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 11th 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?
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.
*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.