Journal clubs have been around a long time, but as a new PhD student in 1977 it was a new experience for me. I was thus somewhat uncertain about what was expected from me when my supervisor presented me with a copy of Owen, D.F. & Wiegert, R.G. (1976) Do consumers maximise plant fitness? Oikos, 27, 488-492, and informed me that I was going to present my views on the paper the following month. In those days organised PhD training programmes in the UK did not exist. Nowadays, PhD students in the UK follow a programme of lectures and workshops ranging from statistics, presentation skills, paper writing, ethics, use of social media, how to run tutorials, IPR, critical appraisal, etc. etc. Given my lack of experience, I was a little apprehensive to say the least. Luckily I had the chance to see how the older members of our research group dealt with their papers in the preceding weeks and was somewhat moe confident about what was expected of me. I duly read the paper and highlighted the areas that I wanted to critique.
Parts of the Owen & Weigert (1976) paper showing the bits that I highlighted for my critique.
Owen & Weigert’s hypothesis was, that contrary to accepted doctrine, consumers, especially those feeding on trees, were beneficial to their host plants and not harmful. Coming fresh from an agriculture department where I had been taught that anything that ate a plant was a pest, this was a startling and heretical concept for me to digest! I remember at the time that I was not particularly convinced by the arguments and that within the group the general consensus was that Denis Owen was a bit of an eccentric. In fact, the senior members of the group entered into a printed debate in the popular scientific press (McLean et al., 1977; Owen, 1977) which resulted in what I still consider to be the best ever front cover of New Scientist 😉
Arguably the best ever front cover of New Scientist
We were not the only ones who expressed scepticism about Owen’s hypothesis, although experimental rebuttals of Owen’s claim that aphids and trees were in a mutualistic relationship via honeydew production did not appear until some years later (Petelle, 1980; Choudhury, 1984, 1985). These papers resulted in a series of spirited responses from Owen (Owen & Wiegert, 1982a, b, 1985, 1987). Some years later, however, Joy Belsky provided further evidence against Owen’s hypothesis (Belsky, 1986,1987; Belsky et al., 1993) and I too entered the fray (Leather, 1988,2000).
Thus by the end of the last century it appeared that all the evidence indicated that if you were a plant, being eaten was not good for you. On the other hand, if Owen had posed his hypothesis at a population or group level, he might have been able to make a better case for herbivores increasing plant fitness. In an earlier post, in which I wrote about the plant immune response and how plants communicate with each other when attacked and warn their neighbours of potential attack, one could definitely make a stronger case for plants benefitting from being eaten. Induced resistance can even work at an individual level, some recent work (McArt et al., 2013) has shown that evening primroses (Oenothera biennis) attacked early in the season by the Japanese beetle, Popillia japnonica, become more resistant to attack from seed predators than those that escape early season defoliation. As a result the beetle attacked plants produce more seed than those that escaped attack. Given that a general measure of fitness is reproductive success (i.e. how many seeds are produced) then in this case, consumers do maximise plant fitness and Denis Owen can have the last word.
Belsky, A.J. (1986) Does herbivory benefit plants? A review of the evidence. American Naturalist 127, 870-892
Belsky, A.J. (1987) The effects of grazing: confounding of ecosystem, community and organism scales. American Naturalist, 129, 777-783.
Belsky, A.J., Carson, W.P., Jensen, C.L. & Fox, G.A, (1993) Overcompensation by plants – herbivore optimization or red herring. Evolutionary Ecology, 7, 109-121.
Choudhury, D. (1984) Aphids and plant fitness – a test of Owen and Wiegert’s hypothesis. Oikos, 43, 401-402.
McLean, I., Carter, N., & Watt, A. (1977) Pests out of Control. New Scientist, 76, 74-75.
Owen, D.F. (1977) Are aphids really plant pests? New Scientist, 76, 76-77.
Owen, D.F. & Wiegert, R.G. (1982) Beating the walnut tree: more on grass/grazer mutualism. Oikos, 39, 115-116.
Owen, D.F. & Wiegert, R.G. (1984) Aphids and plant fitness. Oikos, 43, 403.
Owen, D.F. & Wiegert, R.G. (1987). Leaf eating as mutualism. In Insect Outbreaks (ed. by P. Barbosa & J.C. Schultz), pp. 81-95. Academic Press, New York.
Petelle, M. (1980) Aphids and melezitose: a test of Owen’s 1978 hypothesis. Oikos, 35, 127-128.
Denis Owen died at a relatively young age and for those interested in his career and life, his obituary can be found here.