Weevily clever – on being behaviourally resistant

I am currently sharing my office with a Tupperware container of weevils, Hylobius abietis, the Large pine weevil to be exact.  The reason, just in case you were wondering, is that I have had an undergraduate doing her final year research project with me on ways in which this highly pestiferous weevil might be prevented from feeding on newly planted conifers.  The weevils in my office are those that were left over from her project and being the old softie that I am, and having worked on Hylobius since 1987 I couldn’t bear to throw them away :.)

My office pets – easy to maintain and quite cute

Adult and larvae of Hylobius abietis

You might think that having worked on an insect with the sole aim of trying to reduce its pestiferousness, that I might have succeeded by now.  Say that to the many scientists who have addressed this problem for more than a century and you will be rewarded with the sound of hollow laughter.  The laughter is even hollower if you point them to the statement made by the first UK Forestry Commission entomologist,  J W Munro, who a mere ten years after the formation of the Forestry Commission wrote “The pine weevil (Hylobius abietis) problem still occupies the attention of the Forestry Commissioners” Munro (1929).  Ninety years on I can make exactly the same statement and judging by the global number of papers written about Hylobius, I think I can confidently state that the same can be said for the forest industry as a whole.

Not a problem that is going away! Papers published on Hylobius abietis since 1910.  Data from Google Scholar and Web of Science.

So why is the large pine weevil, or Hylobius as those of us who work on it or attempt to control it, call it so hard to manage? The simple answer is that we have helped it become a pest in the first place and in the second place it has a couple of attributes that give it a bit of an edge. You might even go so far as to say that it is a clever little beast.

First a little bit of history is in order. Up until the beginning of the 20th century references to Hylobius are few and far between, especially in the UK, although there are some German references from the latter half of the 19th Century, a reflection of the fact that the German forest industry was well in advance of that in the UK. Prior to the establishment of conifer plantations, populations of Hylobius would have been small and scattered as the larvae need conifer stumps or large pieces of fallen branch in which to develop.  The adults, which can live for up to four years (Leather et al., 1999), would normally feed on the cambium of thin barked twigs in the upper canopy of conifer trees, and the larvae, depending on how shaded the host stump was, could take from a year to two years to reach adulthood.  The adults are extremely responsive to host volatiles (Nordenhem & Eidmann, 1991) and can locate host plants and egg-laying sites remarkably quickly*.  Plantation forestry with its cycles of clear-fell and subsequent restocking with two year old conifer saplings has been akin to setting up a deliberate breeding programme for Hylobius.  In some cases 100% of all new planting can be destroyed by the adults ring-barking the saplings and on average 30% would be lost if plants were not pre-treated with insecticide.

How to turn an innocuous forest insect into a major pest. Plantation forestry and how it created a forest pest. (Figure adapted from Leather et al, 1999).

Over the years there have been a number of attempts at controlling Hylobius without using insecticides, including cultural methods, physical barriers and biological control using entomopathogenic nematodes (Williams et al., 2013), none of which have been as effective as insecticidal treatment. The latter, although reasonably effective at preventing sapling damage, may not, however, be reducing Hylobius numbers.  This is because Hylobius is, as well as being good at detecting host volatiles, also great at detecting and avoiding insecticides.  A former PhD student of mine, Dan Rose, showed this is in a series of elegant experiments where he manipulated insecticide presence and absence at different scales (Rose et al., 2005).  First he tested if adult Hylobius could detect the presence of an insecticide at a whole plant level, by giving them a choice in semi-field conditions between treated and untreated saplings.  They could, they avoided feeding on treated plants.  Then he gave them a choice of plants where he had sprayed half the canopy with an insecticide, and, yes, you guessed it, they only fed on the untreated parts.

 Given a choice, adult Hylobius abietis will not feed on insecticide treated plants or on those parts of a tree that have been treated with an insecticide

Dan wondered just how good their discriminatory powers were, so using our standard choice boxes,

Standard Hylobius abietis host choice test box

he presented his weevils with pieces of pine twig that had had insecticide painted on to them alternating with equal width untreated stripes, and yes, you guessed, they only ate the untreated parts of the twig.

  Adult Hylobius abietis only fed on the untreated stripes.

Next he sprayed twigs all over, but some with large droplets and some with fine droplets and then gave them the choice between a coarse sprayed twig and a fine sprayed one and as you may have guessed,  they were able tell the difference, and fed on the twigs with the bigger spaces between the droplets of insecticide.

Given a choice between twigs treated with a large droplet spray and a fine droplet spray, adult Hylobius abietis will feed on the twigs with the large droplet size spray application.

 

So this is an indication that adult Hylobius are behaviourally resistant to insecticides, well at least the ones he tested them against. Hylobius are not alone in possessing this trait, other weevils (Haddi et al., 2015) and at least one aphid species (Fray et al., 2014) are also able to detect and avoid insecticide treated substrates.

Hylobius adults are also quite resistant to insecticide poisoning when you force them to eat treated plant material. Some individuals take almost three weeks to die and then if they are removed from the insecticide treated food they soon return to normal.

Figure borrowed from Rose et al.,( 2005)

Remarkable rate of recovery (Figure borrowed from Rose et al., (2006)

 

Hylobius abietis adults are able to recover from pesticides if given the chance, even after a week of exposure.

Given that they are able to recognise and avoid eating treated plant material and if they do, show remarkable powers of recovery, it is very likely that in the field, the reason that the insecticidal treatment works is more to do with repellence than toxicity, so it is unlikely that weevil popualtions are reduced.

To reduce populations rather than divert them elsewhere and given the pressure to remove pesticides from the forest environment, a biological control approach is the logical best option. Entompathogenic nematodes are probably the best option and have received  a lot of attention over the last thirty years or so (Williams et al., 2013), but again Hylobius has a tactic or two up its elytra to make it more difficult to control than other insect pests.  First, like its North American cousin, Hylobius pales (Cornell & Wilson, 1984; Moore, 2001), it can play dead, a phenomenon known as thanatosis or death feigning. In human terms, when they see/feel a nematode approaching, they hold their breath and collapse in a heap. In insect terms, they close their spiracles, the point of entry for the nematodes, and hope that the nematodes give up and go away before they have to breathe again.  If they do have to breathe when the nematodes are still in contact with them then clever old Hylobius is able to brush them away (Ennis et al., 2010). Biological control of adult Hylobius is thus unlikely to be successful, and the larvae and their stump habitats are now the main target of biological control methods (Williams et al., 2013).

Clever, cute and long-lived, what more can you ask for in a pet or should that be pest? 🙂

 

References

Cornell, J.A. & Wilson, L.F.  (1984) Dispersion and seasonal activity of the pales weevil, Hylobius pales (Coleoptera: Curculionidae), in Michigan Christmas tree plantations. Canadian Entomologist, 116, 711-717.

Ennis, D.E., Dillon, A.B. & Griffin, C.T. (2010) Pine weevils modulate defensive behaviour in response to parasites of differing virulence. Animal Behaviour, 80, 283-288.

Fray, L.M., Leather, S.R., Powell, G., Slater, R., McIndoe, E. & Lind, R.J. (2014) Behavioural avoidance and enhanced dispersal in neonicotinoid-resistance Myzus persicae (Sulzer). Pest Management Science, 70, 88-96.

Haddi, K., Mendonça, L.P., Dos Santos, M.F., Guedes, R.N.C & Oliveira, E.E. (2015) Metabolic and behavioral mechanisms of Indoxacarb resistance in Sitophilus zeamais (Coleoptera: Curculionidae). Journal of Economic Entomology, 108, 362-369.

Leather, S.R., Day, K.R. & Salisbury, A.N. (1999) The biology and ecology of the large pine weevil, Hylobius abietis (Coleoptera: Curculionidae): a problem of dispersal? Bulletin of Entomological Research, 89, 3-16.

Moore, R. (2001) Emergence trap developed to capture adult large pine weevil Hylobius abietis (Coleoptera: Curculionidae) and its parasite Bracon hylobii (Hymenoptera: Braconidae). Bulletin of Entomological Research, 91, 109-115.

Munro, J.W. (1929) The biology and control of Hylobius abietis L. Part 2. Forestry, 3, 61-65.

Nordenhem, H. & Eidmann, H.H. (1991) Response of the pine weevil Hylobius abietis L. (Col. Curculionidae) to host volatiles in different phases of its adult life cycle. Journal of Applied Entomology, 112, 353-358.

Nördlander, G., Hellqvist, C., Johansson, K. & Nordenhem, H. (2011) Regeneration of European boreal forests: effectiveness of measures against sedling mortality caused by the pine weevil Hylobius abietis. Forest Ecology and Management, 262, 2354-2363.

Rose, D., Leather, S.R. & Matthews, G.A. (2005) Recognition and avoidance of insecticide-treated Scots pine (Pinus sylvestris) by Hylobius abietis (Coleoptera: Curculionidae): implications for pest management strategies. Agricultural and Forest Entomology, 7, 187-191.

Rose, D.R., Matthews, G.A. & Leather, S.R. (2006) Sub-lethal responses of the large pine weevil, Hylobius abietis, to the pyrethroid insecticide lambda-cyhalothrin. Physiological Entomology, 31, 316-327.

Williams, C.D., Dillon, A.B., Harvey, C.D., Hennessy, R., McNamara, L. & Griffin, C.T. (2013) Control of a major pest of forestry, Hylobius abietis, with enomopathogenic nematodes and fungi using eradicant and prophylactic strategies. Forest Ecology & Management, 305, 212-222.

 

6 Comments

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6 responses to “Weevily clever – on being behaviourally resistant

  1. Marlies

    Wow! Such a clever beast!

    Liked by 1 person

  2. jim kirby

    Thanks again-educative and entertaining. My money is on the Weevil but there ya go. I will try thanatosis if I encounter a forestry commission gang.

    Liked by 1 person

  3. I can sense your admiration of these fascinating tactics but they sound so frustrating. I’ll pass on the idea of having them as pets. Amelia

    Liked by 1 person

  4. One of my favourite insects, which I worked with briefly as a visiting scientist with Goran Nordlander in 1993. I was so enamoured with it that I spent a considerable amount of time working on a less pestiferous, but equally beguiling congener, Hylobius warreni. You literally become attached to these insects (they clamp on pretty tight to your finger if you let them). Bad for forestry, but what’s not to love otherwise!

    Liked by 1 person

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