Tag Archives: aphids

Aphids don’t suck sap! (usually)

Aphids are sap feeding, most of the time they feed from the phloem, or sieve elements, that part of the plant responsible for transporting the food made in the leaves by photosynthesis, around the plant.  Aphids face three problems arising from their phloem feeding habit. First, the phloem sap is largely composed of sugars, with a few trace elements and nitrogen in the form of soluble amino acids.  The aphids are mainly interested in the nitrogen and that poses the second problem, the amino acids are mainly non-essential ones.  Thirdly, the phloem is under pressure, figures range from 2 to 40 Bars* (about twice to forty times atmospheric pressure) (e.g. Mittler, 1957; Rogers & Peel, 1975; Barlow & Randall, 1978; Wright & Fisher, 1980).  Imagine that you are trapped in an air-tight room and your only source of air is an inflated tractor tyre.   You have a sharp metal straw which you can stick into the tyre to release the air into your mouth.  If you put one end of the straw in your mouth and then pierced the tyre wall, your head would explode.

Sadly I couldn’t find a picture of an exploding aphid and my cartoon version was a failure, so this is it 🙂

Aphids face the same sort of pressure. Fortunately evolution has provided them with a very strong pharyngeal pump and incorporated a series of valves in their mouth-parts (stylets = straw) with which they are able to control the flow of the phloem into their bodies.  The last thing they want to do when plugged into the phloem is suck, it would be the last thing they did 🙂 and that’s why aphidologists get upset when people describe aphids as sap-suckers!

 

Aphid feeding apparatus – adapted from McLean & Kinsey (1984)

To be fair, we are being somewhat pedantic, the fluid transported in the xylem tubes, largely water, is also colloquially known as plant sap. The xylem, unlike the phloem is not under pressure (Sperry et al., 1996), so on those rare occasions when the aphid does need to drink water, they do have to suck sap (Spiller et al., 1990).  The other occasion on which aphids need to suck rather than regulate the flow of sap is when they are feeding in very artificial laboratory situations, on leaf discs or on artificial diets where the nutrient solution is between two pieces of Parafilm™.  In both these cases there is negative pressure and the cibarial pump does then come into operation. Interestingly, it is sometimes quite difficult to get aphids to feed on artificial diets unless a phagostimulant is included to overcome their reluctance to feed on sap that is not under pressure (Mittler & Dadd, 1963), but that’s a story for a future post.

Aphids feeding on leaf discs, in this case for insecticide assays at Rothamsted Research

 

Aphids feeding on artificial diet through Parafilm™. Photo Meena Haribal https://www.sciencedaily.com/releases/2015/12/151216151742.htm

 

References

Barlow, C.A. & Randolph, P. A.  (1978) Quality and quantity of plant sap available to the pea aphid.  Annals of the Entomological Society of America, 71, 46-48.

McLean, D.L. & Kinsey, M.G. (1984) The precibarial valve and its role in the feeding behavior of the pea aphid, Acyrthosiphon pisum. Bulletin of the Entomological Society of America, 30, 26-31.

Mittler, T.E. (1957) Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) (Homoptera, Aphididae) I. The uptake of phloem sap. Journal of Experimental Biology, 34, 334-341.

Mittler, T.E. & Dadd, R.H. (1963) Studies on the artificial feeding of the aphid Myzus perslcae (Sulzer) – I. Relative uptake of water and sucrose solutions. Journal of Insect Physiology, 9, 623-645.

Sperry, J.S., Saliendra, N.Z., Pockman, W.T.,  Cochard, H., Cruiziat, P., Davis, S.D., Ewers, F.W. & Tyree, M.T. (1996) New evidence for large negative xylem pressures and their measurement by the pressure chamber method. Plant, Cell & Environment, 19, 427-436.

Rogers, S. & Peel, A.J. (1975) Some evidence for the existence of turgor pressure gradients in the sieve tubes of willow Planta (Berl.) 126, 259-267.   

Spiller, N.J., Koenders, L. & Tjallingii, W.F. (1990) Xylem ingestion by aphid – a strategy for maintaining water balance.  Entomologia experimentalis et applicata, 55, 101-104.

Wright, J.P. & Fisher, D.P. (1980) Direct measurement of sieve tube turgor pressure using severed aphid stylets. Plant Physiology, 65, 1133-1135.

 

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The Natural World in Haiku Form – Volume 2

Nature versified.

Haikus from the year gone by

To enjoy or not.

 

Cryptic and not

Grasshoppers blend in;

 Busy ants don’t care at all

 If you see them there

17th August 2018 Vinca

 

Ants

Mountainous thunder

Sends ants scuttling to their nest.

Seeds await the wind

 

Ants again – Reverse Haiku

Ants, sensing distant thunder,

Scuttle to their nest,

While seeds pods wait for the wind.

22nd May 2018 Vinca

 

Aphids

 

Aphids are so cool.

Three generations, making

One clonal body

25 December 2017

 

Raucous Rooks

Starkly black on blue.

Rudely cawing rooks disturb

My morning coffee

15 February 2018

 

Raucous rooks railing.

Sable, swooping, skyward sailing,

Disturb my morning

26th February 2018

 

Mountain

Sunny Canigou,

Snowy peak shining brightly.

Winter in Vinca

20th January 2018

 

Malham Tarn

Rising from the rain

Summer mist, slowly rolling,

Hides Malham Tarn

July 16th 2018

 

Prunella

Commonly overlooked,

 Elastically plastic;

Purple Prunella

July 17th 2018

 

Four Brothers?

Four trees in a row
Standing smallest to tallest.
What is their story?

August  20th 2018, Vinca

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Global Insect Extinction – a never ending story

I have had an unexpectedly busy couple of weeks talking about declines in insect populations.  Back in November of last year I wrote a blog about the sudden media interest in “Insect Armageddon” and followed this up with a more formal Editorial in Annals of Applied Biology at the beginning of the year (Leather, 2018).  I mused at the time if this was yet another media ‘storm in a teacup’ but it seems that the subject is still attracting attention.  I appeared on television as part of TRT World’s Roundtable programme and was quoted quite extensively in The Observer newspaper on Sunday last talking about insect declines since my student days 🙂 At the same time, as befits something that has been billed as being global, a similar story, featuring another veteran entomologist appeared in the New Zealand press.

The TV discussion was quite interesting, the panel included Nick Rau from Friends of the Earth, Lutfi Radwan, an academic turned organic farmer, Manu Saunders from Ecology is Not a Dirty Word and me.  If they had hoped for a heated argument they were out of luck, we were all pretty much in agreement; yes insects did not seem to be as abundant as they had once been, and this was almost certainly a result of anthropogenic factors, intensive agriculture, urbanisation and to a lesser extent climate change.  Unlike some commentators who firmly point the finger at the use of pesticides as the major cause of the declines reported, we were more inclined to towards the idea of habitat degradation, fragmentation and loss.  We also agreed that a big problem is a lack of connection with Nature by large sections of the population, and not just those under twenty.  We also felt very strongly that governments should be investing much more into research in this area and that we desperately need more properly replicated and designed long-term studies to monitor the undeniable changes that are occurring.  I had, in my Editorial and an earlier blog post, mentioned this point and lamented the paucity of such information, so was pleasantly surprised, to receive a couple of papers from Sebastian Schuh documenting long-term declines in Hemiptera and Orthoptera in Germany (Schuh et al., 2012ab), although of course sad, to see yet more evidence for decreasing insect populations.

The idea that insects are in terminal decline has been rumbling on for some time; more than a decade ago Kelvin Conrad and colleagues highlighted a rapid decline in moth numbers (Conrad et al., 2006) and a few years later, Dave Brooks and colleagues using data from the UK  Environmental Change Network revealed a disturbing decline in the numbers of carabid beetles across the UK (Brooks et al., 2012).   In the same year (2012) I was asked to give a talk at a conference organised by the Society of Chemical Industry. Then, as now, I felt that pesticides were not the only factor causing the biodiversity crisis, but that agricultural intensification, habitat loss and habitat degradation were and are probably more to blame.  In response to this quote in the media at the time:

“British Insects in Decline

Scientists are warning of a potential ecological disaster following the discovery that Britain has lost around 7% of its indigenous insect species in just under 100 years.

A comparison with figures collected in 1904 have revealed that around 400 species are now extinct, including the black-veined white butterfly, not seen since 1912, the Essex emerald moth and the short-haired bumblebee. Many others are endangered, including the large garden bumblebee, the Fen Raft spider, which is only to be found in a reserve on the Norfolk/Suffolk border, and the once common scarlet malachite beetle, now restricted to just three sites.

Changes to the insects’ natural habitats have been responsible for this disastrous decline in numbers. From housing and industrial developments to single-crop farming methods, Britain’s countryside has become increasingly inhospitable to its native insects.”

I chose to talk about “Forest and woodland insects: Down and out or on the up?” I used data from that most valuable of data sets, the Rothamsted Insect Survey to illustrate my hypothesis that those insects associated with trees were either doing better or not declining, because of increased tree planting over the last fifty years.  As you can see from the slides from my talk, this does indeed seem to be the case with moths and aphids that feed on trees or live in their shade.  I also showed that the populations of the same species in northern Britain, where agriculture is less intensive and forests and woodlands more prevalent were definitely on the up, and this phenomenon was not just confined to moths and aphids.

Two tree aphids, one Drepanosiphum platanoidis lives on sycamore, the other Elatobium abietinum, lives on spruce trees; both are doing rather well.

Two more tree-dwelling aphids, one on European lime, the other on sycamore and maples, both doing very well.  For those of you unfamiliar with UK geography, East Craigs is in Scotland and Newcastle in the North East of England, Hereford in the middle and to the west, and Starcross in the South West, Sites 2, 1, 6 and 9 in the map in the preceding figure.

Two conifer feeding moth species showing no signs of decline.

On the up, two species, a beetle, Agrilus biguttatus perhaps due to climate change, and a butterfly, the Speckled Wood Pararge aegeria, due to habitat expansion and climate change?

It is important however, to remember that insect populations are not static, they vary from year to year, and the natural fluctuations in their populations can be large and, as in the case of the Orange ladybird, Halyzia sedecimguttata, take place over a several years, which is yet another reason that we need long-term data sets.

The Orange ladybird Halyzia sedecimguttata, a mildew feeder, especially on sycamore.

It is obvious, whether we believe that an ecological catastrophe is heading our way or not, that humans are having a marked effect on the biodiversity that keeps our planet in good working order and not just through our need to feed an ever-increasing population.  A number of recent studies have shown that our fixation with car ownership is killing billions of insects every year (Skórka et al., 2013; Baxter-Gilbert et al.,2015; Keilsohn et al., 2018) and that our fear of the dark is putting insects and the animals that feed on them at risk (Eccard et al.,  2018; Grubisic et al., 2018).  We have a lot to answer for and this is exacerbated by our growing disconnect from Nature and the insidious effect of “shifting baselines” which mean that succeeding generations tend to accept what they see as normal (Leather & Quicke, 2010, Soga & Gaston, 2018) and highlights the very real need for robust long-term data to counteract this dangerous and potentially lethal, World view (Schuh, 2012; Soga & Gaston, 2018).  Perhaps if research funding over the last thirty years or so had been targeted at the many million little things that run the World and not the handful of vertebrates that rely on them (Leather, 2009), we would not be in such a dangerous place?

I am, however, determined to remain hopeful.  As a result of the article in The Observer, I received an email from a gentleman called Glyn Brown, who uses art to hopefully, do something about shifting baselines.  This is his philosophy in his own words and pictures.

 

References

Baxter-Gilbert, J.H., Riley, J.L., Neufeld, C.J.H., Litzgus, J.D. & Lesbarrères, D.  (2015) Road mortality potentially responsible for billions of pollinating insect deaths annually. Journal of Insect Conservation, 19, 1029-1035.

Brooks, D.R., Bater J.E., Clark, S.J., Monteith, D.T., Andrews, C., Corbett, S.J., Beaumont, D.A. & Chapman, J.W. (2012)  Large carabid beetle declines in a United Kingdom monitoring network increases evidence for a widespread loss in insect biodiversity. Journal of Applied Ecology, 49, 1009-1019.

Conrad, K.F., Warren. M.S., Fox, R., Parsons, M.S. & Woiwod, I.P. (2006) Rapid declines of common, widespread British moths provide evidence of an insect biodiversity crisis. Biological Conservation, 132, 279-291.

Eccard, J.A., Scheffler, I., Franke, S. & Hoffmann, J. (2018) Off‐grid: solar powered LED illumination impacts epigeal arthropods. Insect Conservation & Diversity, https://onlinelibrary.wiley.com/doi/full/10.1111/icad.12303

Estay, S.A., Lima, M., Labra, F.A. & Harrington, R. (2012) Increased outbreak frequency associated with changes in the dynamic behaviour of populations of two aphid species. Oikos, 121, 614-622.

Grubisic, M., van Grunsven, R.H.A.,  Kyba, C.C.M.,  Manfrin, A. & Hölker, F. (2018) Insect declines and agroecosystems: does light pollution matter? Annals of Applied Biology,   https://onlinelibrary.wiley.com/doi/full/10.1111/aab.12440

Keilsohn, W., Narango, D.L. & Tallamy, D.W. (2018) Roadside habitat impacts insect traffic mortality.  Journal of Insect Conservation, 22, 183-188.

Leather, S.R. (2009) Taxonomic chauvinism threatens the future of entomology. Biologist, 56, 10-13.

Leather, S.R. (2018) “Ecological Armageddon” –  more evidence for the drastic decline in insect numbers. Annals of Applied Biology, 172, 1-3.

Leather, S.R. & Quicke, D.J.L. (2010) Do shifting baselines in natural history knowledge therten the environment? The Environmentalist, 30, 1-2.

Schuh, S. (2012) Archives and conservation biology. Pacific Conservation Biology, 18, 223-224.

Schuh, S., Wesche, K. & Schaefer, M. (2012a) Long-term decline in the abundance of leafhoppers and planthoppers (Auchenorrhyncha) in Central Europe protected dry grasslands. Biological Conservation, 149, 75-83.

Schuh, S., Bock, J., Krause, B., Wesche, K. & Scgaefer, M. (2012b) Long-term population trends in three grassland insect groups: a comparative analysis of 1951 and 2009. Journal of Applied Entomology, 136, 321-331.

Skórka, P., Lenda, M., Moroń, D., Kalarus, K., & Tryjanowskia, P. (2013) Factors affecting road mortality and the suitability of road verges for butterflies. Biological Conservation, 159, 148-157.

Soga, M. & Gaston, K.J. (2018) Shifting baseline syndrome: causes, consequences and implications. Frontiers in Ecology & the Environment, 16, 222-230.

 

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Entomological classics – Aphids spit: visualising aphids feeding, the electrical penetration graph

Aphids as a taxonomic group, have been recognised since at least 1758 when Linnaeus coined the genus Aphis and have been cited as important pests for more than 200 years “The Aphis or Blighter, as we now for the first time venture to call it, from its being the most general cause of what are termed blights in plants..” (Curtis, 1802).  A detailed understanding of how they fed, was however, longer in being reached, but by 1914 the anatomy of the aphid mouthparts and the process of stylet insertion was fully described (Davidson, 1914).  Davidson (1923) also described the role that aphid saliva plays in helping the aphid feed by making it easier for the stylet to move between cells on its convoluted journey to the phloem, made visible as the so-called stylet tracks.

Drawings showing the effects produced by the passage of aphid stylets of three different aphid species through leaf tissue (Davidson, 1923).

Fast forward a couple of years and we have intrepid entomologists producing photographic evidence of aphid stylets in action (Smith, 1926).

Photomicrographs of the stylet of Myzus persicae in situ and the resultant stylet track (Smith, 1926).

One of the reasons that applied entomologists were so interested in aphid feeding was the role that aphids, and other insects, played as vectors of plant viruses, which until the 1920s, was not formally proven (e.g. Kunkel, 1926, Smith, 1926, 1929). You would be forgiven for thinking that once the connection between aphid feeding and plant virus transmission had been demonstrated then that would be it.  But no, much wants more, and aphidologists became intrigued about the link between aphid feeding and salivation, in particular when and exactly where these activities occurred in the plant.  Those entomologists working on plant viruses wanted to know which part of the feeding process was linked to the acquisition and inoculation of the viruses from and to the aphid host plant.  A possible solution to these conundrums, was, however, on the horizon.

In the early 1960s, two entomologists from the Department of Entomology, at the University of California, Davis, Donald McLean and Marvin Kinsey,  came up with a system that was to revolutionise the study of the feeding behaviour of aphids and other insects that feed internally on plant using piercing mouthparts (McLean & Kinsey, 1964). In essence, what they did was to make an aphid part of an electrical circuit by attaching a thin copper wire to its back using a quick-drying silver paint.  The feeding substrate, a leaf, had a 2.0 Volt, 60-cycle alternating current introduced to it and this was placed on an insulated grid connected to an amplifier connected in parallel with an oscilloscope, a chart-recorder and a speaker. The wire attached to the aphid, was joined to the grid and when the aphid began to feed this completed the circuit, and changes in voltage were able to be observed and recorded.  The next step was to identify which chart recordings were associated with sap ingestion and salivation by the aphid.  Using an artificial leaf, Parafilm stretched over a well containing a sucrose solution, and watching the aphids under a high power microscope, these innovative entomologists were able to identify four different stages involved in aphid feeding (Mclean & Kinsey, 1965).

The ground-breaking chart recording (Mclean & Kinsey, 1965) and as you might expect it was a pea aphid 🙂

 

A visual summary of what McLean and Kinsey were watching and recording (from Dixon (1973).

Not satisfied with these findings McLean and Kinsey modified their equipment and intensified their observations, sacrificing a number of aphids in the process.  When different waveforms were seen the poor aphids had their stylets amputated and the plant material with the stylet still in place was then examined under a high power microscope.  This meant that they were able to definitively correlate their recordings with the position of the stylet in different leaf tissues and during different behaviours (McLean & Kinsey, 1967).  As well as trying to understand how, when and where plant viruses were acquired or transmitted, it turns out that using the waveforms generated by the aphid mouthparts as they weave their way through the leaf tissues, is not only a useful way of assessing the resistance mechanism of a plant (e.g. Nielson & Don, 1974; Paul et al., 1996; ten Broeke et al., 2016) but also for detecting resistance to insecticides (e.g. Garzo et al., 2016).

Modifications to the original equipment happened very quickly; by 1966, a more compact and easier to use version using Direct Current had been developed (Schaefers, 1966). That said, the first correlation of a specific waveform and virus acquisition by the pea aphid, was shown using the original AC equipment (Hodges & Mclean, 1969).  A further modification of the Schaefers DC equipment was developed during the 1970s, such that test aphids were able to live and reproduce for up to ten days whilst attached to the set-up, thus allowing very detailed investigation of the correlations between the electrical signal patterns produced and the feeding behaviours of the aphids (Tjallingii, 1978).

Those of you who take note of such things, will have noticed, that so far, some 14-years after its invention, the term electrical penetration graph has not yet appeared, either here or in the scientific literature.   Earlier references to recordings using the technique use the term actograph which was somewhat non-specific, as it refers to any graphical representation of behavioural activity.  So when did the term Electrical Penetration Graph (EPG) first appear in the literature.  Google Scholar gave me a date of 1984 from a paper looking at the resistance of lettuce to the cabbage aphid Brevicoryne brassicae, a paper that includes Freddy Tjallingii in the authorship list (Mentink et al., 1984).  In this paper the authors refer to a conference proceedings paper (Tjallingii, 1982) as being the source of the name.  On tracking down that paper I found that it doesn’t actually mention the term EPG.  The first paper that specifically mentions and defines the term as “the recorded graph as a result of an overall electrical signal caused by stylet penetration activities” is Tjallingii (1985).  Strangely the author introduces the term thus “Here we introduce the term ‘electrical penetration graph (EPG)”, which I found slightly odd as it is a single author paper 😊  Inputting EPG or electrical penetration graph into Web of Science shows an increasing number of papers using and mentioning the technique, but surprisingly the first paper recorded is from 1999.

NGram finds the first mention slightly earlier, 1981.  A puzzle waiting to be solved for anyone with the time or inlcination.

The frequency of the occurrence of the phrase “Electrical penetration graph” according to Ngram Viewer (accessed and downloaded May 1st 2018).

The technique is now very well established and used around the world.  The equipment is commercially available through EPG Systems, which is where we got ours from and just in case you were wondering, this is what it looks like.

Faraday Cage (an earthed metal screen) surrounding the equipment to exclude electrostatic and electromagnetic influences

Our test plants in situ connected up to the electrical supply, recording equipment and amplifier.

Close up of the plants and EPG electrodes

Aphids connected up to the EPG. Photo courtesy of https://sites.google.com/site/ezwear1/epgIMG_0903.jpg

A simple guide to interpreting the waveforms

http://www.epgsystems.eu/file/46-waveform-features

For Open Days and public displays it is not unknown for mischievous entomologists to link particular waveforms to recordings of sucking and spitting sounds and to play these back when the equipment is being demonstrated 🙂

 

References

Curtis, W.L. (1802) IV. Observations on aphides, chiefly intended to show that they are the principal cause of blights in plants, and the sole cause of the honeydewTransactions of the Linnaean Society of London, 6, 75-94.

Davidson, J. (1914) On the mouth-parts and mechanism of suction in Schizoneura lanigera, Hausmann. Zoological Journal of the Linnaean Society, 32, 307-330.

Davidson, J. (1923) Biological studies of Aphis rumicis Linn. The penetration of plant tissues and the source of the food supply of aphids.  Annals of Applied Biology, 15, 35-54.

Gabrys, B., Tjallingii, W.F. & van Beek, T.A. (1997) Analysis of EPG recorded probing by cabbage aphid on host plant parts with different glucosinolate contents. Journal of Chemical Ecology, 23, 1661-1673.

Garzo, E., Moreno, A., Hernando, S., Marino, V., Torne, M., Santamaria, E., Diaz, I. & Fereres, A. (2016) Electrical penetration graph technique as a tool to monitor the early stages of aphid resistance to insecticides. Pest Management Science, 72, 707-718.

Hodges, L.R. & McLean, D.L. (1969) Correlation of transmission of Bean Yellow Mosaic Virus with salivation activity of Acyrthosiphon pisum (Homoptera: Aphididae). Annals of the Entomological Society of America, 62, 1398-1401.

Kunkel, L.O. (1926) Studies on Aster Yellows. American Journal of Botany, 13, 646-705.

McLean, D.L. & Kinsey, M.G. (1964) A technique for electronically recording aphid feeding and salivation. Nature, 202, 1358-1359.

McLean, D.L. & Kinsey, M.G. (1965) Identification of electrically recorded curve patterns associated with aphid salivation and ingestion. Nature, 205, 1130-1131.

McLean, D.L. & Kinsey, M.G. (1967) Probing behavior of the pea aphid, Acyrthosiphon pisum. I. Definitive correlation of electronically recorded waveforms with aphid probing activitiesAnnals of the Entomological Society of America, 60, 400-405.

Mentink, P.J.M., Kimmins, F.M., Harrewijn , P., Dieleman, F.L., Tjallingii, W.F.,  van Rheenen, B. &  Eenink, A.H. (1984)  Electrical penetration graphs combined with stylet cutting in the study of host plant resistance to aphids. Entomologia experimentalis et applicata, 35, 210-213.

Nielson, M.W. & Don, H. (1974) Probing behaviour of biotypes of the spotted alfalfa aphid on resistant and susceptible and alfalfa clones.  Entomologia experimentalis et applicata, 17, 477-486.

Paul, T.A., Darby, P., Green, C.P., Hodgson, C.J. & Rossiter, J.T. (1996) Electrical penetration graphs of the damson-hop aphid, Phorodon humuli on resistant and susceptible hops (Humulus lupulus).  Entomologia expeimentalis et applicata, 80, 335-342.

Powell, G. (1991) Cell membrane punctures during epidermal penetrations by aphids: consequences for the transmission of two potyviruses. Annals of applied Biology, 119, 313-321.

Schaefers, G.A. (1966) The use of direct current for electronically recording aphid feeding and salivation. Annals of the Entomological Society of America, 59, 1022-1024.

ten Broeke, C.J.M., Dicke, M. & van Loon, J.J.A. (2016) Feeding behaviour and performance of Nasonovia ribisnigri on grafts, detached leaves, and leaf disks of resistant and susceptible lettuce.  Entomologia experimentalis et applicata, 159, 102-111.

Tjallingii, W.F. (1978) Electronic recording of penetration behaviour by aphids. Entomologia experimentalis et applicata, 24, 521-530.

Tjallingii, W.F. (1982) Electrical recording of aphid penetration. [In] J.H. Visser & A.K. Minks (eds.) Proceedings of the 5th Symposium on Insect Plant-Relationships, 1-4 March, 1982, Wageningen, Pudoc, pp 409-410.

Tjallingii, W.F. (1985) Electrical nature of recorded signals during stylet penetration by aphids. Entomologia experimentalis et applicata, 38, 177-185.

Smith, K.M. (1926) A comparative study of the feeding methods of certain Hemiptera and of the resulting effects upon the plant tissue, with special reference to the potato plant. Annals of Applied Biology, 13, 109-139.

Smith, K.M. (1929) Studies on potato virus diseases, V. Insect transmission of potato leaf roll.  Annals of Applied Biology, 16, 209-229

 

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Not all aphids grow up to be aphids – the enemy within

It has been said that if aphids had their own way and unlimited resources the world as we know it would be 149 km deep in the cute little beasts (Harrington, 1994 ). Last year I wrote about how predators that feed on aphids, although useful, don’t really cut the mustard when it comes to keeping them in check and suggested that their host plants played a major role in keeping aphids from taking over the World.  While they do play an important part in keeping aphid populations under control, and are aided and abetted by aphid specific predators, there are, however, some much more efficient aphid-specific natural enemies out there.  They may be less conspicuous than the brightly coloured ladybirds that we often see munching their way through aphid colonies; public perception of their name may make people wince, but these beautiful and graceful creatures make sure that our appetite for salads and exotic vegetables out of season is satisfied safely and efficiently.  Their life cycles rival that of their prey, or should that be hosts, and entomologists fondly imagine that the film Alien was inspired by them 😊

I am, of course, talking about parasitic wasps, or parasitoids as they are more commonly known.  They are called parasitoids because unlike true parasites which generally speaking keep their hosts alive, insect victims of these wasps will, if successfully parasitized, die well before their non-parasitized relatives. In case you were wondering, the term parasitoid was coined by the Finnish Hemipterist, Odo Reuter (1913).  Aphids are not the only insects that are attacked by parasitoid wasps. The action of insect parasites has been known about for over two hundred years.  Erasmus Darwin, grandfather of the more famous Charles, noted that Ichneumonid wasps parasitised cabbage white butterfly caterpillars and so should be encouraged by gardeners (Darwin, 1800).  This is not the only early mention of parasitic insects in this context; Wheeler (1928), points out that back in the 1850s, two Italian entomologists, Camillo Rondani and Vittore Ghiliana also suggested the use of parasitic insects as biological control agents.  Aphid pests of glasshouse crops originally controlled mainly by predators (van Lenteren & Woets, 1988) are now routinely controlled by the application of commercially produced Braconid and Chalcid wasps (Boivin et al., 2012; van Lenteren, 2012).

Three commonly used aphid parasitoid biological control agents in action. Images from http://biologicalservices.com.au/products/aphelinus-2.html and https://www6.inra.fr/encyclopedie-pucerons/Especes/Parasitoides/Braconidae-Aphidiinae/Praon-volucre

When people think of Hymenoptera, they tend to think of bees, Vespid wasps and ants as being the most important and abundant.  They are very much mistaken.  The Parastica, or parasitoid wasps, are, by a huge margin, the most speciose and abundant section of

Parasitoids clearly dominate the Hymenopteran fauna of the British Isles (Many thanks to Natalie Dale-Skey of the NHM for permission to use this).

the Hymenoptera both in the UK and elsewhere

In the tropics the parasitoids are even more dominant. Data from Gaston et al., (1996).

Once parasitized, the egg(s), unless they are encapsulated by the aphid ‘immune’ system, hatch and begin to feed on the internal tissues of their, presumably, unsuspecting aphid host.  The parasitoid larvae avoid feeding on vital parts of the aphid, so that it can continue to grow and develop and provide food for the parasitoid, until the parasitoid is ready to pupate. Once the parasitoid is ready to pupate it delivers the coup de grace putting the aphid out of its misery and allowing the formation of the ‘mummy’ in

The three most common types of aphid mummies.  Images from http://resources.rothamsted.ac.uk/science-stories/aphids-mummies-and-cadavershttp://biologicalservices.com.au/products/aphelinus-2.html and https://farm1.static.flickr.com/327/18532751584_becc0e56e9_b.jpg respectively.

which the parasitoid completes its development before sawing its way out to emerge as a winged adult ready to seek out new hosts, leaving a characteristic neat circular hole in mummy case. In case you were wondering why the mummy of Praon volucre looks like it is sitting on a plate, this because, unlike the other aphid parasitoids, the final instar cuts its way out of the bottom of the aphid and spins its cocoon externally underneath the remnants of the aphid, hence the ‘plate’ (Beirne, 1942).

And out she comes; emerging parasitoid – http://resources.rothamsted.ac.uk/science-stories/aphids-mummies-and-cadavers

 

Lysiphelbus testaceipes  Photo by J.K.Clark, University of California Statewide IPM Project

Once an aphid, now a hollow mummy; note the neat emergence holes.  Aphid parasitoids are very much tidier than the parasitic lifeform in the classic film Alien 🙂

Another aspect of their life style that makes parasitoids a breed apart from true parasites, is that as well as using aphids as egg laying sites for their larvae, the adults like to snack on them every now and then to help mature more eggs and to keep up their energy levels; sometimes quaintly described as predatism (Flanders, 1953).  Although the parasitoids can make feeding attacks at any time, they appear to feed first and then start laying their eggs (e.g. Collins et al., 1981).

Parasitoids are widely used as biological control agents in glasshouses and other protected environments as they are generally regarded as being more effective than predators (Debach & Rosen, 1991), although there is some support that generalist predators can play a significant part in biological control in the wider environment (Symondson et al., 2002; Gontijo et al., 2015).  That said, aphid parasitoids seem to be fairly host specific in that commercial companies offer specific parasitoid mixtures to control different aphid pest species e.g.  https://www.koppert.com/pests/aphids/product-against/aphipar/ [Note this is NOT an endorsement]. In fact it has been suggested that the relationship between aphids and their parasitoids can be used to clarify aphid taxonomic relationships (Mackauer, 1965). On the other hand, there are very few examples of monophagous aphid parasitoids, most being described as oligophagous (Stary & Rejmanek, 1981).   So given that there is a fair bit of evidence that the parasitoids attacking aphids do show some discrimination in their choice of hosts, how do they find them?

Parasitoids in general were originally thought to be “possessed of an unerring instinct that guided them in their search for hosts” but Cushman (1926) rebutted this idea pointing out that actually the parasitoids first home in on the habitat or food plant that their host lives in and then search for their host (Laing, 1937).   The parasitoids referred to by Cushman and Laing, are however, not parasitoids of aphids, attacking lepidopteran leaf miners and carrion feeding flies respectively, so you might perhaps think that aphid parasitoids could have a different strategy. Although habitat selection by parasitoids of lepidopteran larvae (Thorpe & Caudle, 1938) and sawfly larvae (Monteith, 1955), using olfactory cues of their host’s food plant was confirmed readily easily and early on, the situation with aphids was less clear cut. Manfred Mackauer for example, suggested that aphid parasitoids might be using visual cues, such as leaf deformities or damage to find their aphids hosts (Mackauer, 1965).  The breakthrough came when three cabbage loving entomologists from the USA used an olfactometer to first show that the Braconid parasitoid Diaeretiella rapae, responded positively to the odour of collards (what we in the UK call spring greens) and second to show a very strong preference for them to lay their eggs in the aphid Myzus persicae when it was feeding on crucifers rather than other host plants.  They attributed this to the presence of mustard oil, the chemical that gives cabbages their distinctive taste and suggested that once the aphid host plant was found then the parasitoids used visual cues to find their aphid victims (Read et al., 1970).  Six years later it was firmly established that parasitoids in general used olfactory cues both to locate the habitat of their host (long-range) and then a short-range to find and confirm the identity (contact chemicals) their insect hosts (Vinson, 1976).

It was thought that the aphid parasitoids were chemically ‘conditioned’ during their larval life within the aphid feeding on a host plant and that this influenced their adult host preferences (e.g. Sheehan & Shelton, 1989; Wickremasinghe & Van Emden, 1992).  These, and other similar results, seemed to support the Hopkins host selection principle (Hopkins, 1917) which states that adult preferences are learnt as larvae.  A very neat experiment by van Emden et al., (1996) proved this hypothesis wrong. They transferred aphid mummies from the plant on which they had been parasitized on to another host plant and this changed the preference of the emerging adult, seeming to suggest that this was how aphid parasitoids developed their host preferences.  Now comes the neat, and very tricky part; if however, the parasitoid pupae were removed (very carefully) from the mummy case and reared to adulthood in the absence of a host plant or mummy and kept in a glass tube, the emerging adults showed no preference for particular host plants, clearly showing that adult preferences were  not determined during larval development but ‘conditioned’ by exposure to the external skin of the aphid mummy on emergence (van Emden et al., 1996).  Using aphids reared on an artificial diet (Douloumpaka & van Emden, 2003) showed that the it was very likely that the mother parasitoid leaves a chemical cue in or around the egg(s) she lays and that this is later incorporated into the silk of the parasitoid pupa, thus inducing the host preference seen as an adult.

An additional twist to the story is that male and female parasitoids differ in their responses to odours.  Both sexes of Aphidius uzbekistanicus and A. ervi, parasitoids of cereal aphids in the UK, respond to plant odours, but only females respond to aphids (Powell & Zhi-Li, 1983).  Males of both species are, however, attracted to the odours of their respective females, suggesting the existence of a sex pheromone. The existence of a sex pheromone in aphid parasitoids had been suggested a few years earlier when it was shown that male D. rapae attempted to copulate with filter paper that had had female abdomens crushed on them (Askari & Alisha, 1979).  The existence of sex pheromones in aphid parasitoids has now been shown in several species (e.g. Decker et al., 1993; McNeil & Broduer, 1995).  Strangely, female parasitoids also respond to sex pheromones, but in their case, the sex pheromones of aphids.  It turns out that they ‘parasitise’ aphids in more than one way, they home in on their prey using the aphid sex pheromone and this enables them to find a suitable overwintering host (Hardie et al., 1991).  At other times of the year they also use other aphid indicators; several studies have shown that parasitoids use the presence of aphid honeydew to help them find their hosts (Budenberg, 1990; Bouchard & Cloutier, 1984; Gardner & Dixon, 1985).

Predators of aphids such as ladybirds use chemical markers to warn other ladybirds that they have laid eggs near aphid colonies, thus reducing the chances of cannibalism and competition (e.g. Oliver et al., 2006). Given that the eggs of aphid parasitoids are laid internally, they are in effect invisible, it would make sense if the parasitoids ‘marked’ their hosts in some way to avoid other parasitoids laying their eggs in an already parasitized aphid, superparasitism.  Sure enough, there is some evidence that some adult parasitoids can recognise aphids that already have larval parasitoids developing inside them although they don’t seem to be able to consistently recognise already parasitized aphids until some hours afterward (e.g. Cloutier et al., 1984).  In some cases, it seems that it is the aphid herself that prevents superparasitism by reacting more aggressively towards parasitoids after being attacked once (Gardner & Dixon, 1984) and also by the presence of dried siphuncular secretions on the aphid’s skin (Outreman et al., 2001).  The waxy secretion had an effect for up to a day or so after which the internal changes caused by the developing parasitoid larvae were enough to deter further oviposition attempts.

It is a good thing for the poor aphids that they have such a high reproductive rate, or they would truly be in dire straits.  On the other hand, as exemplified by the words of Jonathan Swift (1733),

“So naturalists observe, a flea
Has smaller fleas that on him prey;
And these have smaller still to bite ’em,
And so proceed ad infinitum

there are parasites of parasitoids, the hyperparasites, that help keep the numbers of parasitoids under control, and thus, indirectly, help aphids remain relatively abundant.

 

References

Askari, A. & Alisha, A. (1979) Courtship behavior and evidence for a sex pheromone in Diaeretiella rapae (Hymenoptera: Braconidae), the cabbage aphid primary parasitoid. Annals of the Entomological Society of America, 72, 79-750.

Beirne, B.P. (1942) Observations on the life-history of Praon volucre Haliday (Hym.: Braconidae), a parasite of the mealy plum aphis (Hyalopterus arundinis Fab.). Proceedings of the Royal Entomological Society of London, Series A, General Entomology, 17, 42-47.

Boivin, G., Hance, T. & Brodeur, J. (2012) Aphid parasitoids in biological control.  Canadian Journal of Plant Science, 92, 1-12.

Bouchard, Y. & Cloutier, C. (1984) Honeydew as a source of host-searching kairomones for the aphid parasitoid, Aphidius nigripes (Hymenoptera: Aphidiidae).  Canadian Journal of Zoology, 62, 1513-1520.

Budenberg, W.J. (1990) Honeydew as a contact kairomone for aphid parasitoidsEntomologia experimentalis et applicata, 55, 139-148.

Cloutier, C., Dohse, L.A. & Bauduin, F. (1984) Host discrimination in the aphid parasitoid Aphidius nigripes. Canadian Journal of Zoology, 62, 1367-1372.

Collins, M.D., Ward, S.A., & Dixon, A.F.G. (1981) Handling time and the functional response of Aphelinus thomsoni, a predator and parasite of the. Journal of Animal Ecology, 50, 479-487.

Cushman, R.A. (1926) Location of individual hosts versus systematic relation of hots species as a determining factor in parasitic attack. Proceedings of the Entomological Society of Washington, 28, 5-6.

Darwin, E. (1800) Phytologia: or The Philosophy of Agriculture and Gardening. P. Byrne, Grafton Street, London.

Debach, P. & Rosen, D. (1991) Biological Control by Natural Enemies, Cambridge University Press, New York.

Decker, U.M., Powell, W. & Clark, S.J. (1993) Sex pheromone in the cereal aphid parasitoids Praon volucre and Aphidius rhopalosiphiEntomologia experimentalis et applicata, 69, 33-39.

Douloumpaka, S. & van Emden, H.F. (2003) A maternal influence on the conditioning to plant cues of Aphidius colemani Viereck, parasitizing the aphid Mysuze persicae SulzerPhysiological Entomology, 28, 108-113.

Flanders, S.E. (1953) Predation by the adult Hymenopteran parasite and its role in biological control. Journal of Economic Entomology, 46, 541-544.

Gardner, S.M. & Dixon, A.F.G. (1984) Limitation of superparasitism by Aphidius rhopalosiphi: a consequence of aphid defensive behaviour. Ecological Entomology, 9, 149-155.

Gardner, S.M & Dixon, A.F.G. (1985) Plant structure and foraging success of Aphidius rhopalosiphi (Hymenoptera: Aphidiidae).  Ecological Entomology, 10, 171-179.

Gaston, K.J., Gauld, I.D. & Hanson, P. (1996) The size and composition of the hymenopteran fauna of Costa Rica.  Journal of Biogeography, 23, 105-113.

Griffiths, D.C. (1960) The behaviour and specificity of Monoctonus paldum Marshall (Hym., Braconidae), a parasite of Nasonovia ribis-nigbi (Mosley) on lettuce. Bulletin of Entomological Research, 51, 303-319.

Hardie, J., Nottingham, S.F., Powell, W. & Wadhams, L.J. (1991) Synthetic aphid sex pheromone lures female parasitoids.  Entomologia experimentalis et applciata, 61, 97-99.

Harrington, R. (1994) Aphid layer. Antenna18, 50-51.

Hopkins, A.D. (1917) Contribution to discussion.  Journal of Economic Entomology, 10, 92-93.

Holler, C. (1991) Evidence for the existence of a species closely related to the cereal aphid parasitoid Aphidius rhopalosiphi De Stefani-Perez based on host ranges, morphological characters, isoelectric focusing banding patterns, cross-breeding experiments and sex pheromone specificities (Hymenoptera, Braconidae, Aphidiinae. Systematic Entomology, 16, 15-28.

http://www.biologicalcontrol.info/aphid-primary-and-hyperparasitoids.html

Laing, J. (1937) Host-finding byinsect parasites 1. Observations on the finding of hosts by Alysia manducator, Mormoniella vitripennis and Trichogramma evanescensJournal of Animal Ecology, 6, 298-317.

Mackauer, M. (1965) Parasitological data as an aid in aphid classification. Canadian Entomologist, 97, 1016-1024.

McNeil, J.N. & Brodeur, J. (1995) Pheromone-mediated mating in the aphid parasitoid, Aphidius nigripesJournal of Chemical Ecology, 21, 959-972.

Monteith, L.G. (1955) Host preferences of Drino bohemica Mesn. (Diptera; Tachnidae) with particular reference to olfactory responses.  Canadian Entomologist, 87, 509-530.

Oliver, T.H., Timms, J.E.L., Taylor, A. & Leather, S.R. (2006) Oviposition responses to patch quality in the larch ladybird Aphidecta obliterata (Coleoptera: Coccinellidae): effects of aphid density, and con- and heterospecific tracks. Bulletin of Entomological Research, 96, 25-34.

Outreman, Y., Le Ralec, A., Plantegenest, M., Chaubet, B, & Pierre, J.S. (2001) Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability. Journal of Insect Physiology, 47, 339-348.

Powell, W. & Zhi-Li, Z. (1983) The reactions of two cereal aphid parasitoids, Aphidius uzbekistanicus and A. ervi to host aphids and their food-plants.  Physiological Entomology, 8, 439-443.

Reuter, O.M. (1913). Lebensgewohnheiten und Instinkte der Insekten (Berlin: Friendlander).

Stary, P. & Rejmanek, M. (1981) Number of parasitoids per host in different systematic groups of aphids: The implications for introduction strategy in biological control (Homoptera: Aphidoidea; Hymenoptera: Aphidiidae). Entomologica Scandinavica, Suppl. 15, 341-351.

Riley, W.A. (1931) Erasmus Darwin and the biologic* control of insects. Science, 73, 475-476.

Sheehan, W. & Shelton, A.M. (1989) The role of experience in plant foraging by the aphid parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae).  Journal of Insect Behavior, 2, 743-759.

Symondson, W.O.C., Sunderland, K.D., & Greenstone, M.H. (2002) Can generalist predators be effective bicontrol agents? Annual Review of Entomology, 47, 561-594.

Thompson, W.R. (1930) The principles of biological control. Annals of Applied Biology, 17, 306-338.

Thorpe, W.H. & Caudle, H.B. (1938) A study of the olfactory responses of insect parasites to the food plant of their host.  Parasitology, 30, 523-528.

Van Emden, H.F., Spongal, B., Wagner, E., Baker, T., Ganguly, S. & Douloumpaka, S. (1996) Hopkins’ ‘host selection principle’, another nail in its coffin.  Physiological Entomology, 21, 325-328.

Van Lenteren, J.C. (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl, 57, 1-20.

Van Lenteren, J.C. & Woets, J. (1988) Biological and integrated control in greenhouses.  Annual Review of Entomology, 33, 239-269.

Vinson, S.B. (1976) Host selection by insect parasitoids.  Annual Review of Entomology, 21, 109-133.

Wheeler, W.M. (1922). Social life among the insects: Lecture II. Wasps solitary and social. Scientific Monthly, 15, 68-88.

Wheeler, W.M. (1928) Foibles of Insects and Men.  Alfred Knopf, New York

Wickremasinghe, M.G.V. & Van Emden, H.F. (1992) Reactions of adult female parasitoids, particularly Aphidius rhopalosiphi, to volatile chemical cues from the host plants of their aphid prey. Physiological Entomology, 17, 207-304.

*This is how he spelt it; not a mistake on my part J

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Filed under Aphidology, Aphids

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 2nd, 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 persicaeEntomologia 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

 

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Prunella – mistress of plasticity

Now that I have your attention, this is not an article about soft porn or fetishes, but rather a paean for that humble ‘weed’ Prunella vulgaris – Self-heal, Heal all, Woundwort, Heart of the Earth and many other names, depending on where in the World you come from.   Prunella vulgaris is in the family Lamiaceae, so related to mints and dead-nettles.  It is an edible weed, the young leaves can be used in salads and it can also be used in soups, stews, or used whole and boiled as a pot herb.

The instantly (to me at any rate) recognisable flower of Prunella vulgaris

Prunella as I will now familiarly call her, has a very wide geographical native range and has also been introduced into South America where she does very well indeed (Godoy et al., 2011).

Distribution of Prunella vulgaris, blue native, brown introduced. http://powo.science.kew.org/taxon/urn:lsid:ipni.org:names:455176-1

 The name Prunella is derived from ‘Brunella’, a word which is itself a derivative, coming from the German name for quinsy, (a type of throat inflammation), die Braüne, which it was historically used to cure.  That is the other aspect of this glorious plant, it has many medicinal properties, hence the many common names refer to its healing powers, almost as many as Athelas of Lord of the Rings fame 😊  It was traditionally used in European herbal medicine for sore throats, fever reduction and like Athelas, for accelerating the healing of wounds (Matthiolus, 1626).  More recently it has become of interest as a possible cure for conditions associated with the herpes simplex virus (Psotováa et al., 2003) and inhibiting anaphylactic shock and other immediate type allergic reactions (Shin et al., 2001).  So truly a wonder drug, and again proving that “Old Wives Tales” are in many cases based on more than just superstition.

My interest in Prunella vulgaris, is however, based on its wondrous plasticity, as the three photographs below show nicely.  Depending on grazing (or mowing) pressure, Prunella can grow to reproductive maturity at heights  ranging from just over 2 cm to just under 30 cm. Truly remarkable.

I am of course, not the first person to be fascinated by this plasticity and the taxonomic and evolutionary ins and outs of this lovely plant (Nelson, 1965; Warwick & Briggs, 1979) but I still find it fascinating, and who knows, perhaps one day I might do some work on it myself 😊

The other thing that I like about Prunella is that she is also provides a living for aphids.  She has her own rare and specific one, Aphis brunellae, but is also kind enough to let a few other species make a living on her, Aphis gossypii, Aphis nasturtiiAulacorthum solani,  Macrosiphum euphorbiae, the ubiquitous Myzus persicae, M. ornatus and Ovatomyzus chamaedrys (Blackman & Eastop, 2006).

Aphis brunellae, rare in the UK – with thanks to the two Bobs for permission to use the photograph. http://influentialpoints.com/Images/Aphis_brunellae_colony_on_Prunella_vulgaris_c2015-08-21_15-37-27ew.jpg

 

Finally, you will have noticed that the Prunella aphid is A. brunellae, which is derived from the original name of Prunella (I guess Prunella Scales is happy, she could have been Brunella Scales).  Interestingly, her alter-ego was not removed until fairly recently, her tombstone is shown below.

References

Blackman, R.L. & Eastop, V.F. (2006) Aphids on the World’s Herbaceous Plants and Shrubs Volume 1 Host Lists and Keys.  Wiley, Oxford.

Godoy, O., Saldaña, A., Fuentes, N., Valladares, F. & Gianoli, E. (2011)  Forests are not immune to plant invasions: phenotypic plasticity and local adaptation allow Prunella vulgaris to colonize a temperate evergreen rainforest. Biological Invasions, 13, 1615-1625.

Matthiolus, P.A. (1626) Kräuterbuch.  Noringberg.

Nelson, A.P. (1965) Taxonomic and evolutionary implications of lawn races in Prunella vulgaris (Labiatae). Brittonia, 17, 160-174.

Psotová, J., Kolá, M., Sousek, J., Ívagera, Z., Vicar, J. &Ulrichová, J. (2003) Biological activities of Prunella vulgaris extract. Phytotherapy Research, 17, 1082-1087.

Shin, T.Y., Kim, Y.K. & Kim, H.M. (2001) inhibition of immediate-type allergic reactions by Prunella vulgaris in a murine model.  Immunopharmacology & Immunotoxicology, 23, 423–435.

Warwick, S.I. & Briggs, D. (1979) The genecology of lawn weeds III. Cultivation experiments with Achillea millefolium L., Bellis perennis L., Plantago lanceolata L., Plantago major L. and Prunella vulgaris L. collected from lawns and contrasting grassland habitats.  New Phytologist, 83, 509-536.

 

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Pick and mix 9 – a few links to click

Links to things I thought might grab your fancy

Interested in plants?  Find the latest State of the World’s Plants report here

Butterfly lovers?  Special issue of Journal of Insect Conservation devoted to butterfly conservation

Communicating entomology through video

Speaking of which, I did one on aphids once upon a time 🙂

How bees see may help us develop better cameras

How bumblebee flight may help us develop better drones

The Sixth Mass Extinction of vertebrates on the way but what about all the invertebrates that keep the world functioning?

Interesting article on insect symbolism in 19th Century British art

Weirdly interesting art based on the “natural world” by Katie McCann

This account of sexism in academia shocked and horrified m

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Not all aphid galls are the same

A galling experience – what on earth is an aphid-induced phytotoxemia?

Scientists, actually let me correct that, all members of specialist groups, be they plumbers or astrophysicists, love their jargon.  Insect-induced phytotoxemias is a great example. What entomologists and plant physiologists mean by this term is plant damage caused by an insect.  The visible damage that insects can cause to plants ranges from discolouration, lesions, and malformation of stems and leaves. As the title of this post suggests I am going to discuss galls.  Many insects produce galls, some of which can be spectacular such as Robin’s pin cushion gall caused by the wasp, Diplolepis rosae, but being a staunch aphidologist I am going to concentrate on various leaf deformities caused by aphids.

Robin’s pin cushion gall, caused by Diplolepis rosae.

https://upload.wikimedia.org/wikipedia/commons/9/93/Diplolepis-rosae.jpg

Aphids are true bugs, they are characterised by the possession of piercing and sucking mouthparts, the stylets, think of a hypodermic needle, being the piercing part of the mouthparts.

Aphid mouthparts, showing the passage of the stylets to the phloem (Dixon, 1973).

It was originally thought that the various leaf deformities resulting from aphid feeding was a direct result of the mechanical damage caused by the stylet entering the leaf and rupturing cell walls or possibly by the transmission of a disease. A series of elegant experiments by Kenneth Smith in the 1920s showed however, that insect salivary gland extracts were needed to cause the damage (Smith, 1920, 1926).  Puncturing leaves with needles did not produce the same symptoms.  The leaf rolls, leaf curls and pseudo-galls caused by aphids vary between species even when the aphids are closely related or their host plants are.  As an example of the latter, the bird cherry-oat aphid, Rhopalosiphum padi, causes what I would describe as a leaf roll, i.e. the leaves curl in from the edges towards the mid-rib, to make something that resembles a sausage.

Leaf roll pseudo-galls on bird cherry, Prunus padus, caused by the bird cherry oat aphid, Rhopalosiphum padi.

On the other hand, the cherry blackfly, Myzus cerasi, that has Prunus avium as its primary host, causes what I describe as leaf curls (think ringlets and curls in human hair terms), in that the leaf rolls up from the tip down towards the stalk (petiole).

Leaf curl on Prunus avium caused by the Chery black fly, Myzus cerasi

Similarly, there are two closely related aphid species, Dysaphis devecta and D. plantaginea, both feed on apple leaves, but D. devecta prefers to feed on the smaller veins while D. plantaginea prefers to feed on the mid-rib. The former causes a leaf-roll, the latter a leaf curl.

Dysaphis galls http://influentialpoints.com/Gallery/Dysaphis_devecta_species_group_rosy_leaf-curling_apple_aphids.htm

As well as leaf rolls and leaf curls, some aphids are able to induce leaf folds.  The poplar-buttercup gall aphid, Thecabius affinis being a good example.

Leaf fold on poplar caused by Thecabius affinis Poplar-buttercup gall aphid. Photo from the excellent Influential Points web site. http://influentialpoints.com/Gallery/Thecabius_affinis_Poplar-buttercup_gall_aphid.htm

You might think that it is the aphid feeding site that causes the characteristic roll, curl or fold, but if groups of D. devecta or D. plantaginea are caged on the stem of an apple seedling, young leaves several centimetres away will develop leaf rolls characteristic of each species suggesting that they are caused by specific substances in the saliva of each aphid (Forrest & Dixon, 1975).  Aphid saliva is known to contain a huge range of proteins from amino acids to digestive enzymes (Miles, 1999) so it is highly likely that different aphid species have evolved different suites of enzymes that enable them exploit their respective host plants more efficiently.  Entomologists who work on plant galls suspect that there is something in the saliva that makes the plant’s hormones trigger the gall formation, but they freely admit that they are still just guessing.  Leaf rolls and curls are pretty tame when you come to look at the galls some aphids can induce.  Aphids from the family Pemphigidae cause structural deformations that totally enclose them and their offspring.

Petiole galls caused by (left) Pemphigus spyrothecae (photo Graham Calow, http://warehouse1.indicia.org.uk/upload/med-p1771un6n510nt146ugosslt1hip5.jpg) and (right) Pemhigus bursarius gall (Photo Graham Calow http://www.naturespot.org.uk/species/pemphigus-bursarius)

Pemphigus populitransversus, the Cabbage root aphid or poplar petiole aphid (Photo Ryan Gott Ryan Gott‏ @Entemnein)

Not all enclosed galls are on petioles, the witch-hazel cone gall aphid (Hormaphis hamamelidis causes very distinctive galls on the leaves of its host plant.

Cone galls on witch hazel caused by Hormapahis hamamelidis http://www.inaturalist.org/photos/377819

So what is it with insect galls?  Are they of any use?  Peter Price and colleagues (Price et al., 1987) very succinctly summarised the four hypotheses that address the adaptive value of insect galls; a) No adaptive value (Bequaert, 1924), b) adaptive value for the plant (Mani, 1964), c) adaptive value for plant and herbivore (mutual benefit) (Cockerell, 1890) and d) adaptive value for the insect.  This last hypothesis is further subdivided into nutritional improvements, micro-environmental improvements and natural enemy protection (Price et al., 1987).

Becquaert’s non-adaptive hypothesis is and was easily and quickly dismissed (Price et al., 1987), so I will move swiftly on to the plant-protection hypothesis which Price et al., dismiss almost as swiftly.  In essence if galls are not associated with enhanced growth and survival of the galled plant then there is no protection offered.  In fact, galling insects have been used as biological control agents against weeds (e.g. Holloway & Huffaker, 1953; Gayton & Miller, 2012) which to put it mildly, does not suggest any benefits accruing from being galled.  That said, you could argue (weakly) and assuming that the plant is in control of producing the gall, that by confining the insect to a particular part of the plant it is “contained” and can be dealt with if it is causing too much damage by for example premature leaf abscission (Williams & Whitham, 1986).

The mutual benefit hypothesis is also easily dismissed as there is no evidence that galls improve the fitness of a plant as galling insects are parasites of the plant.  You might argue that fig wasps and figs mutually benefit each other, but in this case I think we are looking at special case pleading as the fig wasp are pollinators (Janzen, 1979).

So that takes us on to the adaptive value for insects hypothesis which makes a lot more sense as it is the insect (in this case the aphid), that has made the investment in what you might justifiably term, mutagenic saliva (Miles, 1999).

There is overwhelming evidence so support the nutrition hypothesis that galled leaves and galls are nutritionally superior to ungalled leaves (Llewellyn, 1982); e.g. acting as nitrogen sinks (Paclt & Hässler, 1967; Koyama et al., 2004), enhancing development and fecundity for succeeding generations of aphids (e.g. Leather & Dixon, 1981) and providing better nutrition for non-galling aphids and other insects (e.g. Forrest, 1971; Koyama et al., 2004; Diamond et al., 2008).   I also found a description of an aphid, Aphis commensalis, the waxy buckthorn aphid, which lives in the vacated galls of the psyllid Trichochermes walker, but whether this is for protection or nutritional reasons is not clear (Stroyan, 1952). 

The microenvironment hypothesis which suggests that the galls provide protection from extremes in temperature and humidity was hard to support with published data when Price et al. (1987) reviewed the topic. They mainly relied on personal observations that suggested that this might be true.  I found only two references in my search (Miller et al, 2009) that supported this hypothesis, albeit one of which is for gall wasps.  I have so far only been able to find one reference that suggest galls benefit aphids, in this case protecting them from very high temperatures (Martinez, 2009).

The natural enemy protection hypothesis has been tested almost as much as the nutrition hypothesis and in general terms seems to be a non-starter as gall forming insects seem to be especially attractive to parasitoids; see Price et al., (1987) for a host of references.  Aphids, however, may be a different case, free-living aphids have many parasitoid species attacking them, but those aphids that induce closed galls are singularly parasitoid free, at least in North America (Price et al., 1987). Although this may have been from lack of looking, as parasitoids have been identified from galls of the aphid Pemphigus matsumarai in Japan (Takada et al., 2010).  Closed galls are not always entirely closed as some need holes to allow honeydew to escape and migrants to leave (Stone & Schonrogge, 2003) which can act as entry points for natural enemies, but cleverly, the aphids have soldier aphids to guard against such insect invaders.

Sometimes the potential predator can be a vertebrate.  The aphid Slavum wertheimae forms closed galls on wild pistachio trees, and are, as with many other closed gall formers, not attacked by parasitoids (Inbar et al., 2004).  Wild pistachios are, however, attractive food sources to mammalian herbivores and gall aphids being confined to a leaf, unlike free living aphids could be inadvertently eaten. The galls however, contain higher levels of terpenes than surrounding leaves and fruits and emit high levels of volatiles that deter feeding by goats and other generalist herbivores thus protecting their inhabitants (Rostás et al., 2013). Not only that, but to make sure that any likely vertebrate herbivores avoid their gall homes, they make them brightly coloured (Inbar et al., 2010).   Aphids really are great at manipulating plants.

Cauliflower gall on wild pistachio, caused by Slavum wertheimae (Rostás et al., 2013).

Leaf rolls and curls on the other hand are more open structures, and in my experience, aphids that form leaf rolls or curls, are very vulnerable once a predator finds them crowded together in huge numbers.  Gall-dwelling aphids, including those that live in rolls and curls, tend, however, to be very waxy, and this may deter the less voracious predators.  I tend to support the nutritional benefit hypothesis in that with host alternating aphids, the enhanced nutrition enables rapid growth and development and is a way of building up numbers quickly, and hopefully the aphids are able to migrate to a new host, before the natural enemies find them.

Real life drama, Rhopalosiphum padi on Prunus padus at Harper Adams University May-June 2017.  In this instance the aphids won, and the plant was covered in hungry ladybird larvae eating mainly each other and the few aphids that had not managed to reach adulthood.

One thing that struck me while researching this article was that all the aphids producing galls, rolls or curls were host-alternating species. A fairly easily tested hypothesis for someone with the time to review the biology of about 5000 aphids, is that only host alternating aphids go in for galls.  This could be a retirement job J.

There are, depending on which estimate you agree with, somewhere between 8 000 000 to 30 000 000 insect species (Erwin, 1982; Stork, 1993; Mora et al., 2011), but even the highest estimate suggests that only 211 000 of these are galling species (Espirito-Santos & Fernandes, 2007).  And a final thought, if galls are so great why don’t all aphids and other phloem and xylem feeding insects go in for them?

References

Becquaert, J. (1924) Galls that secret honeydew.  A contribution to the problem as to whether galls are altruistic adaptations.  Bulletin of the Brooklyn Entomological Society, 19, 101-124.

Cockerell, T.D.A. (1890) Galls. Nature, 41, 344.

Diamond, S.E., Blair, C.P. & Abrahamson, W.G. (2008) Testing the nutrition hypothesis for the adaptive nature of insect galls: does a non-adapted herbivore perform better in galls?  Ecological Entomology, 33, 385-393.

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

Erwin, T.L. (1982) Tropical forests: their richness in Coleoptera and other arthropod species. The Coleopterists Bulletin, 36, 74-75.

Espirito-Santos, M.M.  & Fernandes, G.W. (2007) How many species of gall-inducing insects are there on Earth, and where are they?  Annals of the Entomological Society of America, 100, 95-99.

Forrest, J.M.S. (1971) The growth of Aphis fabae as an indicator of the nutritional advantage of galling to the apple aphid Dysaphis devecta. Entomologia experimentalis et applicata, 14, 477-483.

Forrest, J.M.S. & Dixon, A.F.G. (1975) The induction of leaf-roll galls by the apple aphid Dysaphis devecta and D. plantagineaAnnals of Applied Biology, 81, 281-288.

Gayton, D. & Miller, V. (2012) Impact of biological control on two knapweed species in British Columbia. Journal of Ecosystems & Management, 13, 1-14.

Holloway, J.K. & Huffaker, C.B. (1953) Establishment of a root borer and a gall fly for control of klamath weed.  Journal of Economic Entomology, 46, 65-67.

Inbar, M., Wink, M. & Wool, D. (2004) The evolution of host plant manipulation by insects: molecular and ecological evidence from gall-forming aphids on PistaciaMolecular Phylogenetics & Evolution, 32, 504-511.

Inbar, M., Izhaki, I., Koplovich, A., Lupo, I., Silanikove, N., Glasser, T., Gerchman, Y., Perevolotsky, A., & Lev-Yadun, S. (2010) Why do many galls have conspicuous colors?  A new hypothesis. Arthropod-Plant Interactions, 4, 1-6.

Janzen, D.H. (1979) How to be a fig. Annual Review of Ecology & Systematics, 10, 13-51.

Koyama, Y., Yao, I. & Akimoto, S.I. (2004) Aphid galls accumulate high concentrations of amino acids: a support for the nutrition hypothesis for gall formation.  Entomologia experimentalis et applicata, 113, 35-44.

Leather, S.R. & Dixon, A.F.G. (1981) Growth, survival and reproduction of the bird-cherry aphid, Rhopalosiphum padi, on it’s primary host. Annals of Applied Biology, 99, 115-118.

Llewellyn, M. (1982) The energy economy of fluid-feeding insects.  Pp 243-251, Proceedings of the 5th International Symposium on Insect-Plant Relationships, Wageningen, Pudoc, Wageningen.

Mani, M.S. (1964) The Ecology of Plant Galls. W Junk, The Hague.

Martinez, J.J.I. (2009) Temperature protection in galls induced by the aphid Baizongia pistaciae (Hemiptera: Pemphigidae).  Entomologia Generalis, 32, 93-96.

Miles, P.W. (1999) Aphid saliva.  Biological Reviews, 74, 41-85.

Miller, D.G., Ivey, C.T. & Shedd, J.D. (2009) Support for the microenvironment hypothesis for adaptive value of gall induction in the California gall wasp, Andricus quercuscalifornicus. Entomologia experientalis et aplicata, 132, 126-133.

Mora, C., Tittensor, D.P., Adl, S., Simpson, A.G.B., & Worm, B. (2011) How many species are there on earth and in the ocean? PloS Biology, 9(8):, e1001127.doi:10.1371/journal.pbio.1001127.

Paclt, J. & Hässler, J. (1967) Concentrations of nitrogen in some plant galls. Phyton, 12, 173-176.

Price, P.W., Fernandes, G.W. & Waring, G.L. (1987) Adaptive nature of insect galls.  Environmental Entomology, 16, 15-24.

Rostás, M., Maag, D., Ikegami, M. & Inbar, M. (2013) Gall volatiles defend aphids against a browsing mammal.  BMC Evolutionary Biology, 13:193.

Smith, K.M. (1920) Investigations of the nature and cause of the damage to plant tissue resulting from the feeding of capsid bugs.  Annals of Applied Biology,7, 40-55.

Smith, K.M. (1926) A comparative study of the feeding methods of certain Hemiptera and of the resulting effects upon the plant tissue, with special reference to the potato plantAnnals of Applied Biology, 13, 109-139.

Stone, G.N. & Schönrogge, K. (2003) The adaptive significance of insect gall morphology. Trends in Ecology & Evolution, 18, 512-522.

Stork, N.E. (1993) How many species are there? Biodiversity & Conservation, 2, 215-232.

Stroyan, H.L.G. (1952) Three new species of British aphid.  Proceedings of the Royal Entomological Society B, 21, 117-130.

Takada, H., Kamijo, K. & Torikura, H. (2010) An aphidiine parasitoid Monoctonia vesicarii (Hymenoptera: Braconidae) and three chalcidoid hyperparasitoids of Pemphigus matsumurai (Homoptera: Aphididae) forming leaf galls on Populus maximowiczii in Japan.  Entomological Science, 13, 205-215.

Williams, A.G. & Whitham, T.G. (1986) Premature leaf abscission: an induced plant defense against aphids. Ecology, 67, 1619-1627.

 

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Data I am never going to publish – A tale of sixty trees

In 1981 I spent a lot of time trudging through snow, cross-country skiing and snow-shoeing my way across the snowy wastes of Finland to snip twigs off bird cherry trees.  This was part of my post-doc which was to develop a forecasting system for the bird cherry-oat aphid, Rhopalosiphum padi.  On returning to the lab I then spent many a happy hour counting how many aphid eggs were nestled in between the buds and the stem on each twig.  It was while doing this that I noticed that some of the twigs were infested with the overwintering larval shields of the bird cherry ermine moth, Yponomeuta evonymellus.  Of course I then started counting them as well 🙂  I noticed that trees with lots of aphid eggs didn’t have very many larval shields and I wondered why. Some later observations from marked trees in Scotland appeared to provide evidence that the aphids and the moths tended to either prefer different trees or perhaps excluded each other.

Negative correlation between moths and aphids – more moths equals fewer aphids and vice versa

Based on these data I hypothesised that the two insects were indirectly competing for resources by altering plant chemistry and/or architecture thus making the trees less or more suitable for egg laying in the autumn (Leather, 1988).  I tested this experimentally when I was working for the Forestry Commission in Scotland using potted bird cherry trees that I defoliated to a lesser or greater extent to see if I could induce changes in foliar quality and tree growth rates that might influence subsequent colonisation by the aphids and moths. As predicted, those trees that had been defoliated, albeit by me and not by moth larvae, were less attractive to aphids in the autumn (Leather, 1993).  These effects were still apparent five years after the beginning of the experiment (Leather, 1995) when I had to desert my trees as I moved to a new position at Imperial College’s Silwood Park campus.

Given that apart from the location, the SE of England, this was my idea of a dream job for life (colleagues at the time included John Lawton, Mike Hassell, Bob May, Stuart McNeill, Mike Way, Brad Hawkins, Shahid Naeem, Mike Hochberg, Chris Thomas to name but a few), I decided to start up two long-term projects to see me through the next 30 years, one observational (my 52 sycamore tree project), the other experimental, a follow up to my bird cherry defoliation experiment.

I went for a simplified design of my earlier experiments, just two defoliation regimes, one to mimic aphid infestation (50%), the other to mimic bird cherry ermine moth defoliation (100%) and of course a non-defoliated control.  I also planted the trees in the ground to better simulate reality.  Using potted plants is always a little suspect and I figured that I would need to do rather a lot of re-potting over the next 30 years 🙂

The grand plan!

I sourced my trees from a Forestry Commission nursery thinking that as the national organisation responsible for tree planting in the UK I could trust the provenance of the trees.  Things didn’t go well from the start.  Having planted my trees in autumn 1992 and established the treatments in the spring of 1993 I discovered that my bird cherry, rather than being from a native provenance (seed origin) were originally from Serbia! Hmm 🙂  It was too late to start again, so I decided to carry on.  After all, bird cherry although widely planted in the SE, has a native distribution somewhat further north and west, which meant I was already operating close to the edge of ‘real life’, so what did an extra 1600 kilometres matter?

The mainly ‘natural’ distribution of bird cherry (left, Leather, 1996) and the current distribution including ‘introduced’ trees https://www.brc.ac.uk/plantatlas/index.php?q=plant/prunus-padus

Next, I discovered that my fence was neither rabbit nor deer proof.  I almost gave up at this point, but having invested a lot of time and energy in setting up the plot I once again decided to carry on. On the plus side, the trees most heavily defoliated and bitten back were mainly from the 100% defoliation treatment, but did give me some negative growth rates in that year.

My original plan was to record height (annually), bird cherry egg numbers (every December), bird cherry ermine moth larval shields (annually), bud burst and leaf expansion once a week, leaf-fall (annually), and once a month, defoliation rates in two ways, number of damaged leaves and an overall estimation of percentage defoliation.  This was a personal project, so no grant funding and no funding for field assistants.  It soon became clear, especially when my teaching load grew, as Imperial started replacing whole organism biologists with theoretical and molecular biologists, and I was drafted in to take on more and more of the whole organism lecturing, that I would not be able to keep both of my long term projects going with the same intensity.  Given the ‘problems’, associated with the bird cherry project, I decided  that I would ditch some of my sampling, bud burst was scored on 21st March every year and defoliation only measured once, in late summer and egg sampling and height recording came to a halt once the trees grew above me (2005)!  This allowed me to carry on the sycamore project as originally intended*.

I kept an eye on the trees until I left Silwood Park in 2012, but by 2006 I was only monitoring bud burst and leaf fall feeling that this might be useful for showing changes in phenology in our ever-warming world.  One regret as I wandered between the then sizeable trees in the autumn of 2012 was that I had not taken a before and after photograph of the plots.  All I have are two poor quality photos, one from 2006, the other from 2012.

The Sixty Tree site April 2006.

The Sixty Tree site April 2010 with a very obvious browse line

 

So, after all the investment in time, and I guess to a certain extent money (the trees and the failed fencing, which both came out of my meagre start-up funding**), did anything worthwhile come out of the study?

The mean number of Rhopalosiphum padi eggs per 100 buds in relation to defoliation treatment

As a long-time fan of aphid overwintering it was pleasing to see that there was a significant difference not only between years (F= 8.9, d.f. = 9/29, P <0.001), but also between treatments with the trees in the control treatment having significantly more eggs laid on them than the 100% defoliation treatment (F= 9.9, d.f. = 2/ 29, P <0.001 with overall means of 1.62, 1.22 and 0.65 eggs/100 buds).  This also fitted in with the hypothesis that trees that are defoliated by chewing herbivores become less suitable for aphids (Leather, 1988).  I must admit that this was a huge surprise to me as I had thought that as all the trees were attacked by deer the year after the experimental treatments they would all respond similarly, which is why I almost gave up the experiment back in 1994.

Bud burst stage of Prunus padus at Silwood Park on March 21st 1996-2012; by treatment and combined

When it came to budburst there was no treatment effect, but there was a significant trend to earlier budburst as the trees became older which was strongly correlated with warmer springs, although as far as spring temperatures were concerned there was no significant increase with year.

Mean spring temperature (Silwood Park) 1993-2012 and relationship between mean spring temperature and bud bust stage on 21st March.

Mean date of final leaf fall of Prunus padus at Silwood Park 1995-2012; by treatment and combined

At the other end of the year, there was a significant difference between date of final leaf fall between years but no significant difference between treatments.  In retrospect I should have adopted another criterion.  My date for final leaf fall was when the last leaf fell from the tree.  Those of you who have watched leaves falling from trees will know that there are always a few who are reluctant to make that drop to the ground to become part of the recycling process.  Even though they are very obviously dead, they hang there until finally dislodged by the wind.   I should really have used a measure such as last leaf with any pigment remaining.  I am sure that if I could be bothered to hunt down the wind speed data I would find that some sort of correlation.

Mean height (cm) of Prunus padus trees at Silwood Park 1993-2005 and Diameter at Breast Height (DBH) (cm) at the end of 2012

Except for the year after the deer attack, the trees, as expected, grew taller year by year.  There was however, no significant difference between heights reached by 2005 or in DBH at the end of 2012 despite what looked like a widening gap between treatments.

Defoliation scores of Prunus padus at Silwood Park 1993-2004; % leaves damaged and overall defoliation estimates

My original hypothesis that trees that were heavily defoliated at the start of their life would be more susceptible to chewing insects in later life, was not supported.  There was no significant difference between treatments, although, not surprisingly, there was a significant difference between years.  Average defoliation as has been reported for other locations was about 10% (Kozlov et al., 2015; Lim et al., 2015).

Number of Prunus padus trees with severe deer damage

That said, when I looked at the severity of deer attack, there was no effect of year but there was a significant effect of treatment, those trees that had been 100% defoliated in 1993 being most attractive to deer.   In addition, 20% of those trees were dead by 2012 whereas no tree deaths occurred for the control and less severely defoliated treatments.

I confess to being somewhat surprised to find as many significant results as I did from this simple analysis and was momentarily tempted to do a more formal analysis and submit it to a journal.  Given, however, the number of confounding factors, I am pretty certain that I would be looking at an amateur natural history journal with very limited visibility.  Publishing it on my blog will almost certainly get it seen by many more people, and who knows may inspire someone to do something similar but better.

The other reason that I can’t be bothered to do a more formal analysis is that my earlier work on which this experiment was based has not really hit the big time, the four papers in question only accruing 30 cites between them.  Hardly earth shattering despite me thinking that it was a pretty cool idea;  insects from different feeding guilds competing by changing the architecture and or chemsitry of their host plant.  Oh well.  Did anything come out of my confounded experiment or was it a total waste of time?  The only thing published from the Sixty Trees was a result of a totally fortuitous encounter with Marco Archetti and his fascination with autumn colours (Archetti & Leather, 2005), the story of which I have related in a previous post, and which has, in marked contrast to the other papers, had much greater success in the citation stakes 🙂

And finally, if anyone does want to play with the data, I am very happy to give you access to the files.

References

Archetti, M. & Leather, S.R. (2005) A test of the coevolution theory of autumn colours: colour preference of Rhopalosiphum padi on Prunus padus. Oikos, 110, 339-343. 50 cites

Kozlov, M.V., Lanta, V., Zverev, V., & Zvereva, E.L. (2015) Global patterns in background losses of woody plant foliage to insects. Global Ecology & Biogeography, 24, 1126-1135.

Leather, S.R. (1985) Does the bird cherry have its ‘fair share’ of insect pests ? An appraisal of the species-area relationships of the phytophagous insects associated with British Prunus species. Ecological Entomology, 10, 43-56.  14 cites

Leather, S.R. (1988) Consumers and plant fitness: coevolution or competition ? Oikos, 53, 285-288. 10 cites

Leather, S.R. (1993) Early season defoliation of bird cherry influences autumn colonization by the bird cherry aphid, Rhopalosiphum padi. Oikos, 66, 43-47. 11 cites

Leather, S.R. (1995) Medium term effects of early season defoliation on the colonisation of bird cherry (Prunus padus L.). European Journal of Entomology, 92, 623-631. 4 cites

Leather, S.R. (1996) Biological flora of the British Isles Prunus padus L. Journal of Ecology, 84, 125-132.  14 cites

Lim, J.Y., Fine, P.V.A., & Mittelbach, G.G. (2015) Assessing the latitudinal gradient in herbivory. Global Ecology & Biogeography, 24, 1106-1112.

 

 

*which you will be pleased to know, is being analysed as part of Vicki Senior’s PhD project, based at the University of Sheffield.

**£10 000 which even in 1992 was not overly-generous.

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