Seed mass, habitat and life history: a re-analysis of Salisbury (1942, 1974)

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1 New Phytol. (1998), 138, Seed mass, habitat and life history: a re-analysis of Salisbury (1942, 1974) BY KEN THOMPSON * AND DUNMAIL J. HODKINSON Unit of Comparative Plant Ecology, Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK ADAS Newcastle, Kenton Bar, Newcastle-upon-Tyne NE1 2YA, UK (Received 11 April 1997; accepted 12 September 1997) SUMMARY A recent re-analysis of the data of Salisbury (1974) claims his data do not support the hypothesis that seeds of species from shaded habitats are heavier than those from unshaded habitats, partly because the original analysis was inappropriate and partly because of bias in the dataset. We show first that the re-analysis itself contains errors, and second that the charge of bias is based largely on a misunderstanding. We also show that analysis of a larger dataset, drawn from Salisbury (1942) and from Salisbury (1974), provides convincing support for the hypothesis and suggests that the relationship is independent of life history. Key words: Seed size, phylogeny, shade, life history, congeners. INTRODUCTION The recent paper by Kelly (1997) is both an example of the resurgence of interest in the analysis of comparative datasets following the publication of Harvey & Pagel (1991), and testimony to the enduring interest of plant ecologists in the evolutionary ecology of seed size. In recent years, there has been much debate on the relationship between seed size and habitat variables (Foster & Janson, 1985; Foster, 1986; Hodgson & Mackey, 1986; Mazer, 1989, 1990; Kelly & Purvis, 1993; Kelly, 1995; Grubb & Metcalfe, 1996), and especially on what might be inferred from the data published by Salisbury (1942, 1974). The topic has also been extensively discussed at a recent Royal Society meeting; Rees (1996), Venable (1996) and Westoby, Leishman & Lord (1996) are particularly relevant here. Kelly (1997) asserted correctly that Salisbury (1942, 1974) did not use an appropriate statistical analysis and, with less justification, that in the 1974 paper his selection of data for analysis was biased. Here we point out firstly that Kelly s analysis itself contains errors, secondly that the charge of bias is based largely on a misunderstanding, and finally that more can be learned from analysis of a larger data set. * To whom correspondence should be addressed. ken.thompson sheffield.ac.uk RESULTS AND DISCUSSION From the tables and text of Salisbury (1974), Kelly (1997) was able to assemble 32 congeneric pairs. Changing taxonomy means that, strictly speaking, many of these pairs are no longer congeners, but we have throughout this paper retained Salisbury s taxonomy. Kelly (1997) restricted attention to 30 of these pairs, since two are technically ties. Kelly stated Two additional species pairs are noted in which there are habitat differences between the species, but no difference in size. In fact the dataset does not contain any ties of this sort. It does contain ties in which there are differences in seed size between the species (Polygonum aviculare and P. raii, and Veronica persica and V. hederifolia), but no clear difference in light demand, and these are presumably the ties to which Kelly is referring. However, there are not two such ties, but four. It is easy to overlook the other two, since Salisbury is not exactly transparent on the subject. Three of the pairs mentioned in the text of Salisbury (1974) concern shingle species with unexpectedly large seeds. One of these, which concerns a genuine closed open habitat comparison, is Solanum dulcamara and its shingle relative var. maritima. The others are the shingle species Lathyrus maritimus and Honkenya (Arenaria) peploides. Here the congeners with which they are compared (L. aphaca and Arenaria montana, A. gothica and A. tenuifolia respectively) are also plants of open habitats. Indeed two of them (L. aphaca and

2 164 K. Thompson and D. J. Hodkinson Table 1. Mean log seed mass values (mg) of congeners of open and closed habitats Genus Open Closed Closed open Alchemilla Allium Alopecurus Arenaria Artemisia Asperula Astragalus Bromus Calamintha Campanula Cardamine Centaurea Colchicum Convolvulus Corydalis Daphne Euphorbia Festuca Galeopsis Galium Gentiana Geranium Gladiolus Helianthemum Hordeum Hypericum Juncus Lamium Lathyrus Leucojum Lithospermum Luzula Lysimachia Medicago Melampyrum Mercurialis Ononis Ornithogalum Oxalis Phleum Pimpinella Plantago Primula Scilla Sedum Senecio Silene Solanum Sonchus Stachys Stellaria Trifolium Vaccinium Veronica Viburnum Viola A. tenuifolia) also appear in Salisbury (1942), correctly classified as open habitat species. A careful reading of Salisbury (1974) shows that he did not intend the Lathyrus and Arenaria examples to be considered as closed open habitat comparisons, although the relevant paragraph is not very clear on a first reading. Therefore, the data set of Salisbury (1974) contains only 28 valid congeneric contrasts, of which 20 support the hypothesis and eight do not. So far we have followed Kelly (1997) in assuming that the data of Salisbury can be accepted at face value. In reality a good deal of uncertainty attaches to the question of how far congeners must differ in seed mass or in light demand before these differences are accepted as significant. For example, it could be argued that Centaurea jacea is not convincingly more shade tolerant than Centaurea cyanus or Calystegia sepium than Convolvulus arvensis. Most of Salisbury s congeneric comparisons of seed mass are based on single seed collections, yet Salisbury (1942) and (1974) together contain several examples of two collections. In such cases ratios of mean seed masses for the same species vary from 1 1 to2 6, suggesting that little confidence can be placed in comparisons of, e.g., Lysimachia nummularia (0 5 mg) and L. nemorum (0 526 mg), or Viburnum lantana (44 2 mg) and V. opulus (42 mg). Nevertheless, we do not feel that these problems create any consistent bias. Elimination of the doubtful cases described above, together with some others which for various reasons may be regarded as unsound, still leaves 20 valid comparisons, 17 supporting the hypothesis and three against. A second difficulty with Kelly s (1997) analysis is the choice of significance level. The hypothesis is clear: that seeds of plants of shaded habitats are heavier than those of open habitats. The correct test is therefore one-tailed, and not two-tailed as employed by Kelly (1997). If we re-analyse the 28 valid pairs with a one-tailed sign test, P (or if we restrict attention to the 20 cases remaining after eliminating doubtful contrasts, P ). In other words, the data in Salisbury (1974) support the hypothesis. A more fundamental problem, however, is the rationale for analysing the data in Salisbury (1974) in isolation. Salisbury (1942) had already provided a long list which demonstrated that closed-habitat congeners have heavier seeds. In his 1974 paper he was making a different point, i.e. that although this is generally the case, there might be circumstances where other selection pressures cause open-habitat congeners to have equally large, or even larger seeds. He then went on to provide a number of examples which illustrate this point. In other words, the data in Salisbury (1974) are biased in favour of congeneric pairs which do not support the original hypothesis. It is therefore perhaps not surprising that the support for the hypothesis provided by Salisbury (1974) is at the margin of significance. A more sensible course would be to combine the data from Salisbury (1942) and Salisbury (1974) and analyse the combined dataset. Accordingly we combined the data, averaging seed mass values if necessary to provide a single comparison per genus. In some cases this

3 Seed mass, habitat and life history 165 Table 2. Mean log seed mass values (mg) of congeners of open and closed habitats, where both congeners share the same life history Genus Open Closed Closed open Life history Allium Perennial Arenaria Annual Artemisia Perennial Asperula Perennial Astragalus Perennial Campanula Perennial Colchicum Perennial Convolvulus Perennial Corydalis Perennial Daphne Perennial Euphorbia Perennial Euphorbia Annual Festuca Perennial Galeopsis Annual Galium Annual Gentiana Annual Gladiolus Perennial Helianthemum Perennial Hypericum Perennial Lathyrus Perennial Leucojum Perennial Luzula Perennial Lysimachia Perennial Medicago Annual Melampyrum Annual Ornithogalum Perennial Oxalis Perennial Pimpinella Perennial Plantago Perennial Primula Perennial Scilla Perennial Sedum Perennial Senecio Perennial Solanum Perennial Vaccinium Perennial Viburnum Perennial meant taking the average of two seed mass values for the same species. On this occasion we made no allowance for possible unsound comparisons, but as discussed above we are confident that this introduced no systematic bias. Mass values were log -transformed before analysis. The result was 56 comparisons, of which 45 support the hypothesis, ten do not and one is a genuine tie, i.e. two species with the same seed mass value (Table 1). These data support the hypothesis at P (Z 4 585). The relatively large sample size in Table 1 enable us to tackle another problem, raised by Rees (1996). Many of the congeneric comparisons involve annuals of open habitats and perennials of closed habitats. It is therefore not easy to tell whether the relationship is primarily an effect of habitat or of life history. We therefore eliminated all those comparisons where the two taxa compared differed in life history. In some cases (e.g. Euphorbia) we were able to generate two comparisons for a single genus, because there were annuals and perennials of both closed and open habitats. The result was seven comparisons where both parts were annuals, and 29 where both were perennials (Table 2). The annual data set is too small to analyse in isolation, but a one-tailed sign test on either the perennial data alone or the combined data set provides strong support for the hypothesis that species of closed habitats have heavier seeds (n 29, Z 3 34, P and n 36, Z 3 5, P respectively). We therefore conclude that the data of Salisbury (1942, 1974) provide robust support for the hypothesis that species of closed habitats have heavier seeds than related species of open habitats, and that this relationship owes little to differences in life history. ACKNOWLEDGEMENTS This work was supported by the Natural Environment Research Council. We are very grateful for the constructive comments of Peter Grubb on an earlier version. REFERENCES Foster SA On the adaptive value of large seeds for tropical moist forest trees: a review and synthesis. Botanical Review 52:

4 166 K. Thompson and D. J. Hodkinson Foster SA, Janson CH The relationship between seed size and establishment conditions in tropical woody plants. Ecology 66: Grubb PJ, Metcalfe DJ Adaptation and inertia in the Australian tropical lowland rainforest flora: contradictory trends in intergeneric and intrageneric comparisons of seed size in relation to light demand. Functional Ecology 10: Harvey PH, Pagel MD The comparative method in evolutionary biology. Oxford: Oxford University Press. Hodgson JG, Mackey JML The ecological specialisation of dicotyledonous families within a local flora: some factors constraining optimization of seed size and their evolutionary significance. New Phytologist 104: Kelly CK Seed size in tropical trees: a comparative study of factors affecting seed size in Peruvian angiosperms. Oecologia 102: Kelly CK Seed mass, habitat conditions and taxonomic relatedness: a re-analysis of Salisbury (1974). New Phytologist 135: Kelly CK, Purvis A Seed size and establishment conditions in tropical trees: on the use of taxonomic relatedness in determining ecological patterns. Oecologia 94: Mazer SJ Ecological, taxonomic, and life history correlates of seed mass among Indiana Dune angiosperms. Ecological Monographs 59: Mazer SJ Seed mass of Indiana Dune genera and families: taxonomic and ecological correlates. Evolutionary Ecology 4: Rees M Evolutionary ecology of seed dormancy and seed size. Philosophical Transactions of the Royal Society of London B Biological Sciences 351: Salisbury EJ The reproductive capacity of plants. London: G. Bell & Sons. Salisbury EJ Seed size and mass in relation to environment. Proceedings of the Royal Society of London B186: Venable DL Packaging and provisioning in plant reproduction. Philosophical Transactions of the Royal Society of London B Biological Sciences 351: Westoby M, Leishman M, Lord J Comparative ecology of seed size and dispersal. Philosophical Transactions of the Royal Society of London B Biological Sciences 351:

5 Seed mass, habitat and life history 167 COLLEEN KELLY writes I thank Thompson & Hodkinson for noticing that I incorrectly implied my Table 1 included species pairs in which there are habitat differences between species, but no difference in size. As they point out, I included no such ties. Rather, as I noted in the footnote to Table 1, the species in question were not used in my analysis because Although there is a large difference in seed mass between these congeners, there is no difference in shade adaptation. Fortunately, this makes no difference to the analysis. Additionally, Thompson & Hodkinson assert it would have been a more sensible course to have used in my analysis data additional to that found in Salisbury (1974). That would indeed be a reasonable assertion if my goal had been to determine the overall likelihood of a functional relationship between seed size and habitat use. However, as I stated, my goal was to determine whether Salisbury (1974) may be cited as a test of postulated relationship, a concern which arose from seeing Salisbury (1974) used in this way. Thus, inclusion of extraneous data was not only unnecessary, to do so would have prevented evaluation of Salisbury (1974) as an independent instance of support for the hypothesis. A larger data set may well better accomplish Thompson & Hodkinson s quest for a relationship between seed size and habitat use, although these authors have not employed all the applicable data from their sources, e.g., Tables I, IV and VII from Salisbury (1942). They have also excluded from their life history analyses those species occurring in mixed pairs at the genus level. Inclusion of these data would have provided an increased sample size and, because the excluded species could be used to form contrasts at taxonomic levels above that of species within genera, would also allow investigation of patterns among higher taxa (sensu Kelly 1995, 1996; Grubb & Metcalfe 1996). Two additional points of Thompson & Hodkinson serve to illustrate how more and less conservative data treatments can produce very different results. I interpreted as examples contrary to Salisbury s hypothesis two comparisons that Thompson & Hodkinson assert Salisbury never intended to be used as such, and that they believe should therefore be excluded from my analysis. Regarding these species, Salisbury states that This and similar considerations may perhaps explain some of the occasional exceptions to the prevailing seed-mass relation. In the sentences immediately following (still within the paragraph), he lists the questioned examples, whilst also specifying another instance where seed size differences do not accompany habitat differences. I do not find that rereading changes my interpretation of the passage. In such an equivocal situation, it seems more helpful to recognize possible alternative readings, rather than to designate one or the other as right. I used a two-tailed, rather than one-tailed, sign test to assess the pattern of independent contrasts to be found in my analysis. Justifying their use of the latter, Thompson & Hodkinson state The hypothesis is clear: that seeds of plants of shaded habitats are heavier than those of open habitats. The directional hypothesis that larger seed masses are associated with shadier habitats was generated by analyses that have not appropriately accounted for the potential effects of taxonomic relatedness, and may or may not support the hypothesis. Hence, my choice of the more general test. The differences in methodology I have highlighted result in one alternative showing that an association between seed size and habitat type cannot be inferred, and the other, that it can. The negative results found by Thompson & Hodkinson in their analyses of annuals even when a larger dataset is used (7 contrasts are sufficient for the appropriate sign test; P 0 454) further underline the ambiguousness of the support for the hypothesis and suggests a more complex, or differing, causation at work than originally supposed. ACKNOWLEDGEMENTS I thank F. I. Woodward, T. R. E. Southwood, P. Harvey, A. Grafen and S. Clark for their comments. REFERENCES Grubb PJ, Metcalfe DJ Adaptation and inertia in the Australian tropical lowland rain-forest flora: contradictory trends in intergeneric and intrageneric comparisons of seed size in relation to light demand. Functional Ecology 10: Kelly CK Seed size in tropical trees: a comparative study of factors affecting seed size in Peruvian angiosperms. Oecologia 102: Kelly CK Seed mass, habitat conditions and taxonomic relatedness: a re-analysis of Salisbury (1974). New Phytologist 135: COMMENT In publishing papers by Thompson & Hodkinson and by Grubb in this issue, the journal has been pleased to reflect the lively debate that publication of Kelly (1997) stimulated. However, in this area, further commentaries on published data are discouraged. P. G. AYRES