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Brief Communication |
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.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: differential sensitivity storage dynamics • growth–defense trade-off • herbivory • juvenile palatability • slugs • species coexistence
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; 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.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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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 10th 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.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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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).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; but see Kelly and Purvis, 1993
; Kelly, 1995
, 1996
).
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
).
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FOOTNOTES |
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4 Corresponding author (e-mail: colleen.kelly{at}physics.ox.ac.uk
)
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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