Tag Archives: host acceptability

Not all aphids get lost

Although aphids are very good at kicking, we know that aphids would not be very good at football as they are very short-sighted (Doring et al., 2008) but does that mean that they are not very good at finding their host plants? There is a common misperception, and not just confined to non-entomologists, that aphids are no more than aerial plankton. In 1924 Charles Elton

Lost 1

whilst on an expedition to Nordaustlandet* (the second largest of the Spitsbergen group and almost entirely covered by ice) reported finding large numbers of aphids, many still alive, later identified as Dilachnus piceae (now known as Cinara piceae) (Elton, 1925).

Lost 2

Cinara piceae the Greater Black Spruce Aphid –big and beautiful.

 

He suggested that the aphids came from the Kola Peninsula, a distance of about 800 miles (almost 1300 km) due to the strong south and south-east winds blowing at the time. He estimated that they would have made the journey within twelve to twenty-four hours. This was regarded as being an example of totally passive migration and used as one of many examples of aerial plankton** (Gislen, 1948). This is, however, probably not giving aphids credit for what they are capable of doing when it comes to flight. Berry & Taylor (1968), who sampled aphids at 610 m above the grounds using aeroplanes, implied that the aphids, although using jet streams, were flying rather than floating (page 718 and page 720) and that they would descend to the ground in the evening and not fly during the night.

Lost 3

Aphids don’t usually fly during the night. (From Berry & Taylor (1968)).

Dixon (1971) interprets this somewhat differently and suggests that the “movement of the air in which it is flying determines the direction of its flight and the distance it will travel” but then goes on to say “after flying for an hour or two aphids settle indiscriminately on plants”. So yes the speed of the air in which the aphid is flying will determine how far it flies in a set time, but as aphids can fly much longer than an hour or two, active flights of from between 7-12 hours have been recorded (Cockbain, 1961), this rather suggests that the aphids are making a “decision” to stop flying and descend from the jet stream. That said, in the words of the great C.G. Johnson “aphids are weak flyers”, they cannot make progress against headwinds of more than 2 km per hour (Johnson, 1954), although Trevor Lewis gives them slightly more power and suggests that the can navigate against winds of up to 3 km per hour (Lewis, 1964).

Whatever the upper limit is, it doesn’t mean that they are powerless when it comes to ‘deciding’ when to stop flying. In the words of Hugh Loxdale and colleagues, “aphids are not passive objects” (Loxdale et al, 1993). Aphidologists, were until the 1980s (Kennedy, 1986), generally somewhat sceptical about the ability of aphids to direct their flight in relation to specific host finding from the air and not just flying towards plants of the right colour (Kennedy et al., 1961), or at all after take-off (Haine, 1955). The general consensus now, is that aphids control the direction of their flight in the boundary layer*** but that it is determined by the wind at higher altitudes (Loxdale et al., 1993).   Whilst we are discussing viewpoints, another point of debate is on whether aphids migrate or not. Loxdale et al., (1993) state that “migration can be viewed ecologically as population redistribution through movement, regardless of whether deliberate of uncontrolled or from the behavioural viewpoint of a persistent straightened-out movement affected by the animal’s own locomotory exertions or by its active embarkation on a vehicle”. In the case of aphids the vehicle could be the wind. Under both definitions, aphids can be defined as undertaking migrations. Long-distance migration by aphids is defined as being greater than 20 km and short-distance (local) migration being less than this (Loxdale et al., 1993). Long-distance migration is likely to be the exception rather than the rule with most aphids making local flights and not venturing out of the boundary layer, sometimes travelling distances no more than a few hundred metres (Loxdale et al., 1993).

There are different types of winged aphids (morphs) and these show different angles of take-off and rates of climb.  In Aphis fabae for example, which host –alternates between spindle and bean, the gynoparae which migrate from the secondary host to the primary host, have a steeper angle of take-off and climb more rapidly than the alate exules which only disperse between the secondary host plants (David & Hardie, 1988).

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http://influentialpoints.com/Images/Rhopalosiphum_padi_emigrant_alate_departing_from_primary_host_c2013-05-21_11-25-12ew.jpg

The gynoparae are thus much more likely to end up in the jet stream and be carried longer distances, with, of course, a greater chance of getting lost (Ward et al., 1998). The alate exules however, may only land in the next field or even in the same one, and easily find a new host plant (Loxdale et al., 1993). These differences between the morphs of host alternating aphids are also seen in the bird cherry-oat aphid Rhopalosiphum padi (Nottingham et al., 1991).  Once safely air-borne, the aphids then have another set of problems to overcome.

How do they ‘decide’ when to land? How do they ‘know’ that there are host plants below them? Aphids have two main senses that help them locate their host plants, vision and smell (odour recognition) (Kring, 1972; Döring, 2014). Generally speaking, aphids respond positively to what we perceive as green or yellow light and negatively to blue and red light (Döring & Chittka, 2007) although this is not an absolute rule. Some aphids are known to preferentially choose yellowing leaves (sign of previous infestation) e.g. Black Pecan Aphid Melanocallis caryaefoliae (Cottrell et al., 2009) which indicates a pretty sophisticated host finding suite of behaviours. Aphids in flight chambers will delay landing if presented with non-host odours even in the presence of a green target (Nottingham & Hardie, 1993) and conversely can be attracted to colourless water traps that have been scented with host plant odours (Chapman et al., 1981). Aphids are thus using both visual and olfactory cues to locate their host plants and to ‘decide’ when to descend from the jet stream or boundary layer (Kring, 1972; Döring, 2014). They are not merely aerial plankton, nor are they entirely at the mercy of the winds, they do not deserve to be described as passive (Reynolds & Reynolds, 2009).

Once at ground level and on a potential host plant, aphids go through a complicated suite of behaviours to determine if the host is suitable or not; if the plant meets all the required

Lost 5

From air to plant – how aphids chose their host plants – after Dixon (1973).

 

criteria, then the aphid will start feeding and reproducing. It is interesting to note that although there may be a lot of aphids in the air, the number of plants on the ground that

Lost 6

Settled safely and producing babies 🙂

http://beyondthehumaneye.blogspot.co.uk/2012/06/aphids.html  https://simonleather.files.wordpress.com/2016/04/cd0a4-aphidbirth2small.jpg

 

are infested with them is relatively low, about 10% in a diverse landscape (Staab et al., 2015), although in a crop, the level of infestation can approach 100% (e.g. Carter et al., 1980). The fact that in some cases less than 1% of those that set off will have found a host plant (Ward et al., 1998) is not a problem when you are a member of clone; as long as not all of the members of a clone gets lost the journey has been a success.

They may be small, they may be weak flyers, but enough of them find a suitable host plant to keep the clone alive and kicking; not all aphids get lost.

 

References

Carter, N., Mclean, I.F.G., Watt, A.D., & Dixon, A.F.G. (1980) Cereal aphids – a case study and review. Applied Biology, 5, 271-348.

Chapman, R.F., Bernays, E.A., & Simpson, S.J. (1981) Attraction and repulsion of the aphid, Cavariella aegopodii, by plant odors. Journal of Chemical Ecology, 7, 881-888.

Cockbain, A.J. (1961) Fuel utilization and duration of tethered flight in Aphis fabae Scop. Journal of Experimental Biology, 38, 163-174.

Cottrell, T.E., Wood, B.W. & Xinzhi, N. (2009) Chlorotic feeding injury by the Black Pecan Aphid (Hemiptera: Aphididae) to pecan foliage promotes aphid settling and nymphal development. Environmental Entomology, 38, 411-416

David, C.T. & Hardie, J. (1988) The visual responses of free-flying summer and autumn forms of the black bean aphid, Aphis fabae, in an automated flight chamber. Physiological Entomology, 13, 277-284.

Dixon, A.F.G. (1971) Migration in aphids. Science Progress, Oxford, 59, 41-53.

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

Döring, T.F. & Chittka, L. (2007) Visual ecology of aphids – a classcial review on the role of colours in host finding. Arthropod-Plant Interactions, 1, 3-16.

Döring, T., Hardie, J., Leather, S.R., Spaethe, J., & Chittka, L. (2008) Can aphids play football? Antenna, 32, 146-147.

Döring, T. (2014) How aphids find their host plants, how they don’t. Annals of Applied Biology, 165, 3-26.

Elton, C.S. (1925) The dispersal of insects to Spitsbergen. Transactions of the Entomological Society of London, 73, 289-299.

Gislen, T. (1948) Aerial plankton and its conditions of life. Biological Reviews, 23, 109-126.

Haine, E. (1955) Aphid take-off in controlled wind speeds. Nature, 175, 474-475

Johnson, C.G. (1951) The study of wind-borne insect populations in relation to terrestrial ecology, flight periodicity and the estimation of aerial populations. Science Progress, 39, 41-62.

Johnson, C.G. (1954) Aphid migration in relation to weather. Biological Reviews, 29, 87-118

Kennedy, J. S., Booth, C. O. & Kershaw, W. J. S. (1961). Host finding by aphids in the field III Visual attraction. Annals of Applied Biology, 49, 1-21.

Kring, J.B. (1972) Flight behavior of aphids. Annual Review of Entomology, 17, 461-492.

Lewis, T. (1964) The effects of shelter on the distribution of insect pests. Scientific Horticulture, 17, 74-84

Loxdale, H. D., Hardie, J., Halbert, S., Foottit, R., Kidd, N. A. C. &Carter, C. I. (1993).The relative importance of short-range and long-range movement of flying aphids. Biological Reviews of the Cambridge Philosophical Society, 68, 291-312.

Nottingham, S.F., Hardie, J. & Tatchell, G.M. (1991) Flight behaviour of the bird cherry aphid, Rhopalosiphum padi. Physiological Entomology, 16, 223-229.

Reynolds, A.M. & Reynolds, D.R. (2009)  Aphid aerial desnsity profiles are consistent with turbulent advection amplifying flight behaviours: abandoning the epithet ‘passive’. Proceedings of the Royal Society B, 276, 137-143.

Staab, M., Blüthgen, N., & Klein, A.M. (2015) Tree diversity alters the structure of a tri-trophic network in a biodiversity experiment Oikos, 124, 827-834.

Ward, S.A., Leather, S.R., Pickup, J., & Harrington, R. (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology, 67, 763-773.

 

Post script

Political and geographic borders are not factors that deter aphid migrants, Wiktelius (1984) points out that aphids regularly make the journey across the Baltic in both directions to and from Sweden.

Wiktelius, S. (1984) Long range migration of aphids into Sweden. International Journal of Biometeorology, 28, 185-200.

 

*Elton refers to it as North-East Land

** Johnson (1951) objects to this terminology in no uncertain terms. That said, as there are records of non-winged aphids being caught by aircraft (Kring, 1972), it does suggest that there may be some accidental migration going on.

*** The UK Met Office defines the boundary layer as “that part of the atmosphere that directly feels the effect of the earth’s surface” and goes on to say that depending on local conditions it can range in depth from a few metres to several kilometres.

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Can hawkmoths remember being attacked?

As our summer holidays are usually in the south of France or Italy I expect to see a plethora of insects whilst sitting on a sun-lit patio with a glass of wine or beer to hand. I am rarely disappointed, this year (2015) swallowtails being very common. Also present, although not as abundant as I have seen in some years, was the European hummingbird hawkmoth, Macroglossum stellatarum, perhaps my favourite moth. Given that they were foraging so close to my watering hole, it seemed a great opportunity to use my new camera. I was able to capture images of the swallowtails, who obligingly remained still at the crucial moment I took the picture.

Swallowtail

Swallowtail butterfly, Super-las-Illas, France, August 2015

I was however, unable to get a decent still shot of the hawkmoths so had to resort to the video mode.

Hawkmoth

Hummingbird hawkmoth, Super-las-Illas, France, August 2015. For the live action version see here

It was whilst trying to get a successful shot of these incredibly active insects that I thought I might catch one and slow it down in the fridge and thus be able to get a nice close up picture. As usual I had forgotten my butterfly net (one year I will actually remember to pack it) so had to improvise with a T-shirt and stick. Needless to say this was not very successful and I only managed a glancing ‘strike’ on my chosen victim. Not surprisingly he/she flew off. What was surprising was that the flower bed remained hawkmoth-free for about an hour or so. Once they returned I had yet another unsuccessful attempt at capturing one, and again noticed that they disappeared and did not return for another couple of hours. Intrigued I repeated my unsuccessful capture attempts (deliberately this time) over the next few days and found this behaviour repeated. So, no problems if I stood there and filmed/watched them, but if I tried to catch them, off they went (I was unable to see where) not to return for a couple of hours. I hypothesised that they must be able to ‘remember’ being attacked and that this was a predator-avoidance mechanism.

I knew that adult lepidoptera in general are able to ‘remember’ host suitability for oviposition sites and alter their concept of a good quality host depending on the suitability of the previous host plants that they had landed on and the number of eggs left in their reproductive tract.

Host acceptability model

A very simple model to illustrate the trade-off between host plant acceptance, egg load and time in lepidoptera. I thought I had published this figure somewhere but apparently not 🙂

Adult lepidoptera such as the green-veined white butterfly, Pieris napi (Goulson & Cory, 1993) and the Monarch Butterfly, Danaus plexippus (Rodrigues & Weiss, 2012) are also able to remember (retain) learned information about suitable feeding resources e.g. those flowers that are likely to give them the most nectar and this is also true for the hummingbird hawkmoth which is able to remember flower preferences even after hibernation (Kelber, 2010).

Although adult lepidoptera have a number of predator avoidance mechanisms, e.g. mimicry, aposematism, unpalatability or innate behaviours (e.g. Roper & Redston, 1987; Bowers, 1980; Greig & Greenfield, 2004; Stevens, 2005) I have been unable to find any reference to them being able to ‘remember’ being attacked and then avoiding the area for some time afterwards. There are, on the other hand, many papers about predators learning to avoid distasteful lepidopteran prey but nothing about adult lepidoptera learning to avoid predator-rich areas. This would seem a ‘sensible’ trait to evolve so I am surprised that no one seems to have tested its existence. Please let me know if you have ever come across any references to this sort of behaviour or feel free to conduct the experiment formally.

References

Agnew, K. & Singer, M.C. (2000) Does fecundity drive the evolution of insect diet? Oikos, 88, 533-538.

Bowers, M.D. (1980) Unpalatability as a defense strategy of Euphydryas phaeton (Lepidoptera: Nymphalidae). Evolution, 34, 586-600.

Goulson, D. & Cory, J.S. (1993) Flower constancy and learning in foraging preferences of the green-veined white butterfly Pieris napi. Ecological Entomology, 18, 315-320.

Greig, E.I. & Greenfield, M.D. (2004) Sexual selection and predator avoidance in an acoustic moth: discriminating females take fewer risks. Behaviour, 141, 799-815

Kelber, A. (2010) What a hawkmoth remembers after hibernation depends on innate preferences and conditioning situation. Behavioral Ecology, 21, 1093-1097

Rodriques, D. & Weiss, M.R. (2012) Reward tracking and memory decay in the Monarch butterfly, Danaus plexippus L. (Lepidoptera: Nymphalidae). Ethology, 118, 122-1131

Roper, T.J. & Redston, S. (1987) Conspicuousness of distasteful prey affects the strength and durability of one-trial avoidance learning. Animal Behaviour, 35, 739-747

Singer, M.C. (1984). Butterfly-host plant relationships: host quality, adult choice and larval success. In The Biology of Butterflies (ed. by R.I. Vane-Wright & P.R. Ackery), pp. 81-88. Chapman & Hall, London.

Stevens, M. (2005) The role of eyespots as anti-predator mechanisms, principally demonstrated in the Lepidoptera. Biological Reviews, 80, 573-588

 

 

 

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