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Juvenile growth and palatability in co-occurring, congeneric British herbs¹

²Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK; ³School of Biological Sciences, University of Southampton, Bassett Crescent East, Southampton SO16 7PX, UK

Received for publication October 8, 2004. Accepted for publication June 2, 2005.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Differential sensitivity (DS) storage dynamics describe a temporal niche axis that determines coexistence of competing taxa through a trade-off between environmental insensitivity and competitive ability at the recruitment stage. In DS storage dynamics, when the relevant environmental factor is low, the more sensitive, better competitor preferentially recruits; when the environmental factor is high, the environmentally sensitive species suffers high mortality and the environmentally insensitive taxon preferentially recruits. A herbivore defense/growth rate trade-off at the seedling/juvenile stage could support this dynamic. We therefore compared juvenile palatability, a measure of anti-herbivore defense, and early growth rate for five congeneric pairs of native British herbs. All five comparisons showed a positive association between average individual growth rate and average palatability to a native slug species. We observed no evidence of associations between early growth rate and adult palatability or between early growth rate and life history strategy (annual vs. perennial). Seed mass was not associated with either early growth rate or with life history strategy whether or not relatedness was taken into account. We offer two explanations as to why we found statistically significant support for a growth rate– defense trade-off when within-species studies so often produce only equivocal results.

Key Words: differential sensitivity storage dynamics • growth–defense trade-off • herbivory • juvenile palatability • slugs • species coexistence

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Despite the general expectation that plant defense from herbivory will entail costs (Herms and Mattson, 1992 ; Stamp, 2003 ), such costs have been difficult to document. Comparisons of seed set, fruit set, reproductive bud number, or size of plant at maturity (a correlate of seed set) when herbivory is not present have only infrequently shown a significant fitness difference between more and less well-defended plants (Bergelson and Purrington, 1995 ; Koricheva, 2002 ). However, juvenile survival is also a component of fitness, and recent work indicates that differences in juvenile mortality can underlie coexistence between closely related and otherwise similar taxa (Kelly and Bowler, 2002 , 2005 ; Kelly et al., 2005 ).

In the temporal niche axis described by Kelly and Bowler (2002 , 2005) , differential sensitivity to a fluctuating environmental factor coupled with a competitive trade-off allows competing taxa to alternate recruitment in time. That is, when the fluctuating environmental factor is high, juveniles of the sensitive taxon suffer higher mortality than those of its less sensitive competitor, and the less sensitive taxon preferentially recruits. When insensitivity entails a cost, during periods when the environmental factor is low, juveniles of the sensitive taxon are able to outcompete and preempt those of its less sensitive competitor, and the more sensitive taxon preferentially recruits.

Herbivore levels notably fluctuate from year to year (Price, 1997 ; Kelly et al., 2005 ). We predict that if this provides a framework for the DS storage dynamic described, the widely postulated, but difficult to document, herbivore trade-off between growth rate and defense will be effective at the seedling/ juvenile stage rather than at the level of the more oft-examined mature plant. When herbivore levels are high, better-defended seedlings will be more likely to survive herbivore attack than less well-defended seedlings, leaving establishment sites open for capture by the slower-growing—but alive—better-defended taxon (Hanley, 1998 ; Hanley and Lamont, 2001 ). When herbivore levels are low, less defended seedlings suffer lower levels of herbivore-induced mortality and their faster growth will allow them to better dominate establishment sites than seedlings carrying the burden of the now-devalued defense mechanisms.

To test our prediction of an association between investment in defense in juvenile plants and early growth rate, we compared juvenile palatability to slugs, a measure of defense, and early growth rate of five co-occurring, congeneric pairs of native British herbs (10 species). Molluscs (slugs and snails) are the principal herbivores of seedlings and juveniles in the herbaceous communities of the target species (Hanley, 1998 ). We compared congeneric pairs for two reasons. First, congeneric pairs offer a natural "all else being equal" experiment, where differences in defense are more likely to be quantitative than qualitative, and those qualitative differences are more likely to be simple additions or subtractions to those of the defense profile of its close relative (Berenbaum, 1981 ; Harborne, 1993 ). Second, the shared evolutionary history of these co-occurring pairs confers a fundamental physiological similarity that increases the chance and degree of competition (Kelly and Bowler, 2002 , 2003 , 2005 ). We found that in all five comparisons, average individual growth rate in juveniles was positively associated with average palatability of juveniles. We observed no evidence for associations between early growth rate and adult palatability or between early growth rate and life history strategy (annual vs. perennial). Seed mass was not associated with either early growth rate or with life history strategy whether or not relatedness was taken into account.

	MATERIALS AND METHODS

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The target species were Poa annua L. and P. pratensis L., Senecio vulgaris L. and S. jacobaea L., Stellaria media (L.) Vill. and S. graminea L., Trifolium pratense L. and T. dubium Sibth., and Urtica dioica L. and U. urens L. Seeds used for all assays (palatabilities, growth rate, seed mass) came from the same lots of seeds as in Fenner et al. (1999) supplied by Herbiseed (Wokingham, Berkshire, UK). Herbiseed collects seeds from naturally occurring plants at one or a few sites and either sells them or uses them to establish nursery-grown stock. To determine growth rates, seeds were germinated on moistened filter paper (Whatman No. 2) in Petri dishes placed inside a dark incubator set at a constant 15°C. Following germination (appearance of the radicle), 25 seedlings of each species were transferred to 76 mm diameter plastic pots containing Levingtons FS2 potting compost. The pots were randomly arranged in a greenhouse with mean daily temperatures varying between 15.0°C (SE ± 0.1°C) min and 22.7°C (±0.1) max, and watered daily. Twenty-eight days following germination, the plants were harvested and dried at 80°C for 24 h before being weighed. Because seeds of most of the species are quite small (0.004 g for 9 of the 10 species), seed mass was measured as an average of 20 replicates of batches of 10 seeds.

Palatability to native slugs (Deroceras reticulatum Müller) of both juvenile and mature plants of the 10 study species was taken from Fenner et al. (1999) , where the test protocol and the resulting palatability index followed Whelan (1982) . In brief, the palatability value for a target species was assessed relative to that of lettuce (Lactuca sativa L. cv. Little Gem) by offering individual slugs a choice between two agar discs, one containing an extract of the target species, the other an extract of lettuce. The measure represents the percentage removed from the standard-sized discs, averaged over 15 replicates. The quantity is determined as

"Adult" plant material was obtained from individuals that had been grown outdoors in pots for 6–10 weeks; "juvenile" material was harvested from seedlings when they had developed their first pair of true leaves, which varied according to species from 7 to 12 days. We chose to use plants of this age to maximize the probability we would be testing constitutive defense compounds; growing the seedlings to larger sizes would require handling that could stimulate inducible defenses. See Fenner et al. (1999) for further details of the palatability trials.

We compared absolute growth rates for our congeneric pairs rather than the more commonly used relative growth rates (cf. Fenner et al., 1999 ). The competitive advantage of the less over the more palatable seedling entails the former being better able to dominate an establishment site, making the relevant measure for our purposes that measure best indicating which seedling type will get bigger, faster (Kelly and Bowler, 2002 , 2005 ).

Analysis
There are several options in analyzing congeneric comparisons, with the most applicable depending on the nature of the data. If all of the data are normally distributed within all species for all target variables, it is possible to apply a mixed model ANOVA or MANOVA (Sokal, 1995 ). When the data are not normally distributed or cannot reasonably be made so, a Wilcoxon matched-pairs, signed-ranks test is sometimes applied. The Wilcoxon uses both the sign and the magnitude of differences between paired comparisons, and gives the probability that the distribution in the data is drawn from an underlying distribution function that is symmetric about zero (Wilcoxon, 1945). The test is based on the further assumption that the magnitudes of differences between pair members carries information additional to that carried by the signs—this need not be true. If the differences tested are well defined, then the Wilcoxon can be used. If the differences have such uncertainty that ranks could easily be shuffled, especially low ranks, then the ranks contain little information and it is not prudent to accept a Wilcoxon null probability that is lower than that from the sign test. It is likely that if the data are sufficient to determine that the assumptions are valid for a Wilcoxon, they will be sufficient for an analysis of variance. To calculate the nonparametric Wilcoxon and sign tests see Siegel and Castellan (1988)

An error has crept into the literature on the proper treatment of paired comparisons, wherein comparisons are limited to congener pairs showing significant differences in the target variable(s) or to congener pairs showing some a priori degree of difference (e.g., Armstrong and Westoby, 1993 ; Thompson and Hodkinson, 1998 ; Westoby, 2002 ). Such practices are statistically in error in producing a nonrandom selection of data, with the unfortunate capacity to bias results; the P value for the analysis cannot be inferred to demonstrate a simple conclusion of a general pattern of differences between species (Kelly, 1997 ). Ironically, exclusion of "too similar" pairs also conflicts with the fundamental reason for comparing closely related species: related species present a natural "all else being equal" experiment (Harvey and Pagel, 1991 ). The more different (and/or distantly related) the compared pair, the more the comparison deviates from its intended function.

We applied a sign test to our hypothesis of a positive relationship between palatability of juvenile plant tissue and early plant growth rate. Growth rates could be assumed to be normally distributed for only 9 of the 10 species, small sample size in the 10^th disallowing this inference. Additionally, palatability indices contained sufficient numbers of repeat ‘0’ or ‘1’ values in the raw data that there is no appropriate transformation to achieve a normal distribution, with occasions of overlap between species pairs in index distributions.

We also present data on adult palatability and on seed size. It is worth noting that it would be incorrect to subject our result to an analysis for repeated tests: we proposed one hypothesis and tested it. Ancillary data are presented primarily as a convenience to the reader who might otherwise assume that there are data supporting alternative explanations for our result.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Individual growth rate was positively associated with palatability in juveniles in all five comparisons (P = 0.031; Fig. 1a, b). We show measures of other variables obtained as bar graphs and a tabulation of regression analyses. Simple visual inspection is sufficient to conclude that neither adult palatability (Fig. 1c) nor seed mass (Fig. 1d) offered explanations for congeneric differences in early growth rate, but as for all tests other than that of our central hypothesis, P 0.30. Consideration of variables in cross-species correlations similarly revealed no relationships between early growth rate and seed mass, juvenile palatability, or adult palatability (Table 1).

View larger version (16K): [in this window] [in a new window]   Fig. 1. Mean trait values for each species. From top to bottom: (a) Early growth rate. (b) Juvenile palatability index. (c) Adult palatability index. (d) Seed mass. Faster growing species are shown in solid bars, and are Poa annua, Senecio vulgaris, Stellaria media, Trifolium pratense, and Urtica dioica. Slower growing species are shown in striped bars, and are Poa pratensis, Senecio jacobaea, Stellaria graminea, Trifolium dubium and Urtica urens. Species are arranged in the same order in all parts of the figure. The letter A above a bar in part (a) signifies that the species is an annual; the letter P above a bar indicates a perennial species. In part (b), the absence of a bar for Stellaria graminea shows a palatability index of 0, not a lack of data. See Materials and Methods for description of palatability index. All congeneric pairs had significant differences in growth rate. For all but two species, P < 0.0001; for the two Senecio species, P < 0.0066. Because these are not parametric tests of means, there are no error bars on the histograms illustrating our data

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Palatability is not necessarily equivalent to the level of chemical defense in a plant, although when comparing phylogenetically close relatives it is perhaps not a totally unreasonable inference to draw (Berenbaum, 1981 ). With very closely related species, differences in defense chemistry are more likely to represent merely quantitative and not qualitative differences in the secondary compounds involved. Furthermore, quantitative differences in chemical defense investments should produce exactly the pattern found in our study (Herms and Mattson, 1992 ; Stamp, 2003 ).

There are several reasons why Fenner et al. (1999) did not find a relationship between growth rate and palatability, while we have, with the central issue being our very specific hypothesis. From that, we were able to focus our study on particular comparisons (between congeners) and different variables (absolute rather than relative growth rate) than those used in the earlier study. Additionally, we derived all our measures from the same seed pool as that used for the palatability assessments (and seed mass), whereas Fenner et al. (1999) drew their relative growth rate values from the literature.

If we assume that in the congeneric comparisons made here, palatability is a reliable indicator of the level of investment, then we are confronted by a question: why has our simple and straightforward study so easily shown what appears to be evidence of a defense cost–growth rate trade-off when much more elaborate studies have so frequently been equivocal (Bergelson and Purrington, 1995 ; Koricheva, 2002 )? Our target species were not selected for any a priori expectation that they would show this pattern; rather, they were what were available from Fenner et al. (1999) . We offer two possible answers to the question, both of which have implications for the study of cost–benefit relationships in plant–herbivore interactions. First, we suggest that in many cases where a growth–defense trade-off has been difficult to document, the relevant "benefit" may be at the juvenile stage rather than the measures of adult growth, size, or seed set more commonly used as measures of benefit. That juvenile survivorship should play a role in the population and community dynamics of herbivory is not totally surprising: all else being equal, small plants almost invariably suffer more from the same absolute amount of damage—in growth decrement and/or mortality—than large plants (Fenner, 1987 ; Hanley et al., 1995 ). Consistent with the importance of the juvenile stage to the plant, small and young individuals have been found to be better defended than larger and older plants (Kearsley and Whitham, 1989 ; Bowers and Stamp, 1993 ). More important, storage theory, a body of theory that addresses the impact of temporal variation in environmental conditions such as herbivory, has shown predictive success when recruitment from juvenile to adult stages regulates plant persistence and coexistence (Chesson and Warner, 1981 ; Kelly and Bowler, 2002 , 2005 ; Chesson, 2003 ; Kelly et al., 2005 ).

We propose a second reason why costs of defense might have been difficult to establish in within-species studies: where there is a clear cost–benefit relationship between defense from herbivory and competitive advantage, plants can speciate rapidly (from Kelly et al., 2005 ). Thus, within-species studies are more likely to be focused on taxa where costs and benefits of defense are complex and/or may be complicated by gene flow, ecological response, population structure, or some combination of these factors. This logic is supported by the observation that within-species studies have had the most reliable success primarily where all extraneous factors are held constant through the rather radical step of transgenic manipulation of defense levels (Bergelson and Purrington, 1995 ).

In conclusion, regardless of whether the association between juvenile palatability and early growth rate that we have documented is one of cause and effect or not, it has ramifications for species interactions. Differential sensitivity storage dynamics indicates that similar species may coexist when the better competitor is also more vulnerable at recruitment to fluctuations in the environment. Within congeneric pairs, the co-occurring species compared here share the vast majority of their evolutionary histories, dictating fundamental similarity in hardwiring of physiological processes and behavioral options. Slug population sizes vary greatly from year to year (Symondson et al., 2002 ). The faster juvenile growth rate of the congener that is more vulnerable to slug damage means that in low slug years, its seedlings may more quickly dominate a patch of ground than those of the more slowly growing species, with the potential for overtopping and otherwise outcompeting the seedlings of the slower growing species. In high slug years, the faster growing congener is more likely to be attacked by slugs, leaving the less palatable, slower growing species to colonize unchallenged the space left by the removal of the more vulnerable taxon (see Hanley, 1995 ).

	FOOTNOTES

 
¹ The authors thank Michael Fenner for digging out the raw palatability data and Michael Bowler for general discussion.

⁴ Corresponding author (e-mail: colleen.kelly{at}physics.ox.ac.uk )

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Armstrong D. P. M. Westoby 1993 Seedlings from large seeds tolerate defoliation better: a test using phylogenetically independent contrasts. Ecology 74: 1092-1100[CrossRef][ISI]

Berenbaum M. 1981 Patterns of furanocoumarin distribution and insect herbivory in the Umbelliferae: plant chemistry and community structure. Ecology 62: 1254-1266[CrossRef][ISI]

Bergelson J. C. B. Purrington 1995 Surveying patterns in the cost of resistance in plants. American Naturalist 148: 536-558[ISI]

Bowers M. D. N. E. Stamp 1993 Effects of plant age, genotype and herbivory on Plantago performance and chemistry. Ecology 74: 1778-1791[CrossRef][ISI]

Chesson P. 2003 Quantifying and testing coexistence mechanisms arising from recruitment fluctuations. Theoretical Population Biology 64: 345-357[CrossRef][ISI][Medline]

Chesson P. L. R. R. Warner 1981 Environmental variability promotes coexistence in lottery competitive systems. American Naturalist 117: 923-943[CrossRef][ISI]

Fenner M. 1987 Seedlings. In J. P. Grime, R. Hunt, G. A. F. Hendry, and D. H. Lewis [eds.], Frontiers of comparative plant ecology, 35–47. Academic Press, London, UK

Fenner M. M. E. Hanley R. Lawrence 1999 Comparison of seedling and adult palatability in annual and perennial plants. Functional Ecology 13: 546-551[CrossRef][ISI]

Hanley M. E. 1998 Seedling herbivory, community composition and plant life-history traits. Perspectives in Plant Ecology, Evolution and Systematics 1: 191-205[CrossRef]

Hanley M. E. B. B. Lamont 2001 Herbivory, serotiny and seedling defence in Western Australian Proteaceae. Oecologia 126: 409-417[CrossRef][ISI]

Hanley M. E. M. Fenner P. J. Edwards 1995 The effect of seedling age on the likelihood of herbivory by the slug Deroceras reticulatum. Functional Ecology 9: 754-759[CrossRef][ISI]

Harborne J. B. 1993 Introduction to ecological biochemistry, 4th ed. Academic Press, London, UK

Harper J. L. P. H. Lovell K. G. Moore 1970 The shapes and sizes of seeds. Annual Review of Ecology and Systematics 1: 327-356

Harvey P. H. M. D. Pagel 1991 The comparative method in evolutionary biology. Oxford University Press, Oxford, UK

Herms D. A. W. J. Mattson 1992 The dilemma of plants: to grow or defend. The Quarterly Review of Biology 67: 283-335[CrossRef]

Kearsley M. J. C. T. G. Whitham 1989 Developmental changes in resistance to herbivory: implications for individuals and populations. Ecology 70: 422-434[CrossRef][ISI]

Kelly C. K. 1995 Seed size in tropical trees: a comparative study of factors affecting seed size in Peruvian angiosperms. Oecologia 102: 377-388[CrossRef][ISI]

Kelly C. K. 1996 Seed size and habitat use: a reanalysis of Salisbury (1974). New Phytologist 135: 169-174[CrossRef][ISI]

Kelly C. K. 1997 Response to Thompson and Hodkinson. New Phytologist 138: 167

Kelly C. K. A. Purvis 1993 Seed size and establishment conditions in tropical trees: on the use of taxonomic relatedness in determining ecological patterns. Oecologia 94: 356-360[CrossRef][ISI]

Kelly C. K. M. G. Bowler 2002 Coexistence and relative abundance in forest tree species. Nature 417: 437-440[CrossRef][Medline]

Kelly C. K. M. G. Bowler 2003 Communications arising (reply): Competition and coexistence in forest trees. Nature 422: 587

Kelly C. K. M. G. Bowler 2005 A new application of storage dynamics: differential sensitivity, diffuse competition and temporal niches. Ecology 86: 1012-1022[CrossRef][ISI]

Kelly C. K. M. G. Bowler F. M. Breden M. Fenner G. M. Poppy 2005 An analytical model assessing the potential threat to natural habitats from insect resistance transgenes. Proceedings of the Royal Society of London, B, Biological Sciences 272: in press

Koricheva J. 2002 Meta-analysis of sources of variation in fitness costs of plant anitherbivore defenses. Ecology 83: 176-190[ISI]

Price P. W. 1997 Insect ecology. Wiley, New York, New York, USA

Siegel S. N. J. Castellan Jr 1988 Nonparametric statistics for the behavioral sciences, 2nd ed. McGraw-Hill, New York, New York, USA

Sokal R. R. F. James Rohlf 1995 Biometry, 3rd ed. W. H. Freeman, New York, New York, USA

Stamp N. 2003 Out of the quagmire of plant defense hypotheses. Quarterly Review of Biology 78: 23-55[CrossRef][Medline]

Symondson W. O. C. D. M. Glen A. R. Ives C. J. Langdon C. W. Wiltshire 2002 Dynamics of the relationship between a generalist predator and slugs over five years. Ecology 83: 137-147[ISI]

Thompson K. D. Hodkinson 1998 Seed mass, habitat and life history: a reanalysis of Salisbury (1942, 1974). New Phytologist 138: 163-166[CrossRef][ISI]

Westoby M. 2002 Choosing species to study. Trends in Ecology and Evolution 17: 587[CrossRef]

Whelan R. J. 1982 An artificial medium for feeding choice experiments with slugs. Journal of Applied Ecology 19: 89-94[CrossRef][ISI]

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