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OIKOS 81: 99-108. Copenhagen 1998

Top-down vs bottom-up control influenced by productivity in a

North Derbyshire, UK, dale

Lauchlan H. Fraser

Fraser, L. H. 1998. Top-down vs bottom-up control influenced by productivity in a North Derbyshire, UK, dale. - Oikos 81: 99-108.

Fretwell and Oksanen's theory of trophic dynamics was tested in two plant communities located in a North Derbyshire dale, including: (1) a low productivity calcareous grassland; and, (2) a highly productive Urtica dioica (nettle) patch. Two methods (herbivore removal through pesticide application, and transplanting established, intact turves (0.5 M2) between the two community types) were employed, and analysed in a two-way ANOVA, to test the hypothesis that highly productive communities are controlled by 'top-down' forces and low productivity communities are controlled by 'bottom-up' forces. The Fretwell-Oksanen theory proposes that herbivores limit growth in low productivity communities, not highly productive communities. Therefore, removal of herbivores will result in an increase in plant biomass only in the low productivity community. The results presented in this paper support the Fretwell-Oksanen hypothesis. Furthermore, when small turves were transplanted from the highly productive community to the low productivity community the removal of herbivores through pesticide application greatly increased the above-ground plant biomass. This result suggests, firstly, that the vegetation grown in a highly productive environment is generally very palatable, and secondly, it strength- ens the evidence that herbivores are limiting plant growth in low productivity communities but not highly productive communities. Individual plant species response to herbivore removal was related to known relative growth rate values using linear regression and was found to be significant in one case: nettle turves transplanted into the grassland. In this case, relative growth rate accounted for 68.3% of the variation in the response of the plants to herbivore removal. This suggests that fast-growing plants from a highly productive environment are most likely to respond to the release of a limiting factor, in this case herbivory, within a community.

L. H. Fraser, NERC, Unit of Comparative Plant Ecology, Univ. of Sheffield, Sheffield, UK SJO 2TN (present address: Dept of Biology, Univ. of Ottawa, Box 450, Stn A, Ottawa, ON, Canada KIN 6N5 [email protected]]).

There is an increasing volume of theory and evidence suggesting that primary productivity directly influences the trophic interactions of an ecosystem (Fretwell 1977, 1987, Oksanen et al. 1981, Oksanen 1990a, b, Van de Koppel et al. 1996, Moen and Collins 1996, Fraser and Grime 1997). Fretwell and Oksanen have proposed that herbivore communities inhabiting a highly productive habitat are primarily controlled by carnivores ('top-

down' control), whereas herbivore communities in a

low productivity habitat are thought to be primarily

Accepted 14 July 1997

Copyright ? OIKOS 1998 ISSN 0030-1299 Printed in Ireland - all rights reserved

controlled by the supply of available resources ('bottom-up' control) (Fretwell 1977, Oksanen et al. 1981). The rationale for a 'bottom-up' controlled community at a low productivity level is that there are not enough resources in the community to support and sustain the third trophic level (carnivores). Productivity also ap-

pears to determine to a large extent the plant functional types likely to be successful in a plant community (Grime 1974, 1977). Fast-growing plants are associated with high productivity communities, and under labora-

OIKOS 81:1 (1998) 99

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tory conditions are generally more palatable and vul-

nerable to herbivory than slow-growing plants adapted

to low productivity communities (Grime et al. 1968, 1997, Feeny 1976, Rhoades and Cates 1976, Grime

1979, Coley et al. 1985, Southwood et al. 1986). How-

ever, despite the fact that a certain plant species may be

quite palatable, if the herbivore numbers and activity

are severely limited by carnivores, that plant species will

flourish. Therefore, the extent to which herbivores influ-

ence the structure and dynamics of plant communities

only becomes understandable and predictable when trophic interactions are known.

Transplanting of established plants into different

communities and environments is a commonly used test employed by population ecologists to study fine-scale interactions, specifically competition (Silander and An-

tonovics 1982, Turkington 1989). Ecologists have also

used turves containing mixtures of established plants to test the communities' responses to abiotic perturbations (MacGillivray et al. 1995) and herbivory (Moen et al.

1993). The methodology employed in the experiment

described in this paper is unique because it involves

transplanting turves of established plants into very different plant communities (in terms of species composition and site productivity) in order to test the varying roles of herbivory.

The purpose of the experiment was to test Fretwell

and Oksanen's theory of trophic interactions (Fretwell

1977, Oksanen et al. 1981) by employing two interact-

ing methodologies. First, it was intended to study the influence of pesticides on two communities of con-

trasted productivity levels. The second purpose was to measure the impact of herbivores from one community

on the vegetation of the other (and vice versa) by transplanting turves between the two. A complication

which arises when turves are transplanted between

communities is the possibility that herbivory will not depend exclusively upon the activity of the invertebrate

herbivores originating from the 'host' community. To

an unknown extent there may be impacts of inverte-

brate herbivores or carnivores transplanted with the turves. The main vertebrate herbivore (sheep) have been absent from the dale for over 5 years. Other vertebrate herbivores, such as rabbits, mice and voles undoubtedly play important roles in the dale ecosystem, but this experiment was designed to test the importance of invertebrate herbivory and its relation to trophic dynamics.

Methods and materials

Study area

The experiment was conducted in a dale located within the Health and Safety Laboratory property in Der- byshire, near the town of Buxton. This dale is charac-

teristic of the shallow-soiled wet calcareous ancient

pastures found in the dales of the high limestone

plateau (Balme 1953, Lloyd et al. 1971, Lloyd 1972, Pearce 1987). It is the dale used in studies by Burke and

Grime (1996), MacGillivray et al. (1995), and Buckland

(1994) and is the site of current climate change experi-

ments conducted by the Unit of Comparative Plant

Ecology, Sheffield University. The dale has a slope of

approximately 300, and an altitude of 370 m (National

Grid Reference SK 057708). The experiment was located on the north-west facing side of the dale. There is

a high annual rainfall evenly spread throughout the

year and a short growing season between early May

and late September. Virtually no growth occurs during the winter.

Two sites were selected within the dale. One of the

sites was located on continuously moist infertile soil

supporting a relatively species-rich calcareous grassland

community of slow-growing, mainly evergreen species. The second site was situated on an area where mush-

room compost had been dumped ten years previously

(MacGillivray 1993). This site consisted of a relatively high productivity patch of fast-growing perennials

dominated by nettles (Urtica dioica). Table 1 lists the species that were found in both sites and their mean

abundance.

Experimental design

Within each of the two sites selected, 48 0.5-mi2 plots were staked out in April 1994. Half of the plots re-

ceived a pesticide treatment and two-thirds of the plots

were transplanted, either between sites or in situ, for a

2 x 3 factorial combination of six treatments. Each

treatment was replicated eight times. The in situ trans-

planted plots (turves) were simply removed and re-

planted back into their home site, while the other

transplanted plots were transferred into the opposite

plant community (i.e. a reciprocal transplant). Each of

the transplanted plots was excavated to a depth of

approximately 200 mm. The control plots were undisturbed. See Fig. 1 for a map of the study site.

Every 3 weeks, beginning April 1994, 5 g of mol- luscicide (Bio Slug pellets: active ingredient metalde-

hyde), 5 g of systemic below-ground insecticide (Bio Chlorophos: active ingredients chloropyrifos and diazi- non), and 100 ml of a systemic above-ground insecti-

cide (Bio Long-Last: active ingredients dimethoate and permethrin) were applied to half of the 0.5-M2 plots within each site until the final harvest in October 1994. In order to minimize spray drift, the pesticides were

applied between 0400 and 0600 when winds were low. The pesticides were tested independently for possible

stimulatory or phytotoxic effects on five of the domi-

nant plants occurring within the study sites (Fraser

1996). It was found that the pesticides were lightly

100 OIKOS 81:1 (1998)


Table 1. Lists of species in each site and their mean relative abundance in eight 0.2-m2 control plots. Maximum relative growth rate (Rmax) from Grime and Hunt (1975). Canopy height (can ht) and specific leaf area (sla) from FIBS (Functional Interpretation of Botanical Surveys).

Grassland Nettle patch

% abundance Rmax can ht sla % abundance Rmax can ht sla

Festuca ovina 36.5 1.00 2 10.4 Urtica dioica 60.0 2.35 5 21.3 Carexflacca 19.3 1.38 2 15.6 Arrhenatherum elatius 27.3 1.30 5 31.3 Helictotrichon pratense 9.3 0.75 2 9.8 Elytrigia repens 3.2 1.21 3 23.4 Calluna vulgaris 7.2 0.35 4 11.0 Holcus lanatus 2.7 2.01 3 33.8 Potentilla erecta 7.1 0.83 2 22.7 Deschampsiaflexuosa 2.1 0.81 2 16.1 Agrostis capillaris 6.8 1.48 2 28.7 Epilobium montanum 1.3 - 3 28.2 Galium saxatile 4.8 1.16 1 20.5 Rumex obtusifolius 1.1 1.49 2 31.1 Hypericum pulchrum 1.8 - 3 14.9 Poa trivialis 0.9 1.40 1 28.1 Anthoxanthum odoratum 1.7 0.94 2 23.4 Dactylis glomerata 0.6 1.31 3 24.0 Dactylis glomerata 1.3 1.31 3 24.0 Stellaria media 0.4 2.43 2 47.5 Sanguisorba minor 1.1 - 2 11.3 Senecio jacobaea 0.3 1.24 4 25.0 Agrostis vinealis 0.9 1.41 2 18.5 Agrostis stolonifera 0.1 1.48 2 35.5 Senecio jacobaea 0.7 1.24 4 25.0 Viola riviniana 0.4 0.65 2 - Bromopsis erecta 0.3 - 2 19.1 Campanula rotundifolia 0.2 0.81 2 20.2 Helianthemum nummularium 0.2 0.70 2 5.0 Trifolium pratense 0.1 - 2 20.9 Pimpinella saxifraga 0.1 - 1 15.4 Holcus lanatus 0.1 2.01 3 33.8 Lotus corniculatus 0.1 1.05 2 19.7 Lathyrus montanus 0.1 0.49 2 19.7 Koeleria macrantha 0.1 0.94 1 16.2 Leontodon hispidus 0.1 0.89 2 23.9 Scabiosa columbaria 0.1 1.26 1 23.8

phytotoxic (the pesticides caused a reduction in

biomass), but this result was only significant for one

plant species (Urtica dioica).

The final harvest was in early October 1994, before

the first frosts. A 200-mm2 quadrat was placed in the

centre of each plot and all the above-ground parts of

the living plants were harvested within the quadrat. The

plants were then separated into species, oven-dried at

80'C and weighed.

Analysis

A two-way ANOVA was applied to determine the

effect of site (which included the transplanting treat-

ment) and the pesticide treatment on the total above-

ground biomass. Tukey's HSD test was applied to

separate the treatment means. Also, the 95% confidence

limits were calculated for each treatment mean.

The effect of the pesticide treatment was calculated

for each plant species at its site of origin and at the transplanted site and the species ranked according to

their relative abundance. By doing this it was deter-

mined which species benefited by the removal of herbi-

vores and which species suffered. This procedure was

not carried out on the turves which had been excavated

then replaced into their home site because it was deter-

mined through the ANOVA described above (and presented in Tables 2 and 5 and Figs 1 and 5) that transplanting had no effect on plant biomass.

Linear regressions were carried out to examine the

relationship between maximum relative growth rates

(Rmax) available from laboratory screening tests (Grime and Hunt 1975) and the change in above-ground

biomass due to the pesticide treatment. The Rmax was not known for all the species found in this study, so by

necessity the analysis was limited to those species with

available values. The Rmax values used in these analyses are presented in Table 1. This analysis was carried out

on four subsets of the experimental data: nettle turves

in situ; nettle turves transplanted to grassland; grass-

land turves in situ; and grassland turves transplanted to

the nettle patch.

Results

Nettle community

The nettle patch turves transplanted to the grassland

suffered major herbivore attack compared with those

remaining in the nettle patch (Fig. 2). Furthermore, the

nettle turves that were transplanted to the grassland

community responded dramatically to the pesticide

treatment. Visible herbivore damage, including damage by leaf chewers and gall-forming insects, specifically the nettle midge (Dasineura urticae), was apparent on the

plants not treated with pesticides, while the plants which were treated flourished. The mean dry weight of

the total above-ground biomass of the nettle commu-

OIKOS 81:1 (1998) 101


fV0:0XX-;-: X:t ;nettle patch; -grassland

ff 0 0 00;S-aS5|7<flo 00020. fff tf; t0

~~oum ENZN* ~ ~ ~ ~ ~ ~ EULI

LIOW NE ~~~~~~~~~~ 0 WE ~ ~ ~ 00N

OWE ~~~~~~~~ ~~Mz N

;control W 0 X U N control + pesticide

Transplanted in situ

0 transplanted in situ + pesticide

Transplanted btw. sites

* transplanted btw' sites + pesticide

Fig. 1. Layout of experimental design. Squares represent a 0.5-rn area.

nity transplanted to the grassland community was 4.34

g without pesticides, and more than three times that,

14.34 g, with pesticides. In fact, this latter treatment

was associated with the highest recorded mean biomass.

There was no significant difference in the above-ground

biomass between the different treatments within the

nettle patch. The two-way ANOVA confirmed that the

pesticide treatment had a significant effect on the total

above-ground biomass, while the site treatment did not

(Table 2).

The individual species response to the removal of

herbivores was calculated and ranked for both the plots

in situ and the transplanted plots (Fig. 3). There was

very little difference in the way the species responded to

herbivore removal in both sites; the main differences

were in the magnitude of change. Urtica dioica had an increase of 0.85 g in mean above-ground biomass with

the addition of pesticides in the turves remaining in

situ. In the transplanted turves, U. dioica had an in-

crease of 4.57 g and Arrhenatherum elatius responded to a similar extent.

The linear regression model comparing the relation-

ship between maximum relative growth rate (Rmax) and the change in total above-ground biomass mediated by

the pesticide treatment was significant for the nettle

turves transplanted into the grassland, but not for the

nettle turves in situ (Table 3). The relationship between

Rmax and the change in biomass was positive and the model accounted for 68.3% of the variation within the population (Fig. 4).

Grassland community

The application of pesticides to the grassland turves resulted in effects which were quite different from those

observed in the nettle turves. The effects of site and pesticide treatment on the total above-ground biomass were statistically significant (Table 4), but this did not apply to the combined effect of site and pesticides. There was an approximate 50% increase in mean dry weight of the grassland turves in situ (regardless of transplant treatment) when pesticides were applied (Fig. 5). Although this difference was not found to be significant using Tukey's HSD, it was certainly substantial. However, since it was not significant sampling error cannot be ruled out. The grassland turves trans-

planted into the nettle community had very low biomasses, irrespective of pesticide application, compared to the grassland plots in situ.

The individual species response to the removal of

herbivores in the grassland community also differed from the response of species in the nettle community. The biomass of most species in the grassland plots remaining in situ was greater with the application of the

102 OIKOS 81:1 (1998)


Table 2. Results of two-way ANOVA examining the effects of site (SITE) and the pesticide treatment (PEST) on the mean above-ground biomass of the nettle turves. This table presents the sum of squares (SS), degrees of freedom (d.f.), mean squares (MS), F-ratios, and p-values (p).

Source of variation SS d.f. MS F-ratio p

SITE 23.288 2 11.644 0.840 0.439 PEST 123.649 1 123.649 8.920 0.005 SITE x PEST 277.298 2 138.649 10.003 0.000 ERROR 582.173 42 13.861

pesticides (Fig. 6a), particularly Festuca ovina. How-

ever, the species response in the transplanted plots to

the application of pesticides was almost completely

opposite to the response of species in the grassland

plots in situ (Fig. 6b). Instead of being the species most

benefiting from the removal of herbivores (Fig. 6a), F.

ovina suffered the greatest decrease. Other species which

showed a similar pattern were Carex flacca and An-

thoxanthum odoratum. Some of the species that seemed

to benefit from the application of pesticides in the

transplanted grassland turves were species native to the

nettle community (e.g. Urtica dioica, Poa trivialis, and

Arrhenatherum elatius), and were not present in the

grassland turves in situ.

The linear regression models between R max and the

change in total above-ground biomass caused by the

pesticide treatment were not significant (Table 5), even

though the slope tended towards a positive relationship

(Fig. 7).

Discussion

On the basis of the responses to pesticide treatment

Urtica dioica did not appear to suffer much loss through herbivory within the nettle community and yet

25-

20- VA

C 15 J

5-. T e S

0-

C CT T

Fig. 2. Effect of transplanting and pesticide treatment on the mean total shoot biomass (g) of the nettle turves. In this diagram P = pesticide treatment (+ present, - absent); C= control turves; CT = transplanted turves in situ; T = transplanted turves. Error bars represent 95% confidence limits.

it is a fast-growing herb that has highly nutritious,

nitrogen-rich foliage (Davis 1975, 1991). When U.

dioica was transplanted into the low-nutrient grassland

community though, it was subject to herbivory. In

contrast to the nettle community, the application of

pesticides to the grassland community resulted in a

substantial increase in mean dry weight of total above-

ground vegetation. In other words, invertebrate herbi-

vores seemed to be limiting the biomass of the vegetation. When the grassland turves were trans-

planted into the nettle community there was no increase

in mean dry weight with the addition of pesticides. The

effect of transplanting (disturbance of the turves) can

be discounted as a factor in this investigation because

a) Urtica dioica turves in situ 1 o.2

0.8 -

0.6-

.~0.4 B 0~~~~~~~~~~~~~~~~0

0.2 - 0 0 '

-1 al i) L

0.0 - 1U EI

00 -.2 0 ad E

0 U

b) Urtica dioica turves in grassland

4 -

0~~~~~~~~~~~~

3) 2

2 - ~ ~ ~ ~ 0 ~ -

A .5 E ci

*- C S- o ' o a: ii

Fig. 3. Ranked mean abundance measured as the change in dry shoot biomass (g) mediated by the application of pesticides for each species occurring in turves (a) in situ, and (b) in the grassland site. See Table 1 for a key to species.

OIKOS 81:1 (1998) 103


Table 3. Results of linear regression examining the relationship between the maximum relative growth rate (Rmax) and the change in the above-ground biomass of the nettle turves due to the pesticide treatment. This table presents the sum of squares (SS), degrees of freedom (d.f.), mean squares (MS), F-ratios, and p-values (p).

Source of Dependent variable variation

Nettle turves at home Nettle turves in grassland

SS d.f. MS F-ratio p SS d.f. MS F-ratio p

Rmax 0.08 1 0.08 0.75 0.406 10.02 1 10.02 7.52 0.025 residual 1.01 10 0.10 10.66 8 1.33

the results show that there were no significant differ-

ences between the control turves and the turves trans-

planted back into their site of origin (Figs 2 and 5). The results from this study support Fretwell and

Oksanen's top-down hypothesis of community control

(Fretwell 1977, 1987, Oksanen et al. 1981, Oksanen 1990a, b). This is despite the fact that the Fretwell-

Oksanen model explicitly excludes ectotherms (Oksanen

et al. 1981, 1987, Oksanen 1990a). The nettle community was a highly productive community. According to

a) nettle turves in situ 1.0

RO0.264 0 0.8 _

0.6 - 0

0.4 -

0.2-

0.0- 0 0 03

-0.2 0 0

0.5 1.0 1.5 2.0 2.5

Rmax

b) nettle turves in grassland 5.0 -

R-0.696 4.0 -

3.0 - 0

J 2.0-

1.0- 0~~~

0.0 0 0

-1.0 I I 0.5 1.0 1.6 2.0 2.5

Rmax

Fig. 4. The relationship between the change in the mean total shoot biomass (g) due to the pesticide treatment and the maximum relative growth rate (Rmax) for species present in the nettle turves (a) in situ, and (b) in the grassland site.

the Fretwell-Oksanen theory, a community that is highly productive can support at least three trophic levels. A highly productive community with three trophic levels will be controlled by predators, i.e. it is 'top-down' controlled. This means that herbivores

should have little influence on the vegetation because their numbers are limited. In the case of the nettle

community herbivores did not have any significant influence on the mean dry weight of the total above- ground biomass. That does not mean invertebrate herbivores were entirely absent; pitfall traps confirmed that

they were indeed present (Fraser 1996). In fact, herbivores still seemed to exert some influence on the alloca- tion of growth of Urtica dioica. When herbivores were removed, a higher proportion of U. dioica flowered (Fraser 1996). But, overall, herbivores appeared to have a negligible influence on the biomass of the nettle community. Of course, the primary predators within the nettle patch may well be endotherms (e.g. passerine birds) but the results of this study show that the Fretwell-Oksanen model can certainly be extended to include ectotherms (see also Fraser and Grime 1997). The grassland community was at low productivity and apparently could not support or sustain a large or effective third trophic level. The evidence for this is that when herbivores were removed, the mean dry weight of the total above-ground biomass increased substantially indicating that herbivores were limiting plant growth. If herbivores were limiting plant growth, they in turn must not have been limited greatly by carnivores. There could be three factors that contribute to limiting the abundance, and therefore control, of carnivores in the grassland community. The first factor has already been stated, which is that there were not enough resources to sustain an effective third trophic level. The second factor may be that the patches of high quality food (nettle) were readily detected by herbivores (see Davis 1975), but the resulting patches of high herbivore density were so small (in the spatial scale relevant for carnivores) that they were missed by carnivores. Fi- nally, the third possibility may be that there were many refuges within the grassland community that protected herbivores from predators. The architecture of the grassland community was certainly complex and multi- layered, more so than the nettle community, and it has

104 OIKOS 81:1 (1998)


Table 4. Results of two-way ANOVA examining the effects of site (SITE) and the pesticide treatment (PEST) on the mean above-ground biomass of the grassland turves. This table presents the sum of squares (SS), degrees of freedom (d.f.), mean squares (MS), F-ratios, and p-values (p).

Source of variation SS d.f. MS F-ratio p

SITE 494.36 2 247.18 9.237 0.000 PEST 140.77 1 140.77 5.261 0.027 SITE x PEST 90.00 2 45.00 1.682 0.198 ERROR 1123.868 42 26.76

been shown in predator-prey experiments that refuges

for herbivores can be critical for their survival (Huf-

faker 1958, Kareiva 1990, Hixon and Beets 1993).

Another factor to account for is that the complex

architecture of the grassland may simply afford a more

suitable environment, regardless of predators, for the

major invertebrate herbivores (e.g. molluscs) (see Van

de Koppel et al. 1996 for a comparative case).

When turves of the nettle community were transplanted into the grassland community, top-down con-

trol of herbivores was effectively removed. It was

assumed that these transplanted turves were too small

for viable animal populations from the nettle commu-

nity to persist and establish in the grassland. The effect

of transplanting the nettle turves to the opposing site

was to increase the influence of herbivores from the

grassland community on the transplants, and the effect

was dramatic. Firstly, it proved that Urtica dioica was

very palatable, certainly more palatable than the low

nutrient grassland species, otherwise the loss of biomass

of the nettle community would have been similar to the

losses experienced by the grassland community. It also

confirmed that herbivores were not very effective in the

nettle community because U. dioica experienced little

loss of biomass there.

25-

20 -V

C i5

0 _

C CT T

Fig. 5. Effect of transplanting and pesticide treatment on the mean total shoot biomass (g) of the grassland turves. In this diagram P = pesticide treatment (+ present, - absent); C = control turves; CT = transplanted turves in situ; T = transplanted turves. Error bars represent 95% confidence limits.

Turves from the grassland community transplanted

into the nettle community did not respond as expected.

According to the principles already outlined, the trans-

plants should have been released from herbivore pres-

sure because of top-down control of herbivores. Yet,

there was no increase in mean dry weight of total

above-ground vegetation. On the contrary, there was a decrease, even when pesticides were applied. In retro-

spect, this can be explained by competitive suppression

of the transplants through shading and (less likely)

mineral nutrient capture from the fast-growing com-

petitors surrounding the turves. In fact, some of the

small turves were actually invaded by competitors, such

as U. dioica and Poa trivialis, from the surrounding

nettle community. This result actually corresponds to

the predictions of the Fretwell-Oksanen model (Ok-

sanen et al. 1981, Oksanen 1990a). Perhaps, though, if

larger turves had been used, and shading minimized by

cutting surrounding vegetation, an increase in mean dry

weight would have occurred. However, an interesting

outcome was revealed as a result of the competitive

pressure on the transplants. If there was no competition

on the transplants from the surrounding vegetation in

the nettle community, we would have expected both the

transplants with and without pesticides to behave simi- larly to the undisturbed plots in the grassland commu-

nity that had been applied with pesticides. However, there was a difference in the performance

of species between the transplants applied with pesticides to those without pesticides. Even though herbivores were controlled in the nettle community, there

were herbivores present. It seems that those few herbi-

vores were benefiting slow-growing, relatively unpalat- able plants, e.g. Festuca ovina, Carex flacca and Anthoxanthum odoratum. When herbivores were re-

moved through the application of pesticides, the fast-

growing competitors, U. dioica, P. trivialis, and Arrhenatherum elatius benefited. A similar result with

the same plant species was also found in an outdoor microcosm study (Fraser and Grime 1998). As well,

Ostfeld and Canham (1993) showed that fast-growing

tree seedlings were released from intense herbivory from voles following vole removal in an old field.

The relationship between the maximum relative

growth rate (Rmax) and the change in total biomass due to the pesticide treatment was observed fairly consis-

OIKOS 81:1 (1998) 105


a) grassland turves In situ

2-

'CI

O~~~~$ -o.J ls -I

0-1

b) Grassland turves in nettle patch

0.2~~~~~~~~~~~~~~~~~~~0

4.8-

-0.

Fig. 6. Ranked mean abundance measured as the change in dry shoot biomass (g) mediated by the application of pesticides for each species occurring in the grassland turves (a) in situ, and (b) in the grassland site. See Table 1 for key to species.

tently within each of the four different subsets of data

to which the analysis was applied, i.e. nettle turves in

situ; nettle turves transplanted into grassland; grass-

land turves in situ; grassland turves transplanted into

the nettle patch. In each case, the slope of the regres-

sion was positive, meaning that those species with a

higher Rmax had a greater biomass when pesticides

were applied. In other words, they responded more quickly than slower growing species to a release of herbivore pressure. However, this relationship was only

significant for the model applied to nettle turves trans-

planted into the grassland site. This is understandable

assuming that the herbivore pressure within the grass-

land was much higher than within the nettle patch.

Plants with a high Rmax are more palatable than those

with lower Rmax's, therefore the herbivores within the grassland would prefer those species with a higher

Rmax. In addition, the nettle turves that were transplanted into the grassland would have received much

more light than if they remained within their home site

because the grassland species were much shorter.

Plants with a higher Rmax should be able to capitalize on this added resource more rapidly than other plants.

Why was not R max a reliable indicator of species

response to the release of herbivore pressure in the low

productivity turf environment? Perhaps the answer is

that stress-tolerant plants with low relative maximum

growth rates were the dominant species. Unless com-

petitor-type species with high Rmax'S were well established in the community, the plant biomass of the community would be less likely to quickly respond to

the pesticide treatment. A similar response occurs when

fertilizers are applied to an established community of

slow-growing plants. Rather than an increase in

growth rate, slow-growing stress-tolerators accumulate

the extra nutrients in their tissue (Chapin 1980). Com-

petitor species with high Rmax's were dominant in the nettle turves transplanted into the grassland, and there-

fore were able to respond quickly to the pesticide

treatment.

106 OIKOS 81:1 (1998)


Table 5. Results of linear regression examining the relationship between the maximum relative growth rate (Rmax) and the change in the above-ground biomass of the grassland turves due to the pesticide treatment. This table presents the sum of squares (SS), degrees of freedom (d.f.), mean squares (MS), F-ratios, and p-values (p).

Source of Dependent variable variation

Grassland turves at home Grassland turves in nettle patch

SS d.f. MS F-ratio p SS d.f. MS F-ratio p

Rmax 0.26 1 0.26 0.68 0.419 0.09 1 0.09 1.34 0.266 residual 6.89 18 0.38 1.06 15 0.07

grassland turves in situ

2.5 - 0

2.0 - RO0.191

1.6 -

1.0-

0 0 0.6 -

0

0.0- 00 0 0 0 -0.5

0

0 0.6 1.0 1.6 2.0 2.6

Rmax

grassland turves in nettle patch 1.0 -

R-0.286

0.5 - 0

Cm 0.0_ 0e 0

0

-0.6 -

-1.0- I l 0 0.6 1.0 1.6 2.0 2.6

Rmax

Fig. 7. The relationship between the change in the mean total shoot biomass (g) due to the pesticide treatment and the maximum relative growth rate (Rmax) for the grassland turves (a) in situ, and (b) in the grassland site.

Acknowledgements - I wish to thank J.P. Grime for his encouragement, support, and advice throughout this study. I am grateful to L. Oksanen, S. E. Hartley, and J. H. C. Cornelissen for insightful, useful comments, to J. G. Hodgson, K. Thompson and V. K. Brown for species identification, and to J. A. Wells for her tireless help in the field. This work was supported by a post-graduate Univ. of Sheffield fellowship and the NERC Unit of Comparative Plant Ecology.

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