“Ecological Armageddon”, we’ve known for years that insects are in decline so why so much fuss now?

Unless you have lived in a news vacuum for the last two weeks or so, you will be aware of the impending “Ecological Armageddon” that is about to be unleashed upon us.  A paper in the journal PLoS ONE  in which it was reported that there had been a 75% decline in the biomass of flying insects in protected areas in Germany since 1989 was the starting pistol that began the media frenzy.  The newspapers, both broadsheet and tabloids were quick to react as were the radio and TV stations and the coverage was global as this selection of links shows.

https://www.nytimes.com/2017/10/29/opinion/insect-armageddon-ecosystem-.html

https://www.theguardian.com/environment/2017/oct/18/warning-of-ecological-armageddon-after-dramatic-plunge-in-insect-numbers

http://www.independent.co.uk/news/science/flying-insects-numbers-drop-ecological-armageddon-75-per-cent-plummet-a8008406.html

http://www.express.co.uk/news/science/868283/Armageddon-end-of-the-world-Germany-insects-Sussex-University-UK-Government

https://www.hs.fi/ulkomaat/art-2000005414880.html

https://risingsunoverport.co.za/53144/enviro-monday-flying-insect-populations-declining-drastically-germany/

https://www.washingtonpost.com/world/europe/buzz-off-german-study-finds-dramatic-insect-decline/2017/10/19/6a087d40-b4c8-11e7-9b93-b97043e57a22_story.html?utm_term=.00836ee55dca

Entomologists were in great demand for a few days, all being asked to comment gravely on the paper and its implications.   I was also persuaded to air my thoughts on air, Talk Radio having caught me at an unguarded moment.  I should never have answered the ‘phone 😊

As the media frenzy subsided, the more considered responses began to appear.  Manu Saunders very sensibly attempted to put the study in perspective and point out its limitations. Two entomologists from the Game & Wildlife Conservancy Trust which hold an even longer data set, put forward their interpretation and an ecological consultancy also took the opportunity to comment.  The authors of the paper and the blog commentators were careful not to point the finger directly at pesticides as the main cause of this decline, although they did rule out climate change.  Agricultural intensification and the practices associated with it, were however, suggested as likely to be involved in some way, something that has been known for more than a century as the naturalist and novelist Gene Stratton-Porter  pointed out in 1909  in her novel A Girl of the Limberlost,

 “Men all around were clearing available land.  The trees fell wherever corn would grow. The swamp was broken by several gravel roads…Wherever the trees fell the moisture dried, the creeks ceased to flow, the river ran low, and at times the bed was dry.  From coming in with two or three dozen rare moths a day, in three years time Elnora had grown to be delighted with finding two or three. Big pursy caterpillars could not be picked from their favourite bushes, where there were no bushes. Dragonflies could not hover over dry places and butterflies became scare in proportion to the flowers”.

What puzzles me about the media response is why now and why this particular study?  We have known for a long time that some insect groups have been in decline for many years.  The parlous state of UK butterflies and moths has been highlighted on more than one occasion over the last couple of decades (e.g. Conrad et al., 2004; Thomas et al., 2004; Fox et al., 2013), and declines in the abundance of bibionid flies (D’Arcy-Burt & Blackshaw, 1987), dragonflies (Clausnitzer et al., 2009) and carabid beetles (Brooks et al., 2012) have also been noticed and written about.  In addition, the results of a 42-year study on insects associated with cereal fields in SE England was published recently (Ewald et al., 2015), with little or no fanfare associated with it.  I commented on the decline of some insect species (and entomologists) in a blog post in 2013 and in December of last year, wrote about the general decline of insect numbers and lack of long term studies, incidentally citing the German study when it was originally published in a little known German publication back in 2013 and with far fewer authors 😊

The media response to this not new news puts me in mind of the Ash Die Back scare of 2012 when the press and politicians having

Pests and diseases recorded as entering the UK 1960-2015.  The two arrows indicate the replacement of local forest offices with central district offices and reduction in entomology and pathology staff.

been warned and made aware of the increasing incidence of non-native pests and pathogens entering the country for many years beforehand, suddenly, and in response to an intractable problem, went overboard in reporting doom and destruction

https://www.theguardian.com/environment/2012/nov/09/ash-dieback-disease-impossible-eradicate

https://www.theguardian.com/environment/2012/oct/24/ash-dieback-disease-east-anglia

http://www.telegraph.co.uk/news/earth/earthnews/9566224/Deadly-fungus-in-Ash-trees-could-be-next-Dutch-elm-disease-warns-Woodland-Trust.html

http://www.abc.net.au/am/content/2012/s3620359.htm

My hypothesis, for what it is worth, is that it is like when a tap washer starts to wear out, and your tap starts to drip. At first you just ignore it or turn the tap ever more tightly every time you use it.  Eventually something gives, either the tap breaks off (this happened to me very recently) or the drip becomes a flood.  Either way, something needs to be done, i.e. call the plumber.  In the case of the Ash Die Back episode, the UK government responded positively, albeit too late to prevent it, but by setting up the Tree Health and Plant Biosecurity Expert Taskforce of which I was privileged to be a member, recommendations were made that resulted in increased forest research funding and additional legislation being put in force to hopefully reduce the chances of further invasions.  I suspect that the current “Ecological Armageddon” scenario will not result in a similar response, although it may encourage research councils worldwide to think more seriously about funding more research into sustainable agriculture and for governments to encourage farmers to adopt farming strategies that encourage more wildlife and use fewer inputs.  At the same time, given the increasing number of studies that implicate urbanisation as a major factor in the decline of insect numbers (e.g. Jones & Leather, 2012; Dennis et al., 2017) it would behove local planning authorities to increase their efforts to provide much-needed green spaces in our towns and cities and to ban the use of decking in gardens and the replacement of front gardens with concrete and tarmac car parking areas.

What it does highlight as Manu Saunders said in her blog, is that we need funding for more long-term studies.  We also need to find instances where the data already exist but have not yet been analysed, amateur records and citizen science projects may be of use here.  Alternatively, as was very recently done in France (Alignier, 2018), it is possible, using the identical protocol, to resample a site after a gap of decades, to see what changes have occurred.

I hope for the sake of our descendants that the reports of an “Ecological Armageddon” have been exaggerated.  This should however, be a wake-up call to all those with the power to do something to mitigate the decline in biodiversity worldwide.  Governments need to respond quickly and to think long-term and responsibly.  The current attitude of politicians to adopt a short-term ‘how safe is my job’ political viewpoint is no longer a viable one for the planet. It is precisely that attitude that got us into the situation that we find ourselves in now.

References

Alignier, A. (2018) Two decades of change in a field margin vegetation metacommunity as a result of field margin structure and management practice changes. Agriculture, Ecosystems & Environment, 251, 1-10.

Brooks, D.R., Bater, J.E., Clark, S.J., Montoth, D.J., 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 of insect biodiversity. Journal of Applied Ecology, 49, 1009-1019.

Clausnitzer, V., Kalkman, V.J., Ram, M., Collen, B., Baillie, J.E.M., Bedjanic, M., Darwall, W.R.T., Dijkstra, K.D.B., Dow, R., Hawking, J., Karube, H., Malikova, E., Paulson, D., Schutte, K., Suhling, F., Villaneuva, R.J., von Ellenrieder, N. & Wilson, K. (2009)  Odonata enter the biodiversity crisis debate: the first global assessment of an insect group.  Biological Conservation, 142, 1864-1869.

Conrad, K.F., Woiwod, I.P., Parsons, M., Fox, R. & Warren, M.S. (2004) Long-term population trends in widespread British moths.  Journal of Insect Conservation, 8, 119-136.

Darcy-Burt, S. & Blackshaw, R.P. (1987) Effects of trap design on catches of grassland Bibionidae (Diptera: Nematocera).  Bulletin of Entomological Research, 77, 309-315.

Dennis, E.B., Morgan, B.J.T., Roy, D.B. & Brereton, T.M. (2017) Urban indicators for UK butterflies. Ecological Indicators, 76, 184-193.

Ewald, J., Wheatley, C.J., Aebsicher, N.J., Moreby, S.J., Duffield, S.J., Crick, H.Q.P., & Morecroft, M.B. (2015) Influences of extreme weather, climate and pesticide use on invertebrates in cereal fields over 42 years. Global Change Biology, 21, 3931-3950.

Fox, R. (2013) The decline of moths in Great Britain: a review of possible causes. Insect Conservation & Diversity, 6, 5-19.

Hallmann, C.A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., Stenmans, W., Müller, A., Sumser, H., Hörren, T., Goulson, D. & de Kroon, H. (2017) More than 75% decline over 27 years in total flying insect biomass in protected areas. PLoS ONE. 12 (10):eo185809.

Jones, E.L. & Leather, S.R. (2012) Invertebrates in urban areas: a review.  European Journal of Entomology, 109, 463-478.

Knowler, J.T., Flint, P.W.H., & Flint, S. (2016) Trichoptera (Caddisflies) caught by the Rothamsted Light Trap at Rowardennan, Loch Lomondside throughout 2009. The Glasgow Naturalist, 26, 35-42.

Thomas, J.A., Telfer, M.G., Roy, D.B., Preston, C.D., Greenwood, J.J.D., Asher, J., Fox, R., Clarke, R.T. & Lawton, J.H. (2004) Comparative losses of British butterflies, birds, and plants and the global extinction crisis.  Science, 303, 1879-1883.

 

 

Ten Papers that shook my World – Root (1973) – When more means less – crop diversity reduces pest incidence

I can’t remember when I first read this paper but judging by the record card and the state of the actual hard copy of the paper, it was probably when I was doing my PhD in the late 1970s. This paper and its companion, which was published a year earlier* (Tahvanainen & Root, 1972), have had a significant effect on the scientific understanding and development of inter-cropping as a method of crop protection worldwide. Although inter-cropping in some form or another has been around a long time, the idea that it could be used as part of an integrated pest management programme was not proven.  In this landmark study, Root compared pure stands (plots) of collards (spring greens in the UK) (Brassica olercaea) with adjacent rows of collards grown intermingled with other herbaceous plants.  His premise being that it was well documented that pest outbreaks tend to be associated with pure monocultures of crops (Pimentel, 1961; Janzen, 1970) and he wished to test the hypothesis that natural enemies were more abundant and effective in vegetationally diverse areas  than in pure monocultures, the so-called ‘enemies hypothesis’.  This idea had been around a surprisingly long time e.g. Ullyett (1947) who remarked  “where weeds occur around headlands and in hedges, they should be left for the purpose of supporting parasites and predators important in the natural control of the diamond-back moth (Plutclla maculipennis Curt)”.  A decade later, Elton (1958,) refers to this statement, explaining that “these hedge rows form a reservoir for enemies and parasites of insects and mite pests of crops”.  I am not sure what it indicates but note that many groups around the world, including mine, are still working on this both at the local (field-scale) level (e.g. Ramsden et al., 2014) and landscape level (e.g. Rusch et al., 2013; Raymond et al., 2015).

Root explained the premise of the ‘enemies hypothesis’ as follows.  Predators and parasites are more effective at controlling herbivore populations in diverse habitats or plant communities because, diverse plant communities support a diversity of herbivores with a variety of phenologies, providing a steady supply of prey for the predators.  In addition, complex environments provide prey refugia, thus allowing the prey not to be completely eradicated.  Diverse plant communities also provide a broad range of additional resources for adult natural enemies e.g. pollen and nectar.

Root ran his experiment for three years and did indeed find a significant difference in herbivore load between the pure plots and the weedy rows, the former having a greater abundance of pests (mainly aphids and flea beetles) than the latter.

From Root (1973)

To his disappointment (I assume), he did not find any difference in the numbers of natural enemies between the two treatments. He thus had to come up with another idea to explain his results. His ingenious explanation is encapsulated in what he termed the Resource concentration hypothesis which states that herbivores are more likely to find and stay on hosts growing in dense or nearly pure stands and that the most specialised species often reach higher relative densities in simple environments.

Typical modern monocultures, beans, cabbages and wheat

He hypothesised that specialist herbivores were ‘trapped’ on the crop and accumulated whilst more generalist herbivores were able to and likely to move away from the crops to other host plants.  Root added that the ‘trapping effect’ of host patches depends on several factors such as stand size and purity.

In 1968, presumably as a result of what Root was discovering, Jorma Tahvanainen (one of the many great Finnish entomologists who appeared on the scene in the 1970s -, he retired in 2004) came to Cornell to do his PhD with Richard Root. Working on the same system and in the same meadow, Tahbanainen developed two new hypotheses to explain why more diverse cropping systems have fewer pest problems than monocultures. His experiments as he too found little evidence of natural enemies having an effect. He developed two new hypotheses, one he termed Associational resistance which I reproduce below exactly as published:

A natural community, such as a meadow, can be treated as a compound system composed of smaller, component communities (Root, 1973). The arthropods associated with different plant species represent important components in terrestrial systems. The available information indicates that the biotic, structural and microclimatic complexity of natural vegetation greatly ameliorates the herbivore pressure on these individual components, and consequently, on the system as a whole. Thus, it can be said that in a compound community there exists an “associational resistance” to herbivores in addition to the resistance of individual plant species. If the complex pattern of natural vegetation is broken down by growing plants in monocultures, most of this associational resistance is lost. As a result, specialized herbivores which are adapted to overcome the resistance of a particular plant species, and against which the associational resistance is most effective, can easily exploit the simplified system. Population outbreaks of such herbivores are thus more likely to occur in monocultures where their essential resources are highly concentrated

The other, is the Chemical Interference Hypothesis, in which he postulated that reduced herbivory in diverse communities due to chemical stimuli produced by non-host plants interfering with host finding or feeding behaviour of specialist herbivores.  His experimental set-up was very simple, but very effective.

How to send mixed signals to specialist herbivores – reproduced from Tahvanainen & Root (1972)

In simple terms, a monoculture sends out a very strong signal, it could be olfactory, e.g. a strong bouquet of crucifer volatiles, or for other herbivores it could be visual, or a combination of the two.

Conventional intensive agricultural landscape sending out strong ‘signals’ to specialist herbivores

Inter-cropping increases crop diversity and changes the crop ‘signal’ to one that now ‘confuses’ specialists. Note that I am not necessarily advocating a combined crop of wheat, beans and cabbages, as harvesting would be a nightmare 😉

 

The intercrop melange effect

These two papers have had a huge influence on the theory and practice of inter-cropping and agricultural diversification, although Root (1973) has had many more citations (1393 according to Web of Science on 11^th December 2015) than Tahvanainen & Root (1972) which has only had a meagre 429 citation to date.  The message coming out from the many studies that have now investigated the effect of intercropping crop diversification on pest abundance, is, that in general, polyculture is beneficial in terms of promoting biological control and that incorporating legumes into the system gives the best yield outcomes (Iverson et al,  2014).

Another take on intercropping that overcomes the potential problems of harvesting different crops from the same field, is the concept of planting different genotypes of the same species. Resistant plants tend to have fewer generalists present, although their individual yield may be reduced.  By planting a mixture of susceptible and resistant genotypes it is however, possible to have your cake and eat it, especially if it is not essential to have a single genotype crop.  This approach has been used to good effect in the production of short rotation willow coppice, where planting diverse genotypes of the same species reduces both pest and disease levels (Peacock et al., 2000, 2001).

Who would have that two simple field experiments conducted in an abandoned hay meadow outside Ithaca, New York almost fifty years ago would have such a far-reaching influence?

 

References

Elton, C. S. (1958) The Ecology of Invasions by Animals and Plants. London: Methuen & Co., Ltd. 159 pp.

Iverson, A. L., Makin, L. E., Ennis, K. K., Gonthier, D. J., Connor-Barrie, B. T., Remfret, J. L., Cardinale, B. J. &Perfecto, I. (2014). Do polycultures promote win-win or trade-offs in agricultural ecosystem services? A meta-analysis. Journal of Applied Ecology. 51, 1593-1602.

Peacock, L. & Herrick, S. (2000) Responses of the willow beetle Phratora vulgatissima to genetically and spatially diverse Salix spp. plantations. Journal of Applied Ecology, 37, 821-831.

Peacock, L., Hunter, T., Turner, H., & Brain, P. (2001) Does host genotype diversity affect the distribution of insect and disease in willow cropping systems? Journal of Applied Ecology, 38, 1070-1081

Janzen, D.H. (1970) The unexploited tropics.  Bulletin of the Ecological Society of America, 51, 4-7

Pimentel, D. (1961). Species diversity and insect population outbreaks. Annals of the Entomological Society of America, 54, 76-86.

Ramsden, M. W., Menéndez, R., Leather, S. R. & Wackers, F. (2014). Optimizing field margins for biocontrol services: the relative roles of aphid abundance, annual floral resource, and overwinter habitat in enhancing aphid natural enemies. Agriculture Ecosystems and Environment, 199, 94-104.

Raymond, L., Ortiz-Martinez, S. A. &Lavandero, B. (2015). Temporal variability of aphid biological control in contrasting landscape contexts. Biological Control , 90, 148-156.

Root, R. B. (1973). Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards. Ecological Monographs, 43, 95-124.  1393 citations

Rusch, A., Bommarco, R., Jonsson, M., Smith, H. G. &Ekbom, B. (2013). Flow and stability of natural pest control services depend on complexity and crop rotation at the landscape scale. Journal of Applied Ecology, 50, 345-354.

Tahvanainen, J. & Root, R. B. (1972). The influence of vegetational diversity on the population ecology of a specialized herbivore Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia, 10, 321-346. 429 citations

Ullyett, G. C. (1947) Mortality factors in populations of Plutella maculipennis Curtis (Tineidae: Lep.) and their relation to the problem of control. Union of South Africa, Department of Agriculture and Forestry, Entomology Memoirs, 2, 77-202.

Post script

*I suspect, judging by how the two papers cite each other, that the Root (1973) paper was actually submitted first but that the vagaries of the publication system ,  meant that follow-up paper, Tahvanainen & Root (1972) appeared first.