spiders. Aphids also provide a nutritious snack for birds and bats.  Faced with all these hungry and voracious predators you might wonder why it is that aphids ever get numerous enough to become pests.  There are two answers, their fantastic reproductive rates and second, aphids, despite appearing soft and squishy, do have anti-predator defence mechanisms.  These range from kicking predators in the face, dropping off the plant, gumming up the jaws of predators by smearing them with wax from their siphunculi, and even jumping out of the way of the predator (Dixon, 1958).  On top of all that,  many are extremely unpalatable and even poisonous.

Some population modelling work from the 1970s explains why aphids can often become pests, as well as introducing us to the concept of population dynamics geography; the endemic and epidemic ridges, and my favourite, the natural enemy ravine (Southwood & Comins, 1976).

The geography of population dynamics from Southwood & Comins (1976)

 

They suggested that if enough predators are already present in the habitat or arrive shortly after the aphids, then the aphid population either goes extinct or only reaches the “endemic ridge”.  The phenomenal rate at which aphids can reproduce under favourable conditions, usually gets them past the “natural enemy ravine” and up into “epidemic ridge” with only a slight slowdown in population growth.   Evidence for the “natural enemy ravine” is not very convincing and I feel that the suggestion that the dip in population growth at the start of the season is due to intermittent immigration by winged aphids and not the action of polyphagous predators (Carter & Dixon, 1981) is pretty convincing.   That said, later modelling work suggested that the subsequent growth of aphid populations could be slowed down by the action of natural enemies Carter et al., 1982).

Aphids, despite their ability to produce baby aphids extremely quickly, are not equally abundant all year round. Those of us who want to collect aphids know that the best time of year is early in the season, spring and early summer.  This is the time when the plant sap is flowing quickly and is rich in nutrients, especially nitrogen, which aphids need in large quantities.    A characteristic of aphid populations is the way they suddenly disappear during July, a phenomenon known as the “mid-summer or mid-season crash”.  This is not just a phenomenon confined to aphids living on ephemeral herbaceous hosts, it happens to tree-dwelling aphids too e.g. the sycamore aphid, Drepanoisphum platanoidis.  At Silwood Park, where I monitored sycamore aphid populations on fifty-two trees for twenty years**, I saw the same pattern of a rapid build-up followed by an equally rapid collapse every year.  The pattern was the same in both high population and low population years and happened at pretty much the same time every year.  Herbivorous insects are, as you might expect, strongly

High and low population years of sycamore aphid, Drepanosiphum platanoidis at Silwood Park

affected by the quality of their host plant, the availability of nitrogen in the leaves being of most importance (Awmack & Leather, 2002).  Aphids are no exception, and their whole-life cycle is adapted to the ever-changing, but predictable availability of soluble nitrogen and water in their host plants (Dixon, 1977).  Plants become less suitable for aphids as their tissues mature and they lock their nitrogen away in the leaves and other structures, rather than transporting it around in the phloem as they do in spring and autumn (Dixon, 1976).

Aphids respond in two ways to a decline in the nutritional quality of their host plant, they reduce the number of offspring they produce (e.g. Watt, 1979) and those offspring they produce are winged (e.g. Parry, 1977), or if already winged, more likely to take flight and seek new better quality host plants (e.g. Dixon, 1969; Jarosik & Dixon, 1999).  In some aphids there is also an increase in intrinsic mortality (e.g. Kift et al., 1998).

The mid-season crash is not confined to abundant and common aphids, rare aphids show exactly the same changes in their populations, and this is similarly attributed to changes in the nutritional quality of the aphid host plant leading to increased dispersal (e.g. Kean, 2002).

Population crash of the rare aphid Paradoxaphis plagianthi in New Zealand (data from Kean, 2002).

Although some authors, notably Alison Karley and colleagues have suggested that it is the action of natural enemies and not host nutrition that drives the mid-season crash (Karley et al., 2003, 2004), the overwhelming evidence points to the production of winged (alate) morphs and their dispersal, being the major factor in causing the mid-season crash as the graphs below illustrate.

Cereal aphids on wheat showing increased alate production coinciding and subsequent population crash on cereal crops. Data from Wratten, 1975).

Green spruce aphid, Elatobium abietinum on Norway spruce at Silwood Park, showing the population crash and associated increase in the number of winged aphids. Data from Leather & Owuor (1996).

Green spruce aphid in Ireland, population crash associated with marked decline in fecundity and production of winged forms. Data from Day (1984)

Data presented by Way & Banks (1968) might lend some support to the idea that natural enemies cause the mid-season crash.  A close examination of the data however, which might at first glance suggest that keeping natural enemies away, allows aphid populations to prosper, reveals that the process of excluding natural enemies also prevents the dispersal of the winged aphids, which have no choice but to stay on the host plant and reproduce there.

Aphis fabae populations on Spindle bushes from Way & Banks (1968). Top line shows the population kept free of predators until August 2^nd, bottom line, exposed to predators.

Moreover, as the authors themselves state “the rise to peak density in each year, coincided with an enormous increase in the proportion of individuals destined to become alatae” (Way & Banks, 1968).   I do not dispute that natural enemies have an effect on aphid populations, but in my opinion, the evidence does not support the hypothesis that they are the driving force behind the mid-season crash.  Rather, the major factor is the reduction in host quality, caused by a decline in the nutritional status of the plant and overcrowding of the aphids, leading to reduced fecundity and an increase in winged dispersers.

I don’t deny that the natural enemies do a very good mopping-up job of those aphids that are left behind, but they are not the force majeure by any stretch of the imagination. Most aphids do not get eaten 🙂

 

References

Awmack, C.S. & Leather, S.R. (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, 47, 817-844.

Carter, N. & Dixon, A.F.G. (1981) The natural enemy ravine in cereal aphid population dynamics: a consequence of predator activity or aphid biology? Journal of Animal Ecology, 50, 605-611.

Carter, N., Gardner, S.M., Fraser, A.M., & Adams, T.H.L. (1982) The role of natural enemies in cereal aphid population dynamics. Annals of Applied Biology, 101, 190-195.

Day, K.R. (1984) The growth and decline of a population of the spruce aphid Elatobium abietinum during a three  study, and the changing pattern of fecundity, recruitment and alary polymorphism in a Northern Ireland Forest. Oecologia, 64, 118-124.

Dixon, A.F.G. (1958) The escape responses shown by certain aphids to the presence of the coccinellid Adalia decempunctata (L.). Transactions of the Royal Entomological Society London, 110, 319-334.

Dixon, A.F.G. (1969) Population dynamics of the sycamore aphid Drepanosiphum platanoides (Schr) (Hemiptera: Aphididae); migratory and trivial flight activity. Journal of Animal Ecology, 38, 585-606.

Dixon, A.F.G. (1976) Factors determining the distribution of sycamore aphids on sycamore leaves during summer. Ecological Entomology, 1, 275-278.

Dixon, A.F.G. (1977) Aphid Ecology: Life cycles, polymorphism, and population regulation. Annual Review of Ecology & Systematics, 8, 329-353.

Harrington, R. (1994) Aphid layer. Antenna, 18, 50-51.

Hunter, M.D. & Price, P.W. (1992) Playing chutes and ladders – heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology, 73, 724-732.

Huxley, T.H. (1858) On the agmaic reproduction and morphology of Aphis – Part I. Transactions of the Linnean Society London, 22, 193-219.

Jarosik, V. & Dixon, A.F.G. (1999) Population dynamics of a tree-dwelling aphid: regulation and density-independent processes. Journal of Animal Ecology, 68, 726-732.

Karley, A.J., Parker, W.E., Pitchford, J.W., & Douglas, A.E. (2004) The mid-season crash in aphid populations: why and how does it occur? Ecological Entomology, 29, 383-388.

Karley, A.J., Pitchford, J.W., Douglas, A.E., Parker, W.E., & Howard, J.J. (2003) The causes and processes of the mid-summer population crash of the potato aphids Macrosiphum euphorbiae and Myzus persicae (Hemiptera: Aphididae). Bulletin of Entomological Research, 93, 425-437.

Kean, J.M. (2002) Population patterns of Paradoxaphis plagianthi, a rare New Zealand aphid. New Zealand Journal of Ecology, 26, 171-176.

Kift, N.B., Dewar, A.M. & Dixon, A.F.G. (1998) Onset of a decline in the quality of sugar beet as a host for the aphid Myzus persicae.  Entomologia experimentalis et applicata, 88, 155-161.

Leather, S.R. & Owuor, A. (1996) The influence of natural enemies and migration on spring populations of the green spruce aphid, Elatobium abietinum Walker (Hom., Aphididae). Journal of Applied Entomology, 120, 529-536.

Parry, W.H. (1977) The effects of nutrition and density on the production of alate Elatobium abietinum on Sitka spruce. Oecologia, 30, 637-675.

Southwood, T.R.E. & Comins, H.N. (1976) A synoptic population model.  Journal of Animal Ecology, 45, 949-965.

Watt, A.D. (1979) The effect of cereal growth stages on the reproductive activity of Sitobion avenae and Metopolphium dirhodum. Annals of Applied Biology, 91, 147-157.

Way, M.J. & Banks, C.J. (1968) Population studies on the active stages of the black bean aphid, Aphis fabae Scop., on its winter host Euonymus europaeus L. Annals of Applied Biology, 62, 177-197.

Wratten, S.D. (1975) The nature of the effects of the aphids Sitobion avenae and Metopolophium dirhodum on the growth of wheat. Annals of Applied Biology, 79, 27-34.

 

Post script

For those interested this is how Huxley arrived at his number of potential descendants, and here I quote from his paper,  “In his Lectures, Prof. Owen adopts the calculations taken from Morren (as acknowledged by him) from Tougard that a single impregnated ovum  of Aphis may give rise, without fecundation, to a quintillion of Aphides.” I have not, so far, been able to track down Tougard.

Morren, C.F.A. (1836) sur le Puceron du Pecher, Annales des Sciences Naturelle series 2. vi.

You may not know what a grain is, so to help you visualise it, 7000 grains equals a pound so 2 000 000 grains gives you 286 pounds, or 20 stone or approximately 130 Kg depending on where you come from J

 

*and generated some magnificent paper titles and quite acrimonious responses J Hassell, M.P., Crawley, M.J., Godfray, H.C.J., & Lawton, J.H. (1998) Top-down versus bottom-up and the Ruritanian bean bug. Proceedings of the National Academy of Sciences USA, 95, 10661-10664.

**A true labour of love as I also counted maple aphids, orange ladybirds, winter moth larvae and any of their predators and parasites that I came across J

 

Pick and mix 12 – Ten largely entomological and tree-related links

All sorts

 

Plants for bugs – making gardens insect friendly

Bugs for humans – making insects more attractive as food

Bugs for bugs – making carrion diets better for their offspring

Bugs for tourism – fireflies keeping a Mexican town alive

Dead trees for bugs – a free issue on saproxylic insect conservation

How trees can help cool cities and a link to the full report

Courtship behaviour of the Grayling butterfly via Ray Cannon

The chemistry of autumn colours – with a nice downloadable graphic

Why natural history teaching needs to be an increasing part of university education

Good news for those of us who like butter, cheese and meat 🙂

Autumn is on the way

Bringing ecology blogging into the scientific fold: measuring reach and impact of science community blogs

At the end of the year there is a tendency for some scientific bloggers to take advantage of the statistics provided by their host platform to produce a round-up of their year and to compare their figures with previous years.  I too am one of the number crunchers and revel in the data available 🙂  One of the frustrating things, for me at any rate, is the lack of a benchmark, how are you doing compared with other bloggers?  This year I decided to try and get some data and approached Jeff Ollerton to see if he would let me look at his 2016 data, which he kindly did and this allowed me to produce a comparative graph.  Much wants more.  As an entomologist an n of 2 is small beer.  I needed more data to satisfy my craving.  I also talk to our postgraduate students about the value of social media, including blogging, but rely mainly on personal anecdotes.  What was needed was something concrete to support my assertions.

I subscribe to, and follow a number of blogs, but there are a few that I feel are somewhat similar in their aims and scope to mine.  One is Jeff Ollerton’s Biodiversity Blog, the others are Dynamic Ecology, Ecology Bits, Ecology is Not a Dirty Word, Scientist Sees Squirrel and Small Pond Science.  Jeff is also a follower of these blogs and when I suggested that it would be a good idea to try to write something about the value of blogging to academics and why our employees should support us in our endeavours he promptly suggested that we get in touch with those bloggers.  I couldn’t see a downside to this so first approached Manu Saunders of Ecology is Not a Dirty Word and Steve Heard of Scientist Sees Squirrel as these were the two bloggers with whom I had interacted most.  Steve then helped bring the others on board and that is how it all began (at least that is how I remember it).

The Blogging Consortium

Manu very kindly took charge of the data collation and I made a first stab at drafting the paper in mid-January.  Steve did a very good job of rewriting it and Meg Duffy (Dynamic Ecology) Jeff Ollerton and Amy Parachnowitsch (Small Pond Science) got into the swing of things as well.  By the end of January we were really motoring and bouncing ideas of each other and the rapidly growing draft.  As with all non-mainstream activities, the day jobs got in the way and we had a couple of months where very little happened.  I felt that things were slipping a little and in the spring had another go at the draft and this stimulated another flurry of action from what we were now calling the blogging consortium, with major contributions from Meg, Jeff and Steve, which put us all on our mettle and something that was beginning to look like a completed paper appearing.  By May Manu had got us all working on a Google Doc document which greatly improved our efficiency.  As we were now heading toward June, some further analysis was needed and Manu bravely volunteered to become the lead author and general butt kicker 🙂 It worked, and by the beginning of July we were ready to submit and had started discussing potential journals.  As the paper was all about science communication we were very keen to get it in a high-profile Open Access journal, but one that didn’t charge an arm and a leg as our paper had no grant income associated with it.  After a couple of enquiries Manu found a journal that fitted our requirements and was willing to have a look at it and on July 20^th 2017 Manu submitted our paper to Royal Society Open Science.  Six weeks later we were euphoric!

Oh frabjous day!

The comments of the reviewers were some of the best I have ever seen, and I submitted my first paper in 1979 🙂  I have never had the word limpid applied to my writing, it just shows what can be achieved by cooperation.   I can’t resist sharing some of the comments from the reviewers

Associate Editor Comments to Author:

 

Both reviewers are very positive about this manuscript and indeed I agree with them. It is an important piece and a very inspirational read.

Reviewer: 1

At one time, my favourite t-shirt slogan was “More people are reading this t–shirt than your blog” – those days are clearly gone as this paper shows, at least in ecology! ……..Their thoughts on citing blogs will, I suspect, launch many posts and comments on their respective blogs. I think this paper will be an important contribution to what is very much a developing field. I have no comments to add and, for the first time for me, I recommend acceptance without revision.

Reviewer: 2

 This is a fantastic and much needed piece that deserves to be published widely. ……….The authors clearly state this upfront: ‘academics wish to understand whether particular activities influence various audiences’. I command the authors for this rare instance of honesty and for aiming to publish this manuscript with the best academic journals in their discipline. The manuscript is limpid and very well written. The style is engaging and the results significant for the wider academic community. I fully support its publication.

 

These last nine months working on the paper were personally very rewarding and to me, a vindication that becoming a blogger was a good decision.  It was also a huge buzz to work with such a dynamic group of bloggers.  I think Steve sums it up for all of us in this Tweet

If you are not yet a science community blogger or don’t think that they have a place in mainstream science, please take the time to read our paper which you can find here.  It won’t cost you anything but time 🙂 and if any reporters are reading this – here courtesy of Manu, is our press release.

Blogs are no longer simply online personal journals. We define an overlooked category of blogs that holds immense value for the scientific community: science community blogs are written by practising scientists for scientists. As academics and active bloggers, we use data from our own blogs to show how science community blogs are a valuable outreach and professional development tool. Blogs are also a citable primary source with potential to contribute to scientific knowledge. It’s time for blogs to be accepted as a standalone medium with huge benefits for individual scientists and the science community as a whole.   

 

Post script

If you want to know what my fellow authors thought about our collaboration you can find Manu’s story here, Steve’s here, Amy and Terry’s here and Meghan’s here.