Category Archives: Ten Papers That Shook My World

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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Ten Papers that Shook My World – Haukioja & Niemelä (1976) – the plant “immune response”

To me this is a landmark paper, both personally and for ecology in general.   I first came across it in the second year of my PhD at the University of East Anglia (1978) and given where it was published, would probably never have seen it if my supervisor, Tony Dixon, hadn’t had a collaborative link with Erkki Haukioja of Turku University (Finland).

That individual plants of the same species are more or less susceptible (constitutive or innate resistance) to pests and diseases has been known for a very long time (e.g. Painter, 1958; Beck, 1965) and has been exploited by plant breeders as part of many pest management programmes.  Despite the stunning footage of the questing bramble in David Attenborough’s classic documentary The Private Life of Plants, plants are often thought of as passive organisms.  The idea that plants might actually respond directly and quickly to insect attack was more in the realms of science fiction than science fact, but this all changed in the 1970s. In 1972 a short paper in Science (Green & Ryan, 1972) suggested that plants might not be as passive as previously thought. Green & Ryan working in the laboratory with the Colorado Potato Beetle, Leptinotarsus decemlineata, showed that when tomato leaves were damaged by beetle feeding the levels of a proteinase inhibitor were raised not just in the wounded leaves but in nearby leaves as well. As proteinase inhibitors were well-known to be part of the plant defence system, they hypothesised that this was a direct response of the plant to repel attack by pests and that it might be a useful tool in developing new pest management approaches. So what does this have to do with two Finnish entomologists?

Erkki Haukioja and his long-term collaborator, Pekka Niemelä were working on an important lepidopteran defoliator of birch, in the far north of Finland, at the Kevo Subarctic Research Station.Kevo

http://www.eu-interact.org/field-sites/finland-4/kevo/

The defoliator that they were working on was the autumnal moth, now Epirrita autumnata, but then Oporinia autumnata.

Epirrita

http://ukmoths.org.uk/show.php?bf=1797

The autumnal moth, as with many tree-feeding Lepidoptera, has a 7-10 year population cycle (Ruohmäki et al., 2000).

Population cycles

Natural enemies are often cited as the causes of these cycles (Turchin et al., 1999) although other factors such as weather (Myers, 1998) or even sunspot activity (Ruohmäki et al., 2000)

Sunspot

have also been suggested. It had also been suggested that the marked population cycles of the larch bud moth, Zeiraphere diniana were caused by changes in the susceptibility of their host trees after defoliation (Benz, 1974). In 1975, Haukioja and his colleague Hakala, attempting to explain the cyclical nature of the E. autumnata population cycles wondered if they were being driven by the insects themselves causing changes in the levels of chemical defence in the trees. To test this Erkki and Pekka did two neat field experiments, remember Green & Ryan’s work was laboratory based and did not test the effects seen on the insects. They first fed Epirrita larvae on foliage from previously defoliated and undefoliated birch trees and found that the pupae that developed from those larvae fed on previously defoliated trees were lighter than those that had fed on previously undefoliated trees (Hauikioja & Niemelä, 1976). At the same time they also did an experiment where they damaged leaves but then rather than feeding the larvae on those leaves, fed them on nearby adjacent undamaged leaves and compared them with larvae feeding on leaves from trees where no damage had occurred. Those larvae feeding on undamaged leaves adjacent to damaged leaves grew significantly more slowly than those feeding on leaves that came from totally undamaged trees (Haukioja & Niemelä, 1977). So pretty convincing evidence that the trees were responding directly to insect damage and altering their chemistry to become more resistant, i.e. an induced defence and not a constitutive one.

Their results had a major impact on the field. The great and the good from around the world found it a fascinating subject area and a plethora of papers investigating the effects of insect feeding on induced defences in birch and willow trees soon followed (e.g. Fowler & Lawton, 1984a; Rhoades, 1985; Hartley & Lawton, 1987) and not forgetting the original researchers (e.g. Haukioja & Hahnimäki, 1984). I, with the aid of colleagues, also added my ‘two pennorth’ (I did say the idea shook my world) by extending the concept to conifers (Leather et al., 1987; Trewhella et al., 1997). The terms rapid induced resistance and delayed induced resistance soon entered the language, the first to describe those changes that occurred within minutes of feeding damage and the second, those that did not take effect until the following year (Haukioja & Hahnmäki, 1984; Ruohmäki et al., 1992) Such was the interest generated by the topic that by 1989 there were enough studies for a major review to be published (Karban & Myers, 1989).

Controversy reared its ugly head early on when Doug Rhoades suggested that not only did plants resist insect attack actively but that they could talk to each other and warn their neighbours that the ‘bad guys’ were in the neighbourhood (Rhoades, 1983, 1985). This sparked a brief but lively debate (e.g. Fowler & Lawton, 1984b, 1985). Ironically it is now taken as axiomatic that plants talk to each other using a range of chemical signals (van Hulten et al., 2006; Heil & Ton, 2008) as well as informing the natural enemies of the pests that a suitable food source is available (e.g. Edwards & Wratten, 1983; Amo et al., 2013; Michereff et al., 2013).

Ton cartoon

A great cartoon from Jurriaan Ton at Sheffield University. https://www.shef.ac.uk/aps/staff-and-students/acadstaff/ton-jurriaan

We now have a greatly increased understanding of the various metabolic pathways that induce these defences against different insect pests (e.g. Smith & Boyko, 2007) and can, by genetically manipulating levels of compounds such as jasmonic and salicyclic acids or even applying them directly to plants affect herbivorous insect communities and their natural enemies thus improving crop protection (e.g. Thaler, 1999; Cao et al., 2014; Mäntyllä, 2014). No wonder this was an idea that shook my world, and yours.

 

Post script

The study of induced plant defences or resistance is now dominated by molecular biologists and current practice is to use the term priming and not induced defence. The increased understanding that this new generation has brought to the field is undeniable but I always feel it is a great shame that they seem to have forgotten those early pioneers in the field.

 

References

Amo, L., Jansen, J.J., Van Dam, N.M., Dicke, M., & Visser, M.E. (2013) Birds exploit herbivore-induced plant volatiles to locate herbivorous prey. Ecology Letters, 16: 1348-1355.

Baldwin, I.T. & Schultz, J.C. (1983) Rapid changes in tree leaf chemistry, induced by damage: evidence for communication between plants. Science, 221, 277-279.

Beck, S.D. (1965) Resistance of plants to insects. Annual Review of Entomology, 10, 207-232.

Benz, G. (1974). Negative Ruckkoppelung durch Raum-und Nahrungskonkurrenz sowie zyklische Veranderung. Zeitschrift für Angewandte Enomologie, 76: 196-228.

Cao, H.H., Wang, S.H., & Liu, T.X. (2014) Jasomante- and salicylate-induced defenses in wheat affect host preference and probing behavior but not performance of the grain aphid, Sitobion avenae. Insect Science, 21, 47-55.

Edwards, P.J. & Wratten, S.D. (1983) Wound induced defences in plants and their consequences for patterns of insect grazing. Oecologia, 59: 88-93.

Fowler, S.V. & Lawton, J.H. (1984a) Foliage preferences of birch herbivores: a field manipulation experiment. Oikos, 42: 239-248.

Fowler, S.V. & Lawton, J.H. (1984b) Trees don’t talk : do they even murmur? Antenna, 8: 69-71.

Fowler, S.V. & Lawton, J.H. (1985) Rapidly induced defences and talking trees: the devils’ advocate position. American Naturalist, 126: 181-195.

Green, T.R. & Ryan, C.A. (1972) Wound induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science: 175: 776-777.

Hartley, S.E. & Lawton, J.H. (1987) Effects of different types of damage on the chemistry of birch foliage and the responses of birch feeding insects. Oecologia, 74: 432-437.

Haukioja, E. & Hakala, T. (1975) Herbivore cycles and periodic outbreaks. Report of the Kevo Subarctic Research Station, 12: 1-9

Haukioja, E. & Hanhimäki, S. (1984) Rapid wound induced resistance in white birch (Betula pubescens) foliage to the geometrid Epirrita autumnata: a comparison of trees and moths within and outside the outbreak range of the moth. Oecologia, 65, 223-228.

Haukioja, E. & Niemelä, P. (1976). Does birch defend itself actively against herbivores? Report of the Kevo Subarctic Research Station 13: 44-47.

Haukioja, E. & Niemelä, P. (1977). Retarded growth of a geometrid larva after mechanical damage to leaves of its host tree. Annales Zoologici Fennici 14: 48-52.

Heil, M. & Ton, J. (2008) Long-distance signalling in plant defence. Trends in Plant Science, 13: 264-272.

Karban, R. & Myers, J.H. (1989) Induced plant responses to herbivory. Annual Review of Ecology & Systematics, 20: 331-348.

Leather, S.R., D., W.A., & Forrest, G.I. (1987) Insect-induced chemical changes in young lodgepole pine (Pinus contorta): the effect of previous defoliation on oviposition, growth and survival of the pine beauty moth, Panolis flammea. Ecological Entomology, 12: 275-281.

Mäntyllä, E., Blande, J.D., & Klemola, T. (2014) Does application of methyl jasmonate to birch mimic herbivory and attract insectivorous birds in nature? Arthropod-Plant Interactions, 8, 143-153.

Michereff, M.F.F., Borges, M., Laumann, R.A., Dinitz, I.R., & Blassioli-Moraes, M.C. (2013) Influence of volatile compounds from herbivore-damaged soybean plants on searching behavior of the egg parasitoid Telonomus podisi. Entomologia experimentalis et applicata, 147: 9-17.

Trewhella, K.E., Leather, S.R., & Day, K.R. (1997) Insect induced resistance in lodgepole pine: effects on two pine feeding insects. Journal of Applied Entomology, 121: 129-136.

Myers, J. H. (1998). Synchrony in outbreaks of forest lepidoptera: a possible example of the Moran effect. Ecology 79: 1111-1117.

Painter, R.H. (1958) Resistance of plants to insects. Annual Review of Entomology, 3: 267-290.

Rhoades, D.F. (1983) Responses of alder and willow to attack by tent caterpillar and webworms: evidence for pheromonal sensitivity of willows. American Chemical Society Symposium Series, 208: 55-68.

Rhoades, D.F. (1985) Offensive-defensive interactions between herbivores and plants: their relevance in herbivore population dynamics and ecological theory. American Naturalist, 125: 205-238.

Ruohomäki, K., Hanhimäki, S., Haukioja, E., Iso-iivari, L., & Neuvonen, S. (1992) Variability in the efficiency of delayed inducible resistanec in mountain birch. Entomologia experimentalis et applicata, 62: 107-116.

Ruohmäki, K., Tanhuanpää, M., Ayres, M.P., Kaitaniemi, P., Tammaru, T. & Haukioja, E. (2000) Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice. Population Ecology, 42: 211-223

Smith, C.M. & Boyko, E.V. (2007) The molecular basis of plant resistance and defence responses to aphid feeding: current status. Entomologia experimentalis et applicata, 122: 1-16.

Thaler, J. (1999) Induced resistance in agricultural crops: effects of Jasmonic acid on herbivory and yield in tomato plants. Environmental Entomology, 28, 30-37.

Turchin, P., Taylor, A. D. &Reeve, J. D. (1999). Dynamical role of predators in population cycles of a forest insect: an experimental test. Science 285: 1068-1071.

Van Hulten, M., Pelser, M., van Loon, L.C., Pieterse, C.M.J. & Ton, J. (2006) Costs and benefits of priming for defense in Arabidopsis. Proceedings of the National Academy of Sciences USA, 103: 5602-5607.

 

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Entomological Classics – Southwood 1961 – The number of insect species associated with various trees

 

Nineteen-Sixty-One  was a momentous  year for entomology and ecology, although at the time I suspect few realised it.  Skip forward to 2013 when The British Ecological Society published a slim volume celebrating  the 100 most influential papers published in the Society’s journals.  The papers included in the booklet were selected based on the opinions of 113 ecologists from around the world, who were then asked to write a short account of why they thought that paper influential.  I was disappointed not to be asked to write about my nomination but instead asked to write about Maurice Solomon’s 1949 paper in which he formalised the term functional response.

The paper I had wanted to write about was included, but John Lawton had the privilege of extolling its virtues, and given the word limits did a pretty good job.  I do, however, feel that given its importance to ecology and entomology it deserves a bit more exposure, so I am taking the opportunity to write about it here.  I could have included this post in a series I have planned, called Ten Papers that Shook My World, but given the impact that this paper has had on entomologists I felt it deserved an entry in my Entomological Classics series.

For those of you who haven’t come across this paper before, this was an astonishingly influential paper.  Basically, Southwood, who despite his later reputation as one of the ecological greats, was an excellent entomologist, (in fact he was a Hemipterist), wanted to explain why some tree species had more insect species associated with them than others.  He made comparisons between trees in Britain, Russia and Cyprus and demonstrated that those trees that were more common and had a wider range had more insect species associated with them (Figure 1).

Southwood 1961 Fig 1

From Southwood 1961.  I was surprised to see that he had committed the cardinal error in his Figure caption of describing it as Graph and also including the regression equation in the figure pane; two things that I constantly reprimand students about!

Importantly he also showed that introduced trees tended to have fewer insects than native species.  He thus hypothesised that the number of insects associated with a tree species was proportional to its recent history and abundance and was a result of encounter rates and evolutionary adaptation.  He then tested this hypothesis using data on the Quaternary records of plant remains from Godwin (1956) making the assumption that these were a proxy for range as well as evolutionary age.

He commented on the outliers above and below the line suggesting that those above the line were a result of having a large number of congeners and those below the line either as being taxonomically isolated and/or very well defended.

He then went on to test his ideas about the evolutionary nature of the relationship by looking at trees and insects in Hawaii, (ironically this appeared in print (Southwood, 1960), before the earlier piece of work (Journal of Animal Ecology obviously had a slower turnaround time in those days than they do now).

Hawaiin figure

Figure 2.  Relationship between tree abundance and number of insect species associated with them (drawn using data from Southwood 1960).

Considering the research that these two papers stimulated over the next couple of decades, what I find really odd, is that Southwood, despite the fact that he was dealing with data from islands and that Darlington (1943) had published a paper on carabids on islands and mountains in which he discussed species-area relationships and further elaborated on in his fantastic book (Darlington, 1957), did not seem to see the possibility of using the species-area concept to explain his results.  It was left to Dan Janzen who in 1968 wrote

It is unfortunate that the data on insect-host plant relationships have not in general been collected in a manner facilitating analysis by MacArthur and Wilson’s methods (as is the case as well with most island biogeographical data). What we seem to need are lists of the insect species on various related and unrelated host plants, similarity measures between these lists (just as in Holloway and Jardine’s 1968 numerical taxonomic study of Indo- Australian islands), knowledge of the rates of buildup of all phytophagous insect species on a host plant new to a region, where these species come from, etc. Obviously, the insect fauna must be well known for such an activity. The English countryside might be such a place; it has few “islands” (making replication difficult) but a very interesting “island” diversity, with such plants as oaks being like very large islands and beeches being like very small ones, if the equilibrium number of species on a host plant (Elton, 1966; Southwood, 1960) is any measure of island size.”

 

In 1973 Dan Janzen  returned to the subject of trees as islands and cited Paul Opler’s 1974 paper in relation to the fact that the number of  herbivorous insects associated with a plant increases with the size of the host plant population (Figure 3), and further reiterated

Opler Figure

Figure 3.  Opler’s 1974 graph showing relationship between range of oak trees in the USA and the number of herbivorous insect species associated with them.

 his point about being able to consider trees as ecological islands.  Opler’s 1974 paper is also interesting in that he suggested that this approach could be used for predicting pest problems in agricultural systems, something that Don Strong and colleagues did indeed do (Strong et al., 1977; Rey et al., 1981), and that the concept of habitat islands and the species-area relationship could be used when designing and evaluating nature reserves, something which indeed has come to pass.

Again in 1974 but I think that Strong has precedence because Opler cites him in his 1974 paper, Don Strong reanalysed Southwood’s 1961 data using tree range (based on the Atlas of the British Flora)  as the explanatory variable  (figure 4) to explain the patterns seen.

Strong Figure

Figure 4Strong’s reworking of Southwood’s 1961 insect data using the distribution of British trees as shown in Perring & Walters1 (1962).

The publication of this paper opened the floodgates, and papers examining the species-area relationships of different insect groups and plant communities proliferated (e.g  leafhoppers (Claridge & Wilson, 1976); bracken (Rigby & Lawton, 1981); leaf miners (Claridge & Wilson, 1982); rosebay willow herb (McGarvin, 1982), with even me making my own modest contribution in relation to Rosaceous plants   (Leather, 1985, 1986).

Although not nearly as popular a subject as it was in the 1980s, people are still extending and refining the concept  (e.g. Brändle & Brandl, 2001; Sugiura, 2010; Baje et al., 2014).

Southwood (1961) inspired at least two generations of entomologists and ecologists, including me, and is still relevant today.  It is truly an entomological (and ecological) classic.

References

Baje, L., Stewart, A.J.A. & Novotny, V. (2014)  Mesophyll cell-sucking herbivores (Cicadellidae: Typhlocybinae) on rainforest trees in Papua New Guinea: local and regional diversity of a taxonomically unexplored guild.  Ecological Entomology 39: 325-333

Brändle, M. &Brandl, R. (2001). Species richness of insects and mites on trees: expanding Southwood. Journal of Animal Ecology 70: 491-504.

Claridge, M. F. &Wilson, M. R. (1976). Diversity and distribution patterns of some mesophyll-feeding leafhoppers of temperate trees. Ecological Entomology 1: 231-250.

Claridge, M. F. &Wilson, M. R. (1982). Insect herbivore guilds and species-area relationships: leafminers on British trees. Ecological Entomology 7: 19-30.

Darlington, P. J. (1943). Carabidae of mountains and islands: data on the evolution of isolated faunas and on atrophy of wings. Ecological Monographs 13: 37-61.

Darlington, P. J. (1957). Zoogeography: The Geographical Distribution of Animals. New York: John Wiley & Sons Inc.

Elton, C. S. (1966). The Pattern of Animal Communities. Wiley, New York.

Holloway, J. D., & Jardine, N. (1968). Two approaches to zoogeography: a study based on the distributions of butterflies, birds and bats in the Indo-Australian area. Proceedings of the Linnaean Society. (London) 179:153-188.

MacArthur, R. H. & Wilson, E.O. (1967). The Theory of Island Biogeography. Princeton University Press, Princeton, N. J

Janzen, D. H. (1968). Host plants as islands in evolutionary and contemporary time. American Naturalist 102: 592-595.

Janzen, D. H. (1973). Host plants as islands II.  Competitive in evolutionary and contemporary time. American Naturalist 107: 786-790.

Kennedy, C.E.J. & Southwood, T.R.E. (1984) The number of species of insects associated with British trees: a re-analysis. Journal of Animal Ecology 53: 455-478.

Leather, S. R. (1985). Does the bird cherry have its ‘fair share’ of insect pests ? An appraisal of the species-area relationships of the phytophagous insects associated with British Prunus species. Ecological Entomology 10: 43-56.

Leather, S. R. (1986). Insect species richness of the British Rosaceae: the importance of hostrange, plant architecture, age of establishment, taxonomic isolation and species-area relationships. Journal of Animal Ecology 55: 841-860.

Macgarvin, M. (1982). Species-area relationships of insects on host plants: herbivores on rosebay willowherbs. Journal of Animal Ecology 51: 207-223.

Opler, P. A. (1974). Oaks as evolutionary islands for leaf-mining insects. American Scientist 62: 67-73.

Perring, F.J. & Walters, S.M. (1962) Atlas of the British Flora BSBI Nelson, London & Edinburgh.

Preston,  C.D., Pearman, D.A. & Tines, T.D. (2002) New Atlas of the British and Irish Flora: An Atlas of the Vascular Plants of Britain, Ireland, The Isle of Man and the Channel Islands. BSBI, Oxford University Press

Rigby, C. & Lawton, J. H. (1981). Species-area relationships of arthropods on host plants: herbivores on bracken. Journal of Biogeography 8: 125-133.

Solomon, M. E. (1949). The natural control of animal populations. Journal of Animal Ecology 18: 1-35

Southwood, T. R. E. (1960). The abundance of the Hawaiian trees and the number of their associated insect species. Proceedings of the Hawaiian Entomological Society 17: 299-303.

Southwood, T. R. E. (1961). The number of species of insect associated with various trees. Journal of Animal Ecology 30: 1-8.

Sugiura, S. (2010). Associations of leaf miners and leaf gallers with island plants of different residency histories.  Journal of Biogeograpgy 37: 237-244

Rey, J.R.M.E.D. & Strong, D.R. (1981) Herbivore pests, habitat islands, and the species area relation. American Naturalist 117: 611-622.

Strong, D. R. (1974). The insects of British trees: community equilibrium in ecological time. Annals of the Missouri Botanical Gardens 61: 692-701.

Strong, D.R., D., M.E., & Rey, J.R. (1977) Time and the number of herbivore species: the pests of sugarcane. Ecology 58: 167-175

 

1Postscript

The Atlas of the British Flora by Perring and Walters (1962) was an iconic piece of work, although not without its flaws.  As with many distribution atlases it is based on a pence or absence score of plant species within one kilometre squares.  So although it is a good proxy or range it does not necessarily give you an entirely reliable figure for abundance.  A dot could represent a single specimen or several thousand specimens.   Later authors attempted to correct for this by using more detailed local surveys e.g. tetrads.  It must have been particularly galling for  Southwood that the Atlas didn’t appear until after he had published his seminal papers, but he later made up for it by reanalysing and extending his data from that original 1961 paper (Kennedy et al., 1984).

Those of us working in this area using the original Atlas had to count the dots by hand, a real labour of love especially for those widely distributed species; the new edition (Preston et al., 2002) actually tells you how many dots there are so the task for the modern-day insect-plant species-area relationship worker is much easier 😉

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