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).
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).
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
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.
Figure 4. Strong’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.
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
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 😉