Ten Papers that Shook My World – Owen & Weigert (1976) – The things that eat you are good for you

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.

O&W1O&W2O&W3

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 😉

New Scientist cover

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.

References

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.

Choudhury, D. (1985) Aphid honeydew – a re-appraisal of Owen and Wiegert’s hypothesis. Oikos, 45, 287-289.

Leather, S.R. (1988) Consumers and plant fitness: coevolution or competition ? Oikos, 53, 285-288.

Leather, S.R. (2000) Herbivory, phenology, morphology and the expression of sex in trees: who is in the driver’s seat? Oikos, 90, 194-196.

McArt, S.H., Halitschke, R., Salminen, J.P. & Thaler, J.S. (2013)  Leaf herbivory increases plant fitness via induced resistance to seed predators.  Ecology, 94, 966-975.

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. (1980). How plants may benefit from the animals that eat them. Oikos 35: 230-235.

Owen, D.F. & Wiegert, R.G. (1976) Do consumers maximise plant fitness? Oikos, 27, 488-492

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. (1982) Grasses and grazers: is there a mutualism ? Oikos, 38, 258-259.

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.

 

Post script

Denis Owen died at a relatively young age and for those interested in his career and life, his obituary can be found here.

 

 

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5 Comments

Filed under Aphids, Ten Papers That Shook My World

5 responses to “Ten Papers that Shook My World – Owen & Weigert (1976) – The things that eat you are good for you

  1. Fascinating! I can fret less when I see some aphids or other beasties on my plants. Amelia

    Liked by 1 person

  2. Thanks Simon, brought back a lot of memories of Denis who was in fact one of my PhD supervisors (albeit of the arms-length variety). “Eccentric” would certainly describe him – one of the last old school colonial naturalists. Productive and influential in his own way, he certainly had some odd ideas, but also some interesting ones. He was one of the first people to point out that ichneumonid wasps have a reverse latitudinal gradient, being more diverse in the temperate zone (though that’s a conclusion that’s recently been challenged). As well as that Independent obituary there’s also a Wikipedia entry for him – https://en.wikipedia.org/wiki/Denis_Owen

    Liked by 1 person

    • Thanks Jeff – I once had a literary spat with him about using host plant records for species-area relationships 😉 Leather, S. R. (1990). The analysis of species-area relationships, with particular reference to macrolepidoptera on. The Entomologist 109: 8-16.

      Liked by 1 person

      • Doesn’t surprise me. He was a great naturalist but no quantitative ecologist. I recall him drawing arrows all over a graph trying to explain to me that there were alternatives to directional/stabilising/disruptive selection in a population, but his explanation made no sense as far as I could see because his arrows were at all sorts of odd angles. The only thing `i took away from that supervisory meeting was “don’t take the opinions of “experts” at face value” 🙂

        Liked by 1 person

  3. Pingback: Ten papers that shook my world – Way & Banks (1964) – counting aphid eggs to protect crops | Don't Forget the Roundabouts

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