THE PHYTOPHAGOUS FAUNA OF GORSE
(ULEX EUROPAEUS L.) AND HOST PLANT QUALITY
RICHARD LAWRENCE HILL, M.Sc.
A thesis submitted for the degree of Doctor
of Philosophy of the University of London
and for the Diploma of Imperial College
HOUSED IN SILWOOD PARK LIBRARY
Department of Pure & Applied Biology
Imperial College
Silwood Park
Ascot
Berkshire August 1982 2.
ABSTRACT
This study of the interactions between the fauna attacking gorse (Ulex europaeus L.) and their host-plant, was undertaken as part of a project aimed at the biological control of Ulex in New Zealand. In particular, the effects of seasonal changes in host-plant primary and secondary chemistry, plant structure and foliage morphology on the seasonal perform- ance of the phytophagous insect fauna were examined.
Seasonal patterns of flowering and fruiting were described. Seasonal changes in foliage water content and toughness were summarised, and patterns of growth were described. These were discussed in relation to
Lawton's (1978) living space concept and other current literature.
Seasonal variation in the concentrations of 6 types of secondary compounds in the foliage were described. High concentrations of alkaloids may protect vegetative buds from herbivore attack in early spring, but otherwise foliage appeared to be unprotected.
Energy content and soluble carbohydrate content of gorse foliage remained relatively high throughout the growing season. Foliage nitrogen content was high at bud-burst but declined within 6 weeks to a constant low level.
The insect fauna associated with Ulex europaeus in Britain was described, compared and contrasted with the equivalent continental fauna and the faunas of related host-plants. Most species were rare, though the total number of phytophagous species was not low. Seasonal variation in abundance of the 7 commonest folivorous species was described in detail.
All appeared within 3 weeks of bud-burst, no additional species appeared after the end of June, and almost all were fully developed and rare by the end of July. 3.
Comparisons between the patterns of insect occurrence on gorse and seasonal variation of the plant parameters measured show that peak phyto- phagous insect feeding activity was associated with peak nutrient levels, and possibly minimum foliage alkaloid concentration. The impact of each of the measured factors on the phytophagous insect fauna was discussed in relation to current theory, and in particular the concept of "optimal defense theory". It was concluded that Ulex europaeus may be an example of a plant which has developed low nutritional quality as a defence % mechanism against herbivores.
These findings were tested by two experiments. Host-plant character- istics were altered by the use of nitrogenous fertilisers in the field, and the impact of this on the phytophagous fauna was discussed. Neither
the biology of the host-plant or the fauna were changed to a large extent by the fertiliser regimes used.
Feeding experiments using LV larvae of Agonopterzx ulicetella showed that the nutritional quality of gorse foliage declined through summer.
The relevance of such studies to the procedures used in the biological control of weeds is discussed. 4.
TABLE OF CONTENTS
Page
ABSTRACT 2
LIST OF TABLES 8
LIST OF FIGURES 10
LIST OF APPENDICES 13
SECTION 1: INTRODUCTION 14
SECTION 2: SEASONAL CHANGES IN THE FORM AND STRUCTURE OF GORSE
PLANTS 20
2.1 Introduction 20
2.2 Description of .Field Sites 21
2.3 Materials and Methods 22
2.3.1 Analysis of plant structure 22
2.3.2 Foliage water content 22
2.3.3 Foliage toughness 23
2.4 Results 23
2.4.1 Patterns of flowering and fruiting 23
2.4.2 Seasonal patterns of growth in mature Ulex spp ... 25
2.4.3 Seasonal changes in foliage water content 31
2.4.4 Seasonal variation of Ulex europaeus foliage
toughness ...... 34
2.5 Discussion 34
2.6 Summary ... 42
SECTION 3: THE PRIMARY AND SECONDARY CHEMISTRY OF GORSE FOLIAGE ... 44
3.1 Introduction ... 44
3.2 Sampling and Storage Methods 47
3.3 Analytical Methods 48
3.3.1 Analysis of nitrogen content 48 5.
Page
3.3.2 Analysis of foliage calorific content 50
3.3.3 Analysis of soluble carbohydrate content 50
3.3.4 Analysis of alkaloids 51
3.3.5 Analysis of isoflavones 53
3.3.6 Analysis of silica content 54
3.3.7 Amino acid analysis 55
3.3.8 Analysis of foliar cyanogenesis 55
3.3.9 Analysis of foliar enzyme inhibitors ...... 55
3.4 Results ... 57
3.4.1 Nitrogen content - ... 57
3.4.2 Foliage calorific content ...... 63
3.4.3 Soluble carbohydrate content ...... 63
3.4.4 Alkaloid content 63
3.4.5 Isoflavone content 70
3.4.6 Silica content 73
3.4.7 Unusual amino acids 73
3.4.8 Foliage cyanogenesis 75
3.4.9 Foliar enzyme inhibitor content ... 75
3.5 Discussion 77
3.6 Summary 81
SECTION 4: THE PHYTOPHAGOUS INSECT FAUNA OF GORSE 84
4.1 Introduction 84
4.2 Sampling Methods ... 88
4.3 The Fauna of Gorse Roots 91
4.4 The Fauna of Reproductive Structures 97
4.5 The Fauna Attacking Gorse Foliage 105
4.6 Discussion ... 116 6.
Page
4.6.1 Differences in fauna of U. europaeus and U. minor . 116
4.6.2 Fauna 1 differences between YC and WGP 119
4.6.3 Seasonal patterns in the gorse fauna ...... 121
4.6.4 Feeding generalism and specialism of the gorse
fauna ...... 125
4.6.5 Richness of the gorse fauna 127
4.7 Summary ...... 130
SECTION 5: THE EFFECTS OF HOST-PLANT QUALITY ON THE INSECT FAUNA
OR GORSE 131
5.1 Introduction ... 131
5.2 Methods 136
5.3 The Effect of Predators 137
5.4 Patterns of Foliage Use by Insects 140
5.5 The Effects of Plant-Borne Factors 143
5.5.1 Plant structure and living space 143
5.5.2 Plant chemistry 149
5.6 The Relative Importance of Plant-Borne Factors 153
5.7 Discussion ... 156
5.8 Summary ... 159
SECTION 6: THE EFFECTS OF FERTILISER ON GORSE AND ITS FAUNA ... 161
6.1 Introduction ... 161
6.2 Methods ...... 162
6.3 Results 164
6.3.1 Effects on seasonal variation in N content 164
6.3.2 Effects on the growth of new shoots 167
6.3.3 Effect of fertilisation on the insect fauna ... 170
6.4 Discussion ... 180 7.
Page
6.5 Summary ...... 188
SECTION 7: THE FEEDING CHARACTERISTICS OF ONE GORSE SPECIES,
AGONOPTERIX ULICETELLA 190
7.1 Introduction 190
7.2 Methods 193
7.3 Results 196
7.3.1 Experimental monitoring 196
7.3.2 Phytophage quality 198
7.3.3 Daily larval performance 201
7.3.4 Stadial feeding efficiencies 204
7.4 Discussion ...... ••• 206
7.5 Summary 209
SECTION 8: CONCLUSIONS ... 211
2X6 ACKNOWLEDGEMENTS
REFERENCES 217
APPENDICES 230 8.
LIST OF TABLES
Page
3.1 : Seasonal variation of gorse foliage alkaloid composition as
shown by TLC 69
3.2 : Isoflavone content of Ulex europaeus and U. minor 72
3.3 : % silica content of new, dry, Ulex europaeus foliage 74
4.1 : Sources of information concerning the insect fauna of gorse
in Britain ...... 85
4.2 : Feeding sices of arthropod species attacking gorse in Europe . 92
4.3 : Differences in the abundance of insects on Ulex europaeus. and
U. minor 98
4.4 : Differences in the abundance of insects on Ulex europaeus at
Yateley Common and Windsor Great Park 99
4.5 : Infestation of reproductive structures of Ulex europaeus in
spring and summer ...... 101
4.6 : The relative importance of phytophagous insects collected
from Ulex europaeus foliage at YC and WGP in two years ... 108
4.7 : Detritivorous and predaceous insect species encountered in
gorse foliage ...... 117
4.8 : Life histories of fauna associated with reproductives of Ulex
europaeus and Ulex minor 120
4.9 : Seasonal patterns in gorse insects 122
4.10 : Feeding specialism and generalism in gorse insects 126
4.11 : Species richness of phytophagous insects on 5 host-plant ;
species (Tribe: Genisteae) estimated from some standard
references ...... 129
5.1 : Correlation of faunal variables with 8 plant borne factors ... 147
5.2 : Autocorrelations between independent variables used in 9.
Page
regression analysis ...... 152
5.3 : Assessment of the contribution of 8 independent variables to
a multiple regression model 154
6.1 : A statistical comparison of the soluble and total nitrogen
contents found in fertilised and unfertilised gorse foliage . 165
6.2 : Statistical comparison of gorse foliage total nitrogen content
in fertilised and unfertilised plants 168
6.3 : Statistical comparison of median shoot growth (cm) on
fertilised and unfertilised gorse 171
6.4 : Statistical comparison of differences in abundance between
insect species on fertilised and unfertilised Ulex europaeus . 174
6.5 : Comparison of fertilisation effects on Holous Iccncctus and
Ulex europaeus 185
7.1 : Incubation, storage, and rearing details for each treatment . 194
7.2 : Comparison of components in each treatment ... 197
7.3 : Measurements of parameters reflecting insect quality in each
treatment ...... 199
7.4 : Daily comparison of larval performance during LV in treat-
ments 2-4 ...... 202
7.5 : Measurement of ecological efficiencies for fifth instar in
treatments 2-4 ... 205 10.
LIST OF FIGURES
Page
2.1 : (a) Apparatus for measuring foliage toughness and
(b) Foliage nomenclature ...... 24
2.2 : Patterns of flowering and fruiting in U. europaeus and U. minor 26
2.3 : Patterns of foliage growth in Ulex europaeus and Ulex minor . 29
2.4 : The relationship between shoot length and foliage biomass ... 30
2.5 : Seasonal variation of mean foliage water content in Ulex
europaeus and Ulex minor 32
2.6 : Within shoot seasonal variation of foliage water content ... 33
2.7 : Seasonal variation of foliage toughness Ulex europaeus ... 35
2.8 : Dry weight of new growth as a percentage of total green
biomass ...... 38
3.1 : Seasonal variation of total foliage nitrogen content of Ulex
europaeus at Yateley Common ... 58
3.2 : Seasonal variation of total foliage nitrogen content of Ulex
europaeus at Windsor Great Park 59
3.3 : Seasonal variation of soluble foliage nitrogen content of
Ulex europaeus foliage 60
3.4 : Seasonal variation of U. minor foliage nitrogen content ... 62
3.5 : Seasonal variation of foliage calorific value ... 64
3.6 : Seasonal variation of foliage soluble carbohydrate content ... 65
3.7 : Seasonal variation of alkaloid concentration in foliage ... 67
3.8 : Seasonal variation of total isoflavone content 71
3.9 : Enzyme inhibition activity in gorse foliage 76
4.1 : Seasonal variation in the abundance of Polydrusus confluens
adults on U. europaeus and U. minor 95
4.2 : Seasonal variation in the abundance of Sitona regensteinensis 11.
Page
adults on Ulex europaeus 96
4.3 : Seasonal variation in the abundance of Sitona tibialis adults
on Ulex europaeus and Ulex minor 96
4.4 : Seasonal variation in abundance of Agonopterix ulioetella and
Anarsia spartiella in samples beaten from gorse 104
4.5 : Infestation of Ulex europaeus pods 106
4.6 : Seasonal variation in the abundance of Agonopterix ulicetella
beaten from gorse 110
4.7 : Seasonal occurrence of Aphis uliois and Piezodorus lituratus . Ill
4.8 : Seasonal variation in the abundance of Asciodema obsoletum ... 113 i>
4.9 : Seasonal variation in the abundance of Paohylops bicolor ... 114
4.10 : Seasonal variation in the abundance of Dictyonota strichno-
••• « • • ••• ••» ••• ••• ••• ••• • • • ••• 113
4.11 : Patterns of occurrence of gorse insects in relation to host-
plant development ...... 124
5.1 : Applicability of the spider biomass index 138
5.2 : The number of folivorous insect species collected on gorse
through the season ...... 141
5.3 : The total abundance of folivorous insect species collected on
Ulex europaeus at Yateley Common 142
5.4 : The diversity of folivorous insect species through the season
on Ulex europaeus at Yateley Common 144
5.5 : Summary of seasonal trends in folivorous insects and some
plant factors affecting those insects 146
6.1 : Seasonal variation of foliage soluble and total nitrogen
content in fertilised and unfertilised gorse . 166
6.2 : Seasonal variation of foliage total nitrogen content in 12.
Page
fertilised and unfertilised gorse ... 169
6.3 : Growth patterns of fertilised and unfertilised gorse 172
6.4 : Abundance of A. obsoletum in fertilised and unfertilised
^ors6 • • • ••• ••• ••• ••• ••• • • • ••• ••• 175
6.5 : Abundance of Paohylops bicotor in fertilised and unfertilised
gorse 176
6.6 : Abundance of Dictyonota strichnooera on fertilised and
unfertilised gorse 177
6.7 : Abundance of Sericothrips staphylinus on fertilised and
unfertilised gorse 179
6.8 : Seasonal changes in the community structure of all phyto-
phagous insects living on fertilised and unfertilised gorse 181
6.9 : Seasonal changes in the community structure of phytophagous
insects reproducing on fertilised and unfertilised gorse ... 182
6.10 : The number of phytophagous insects per sample from fertilised
and unfertilised gorse ...... 183
7.1 : Growth of LAgonopterix ulicetella larvae - treatments 1-4 . 200
7.2 : Daily larval performance of LV Agonopterix ulicetella ... 203 13.
LIST OF APPENDICES
Page
I : Phenology of Ulex europaeus 230
II : Changes in the proportions of U. europaeus reproductive
structures in different classes 231
III : Water content of Ulex europaeus 232
IV : Nitrogen content of gorse foliage ... 237
V : Ulex europaeus foliage toughness £42
VI : Mean length of new shoots 243
VII : Enzyme - inhibition reaction times 245
VIII : Summarised insect data ... 247
IX : Variables used in regression analysis 267 SECTION 1
INTRODUCTION
A catalogue of the history and potential of biological weed control
has recently been published which records the rising popularity of this
technique in the control of problem weeds. It records attempts at
biological weed control, and the rapid advance of the discipline from
early exercises in natural history to the detailed examinations of insect-
weed relationships which have become more common today (Julien, 1982).
The biological control literature listed in the catalogue often
contains detailed assessments of the impact of phytophagous insects on
their hosts after introduction to a new environment, and cases of substantial
control are very often well-documented. It is much more rare to find
detailed information regarding the relationship between potential bio-
logical control insects and their host-plants in their place of origin,
despite the fact that ideally, choice of suitable control agents should be
firmly based on such studies. For reasons of finance and opportunity,
preliminary studies are more commonly restricted to the determination of
host-plant range, and description of the developmental characteristics of
candidate insects.
Recently, the Entomology Division of the New Zealand Department of
Scientific and Industrial Research recommenced studies aimed at the
biological control of common gorse, Ulex europaeus L. (Leguminosae:
Genisteae). As part of that long-term aim this 3 year investigation of
the insect fauna of gorse and the complex relationship between the host- plant and its insect fauna in Britain was carried out. The aim of the
study was not only to identify potential control agents, but to examine
facets of host-plant biology which could influence the performance of 15.
potential control agents after release in New Zealand.
The genus Ulex comprises 8 species, all of "Atlantic" (Western
European) or North African distribution (Tutin et al., 1967; Zwolfer,
1962). Its centre of distribution appears to be Northern Portugal but only
3 species occur in Northern Europe. Ulex europaeus is found as far north as Belgium, on the Atlantic seaboard of the continent, but is found throughout Britain. Two other species of gorse are native to the British
Isles. Dwarf gorse, Ulex minor Roth. (= U. nanus Forst.) is much smaller % than U. europaeus and often grows with it. Ulex gallii Planch, or Western gorse, is taller than U. minor but is only common in Western Britain and
Ireland. All gorse species in Britain are calcifugous, and characteristic- ally grow in acid heathlands or other acid infertilie habitats. Inform- ation regarding the identification, distribution and general biology of all three gorse species in Britain can be obtained from Chater (1931), Zwolfer
(1962), Proctor (1965), Hamilton (1980), and Tutin et al. (1967). In this study comparisons are drawn between Ulex europaeus and Ulex minor, and between their respective faunas, but the ecology of Ulex gallii is not formally considered.
Hamilton (1980) also provides interesting information regarding the folklore attached to gorse, and an account of the past economic value of gorse as a crop and as fuel.
Gorse continues to be of economic importance, but for a very different reason. Ulex europaeus was introduced to many countries as a hedge plant in the early 19th century, and is now a very serious weed in New Zealand
(e.g. Bascand, 1973), Australia (e.g. Wilson, 1968), Hawaii (Motooka et al., 1969), mainland U.S.A. (Warren & Youngberg, 1968), Chile, and North- west Spain. It is highly invasive in rangeland and also hinders afforestation with exotic timber species such as Pinus radiata (D. Don) (Chavasse & 16.
Fitzpatrick, 1973). Since it is a weed more commonly associated with extensive agriculture and forestry, there are severe economic restraints on the control methods which can be employed to control it. Current practices include cultural management, herbicide application, or a combination of the two. Two recent bibliographies (Agricultural Research
Council, 1975; Gaynor & MacCarter, 1981), have summarised and indexed the
literature on control methods available prior to 1976.
There have been three biological control programmes aimed at establishing phytophagous insects which attack Ulex europaeus. The first led to the establishment of the seed weevil Apion ulicis Forst., firstly in New Zealand and then throughout the world (Chater, 1931; Davies, 1928;
Miller, 1970). The third led to the introduction, (but not the establish- ment) of Apion scutellave Klug., Agonoptevix ulicetella (Stnt.) and Scythris gall-ioella d. Joannis into Hawaii (Davis, 1959; Davis & Kraus, 1962a, b), while the second was a survey of potential control agents in Europe, and forms the basis for the present study (Zwolfer, 1962, 1963, 1965; Schroder
& Zwolfer, 1970; Girling, 1977).
The bibliography compiled by Gaynor & MacCarter (1981) demonstrates
the heavy bias towards chemical and cultural control measures which is found in the literature. Those few papers which cover other aspects of gorse ecology deal largely with seed and seedling ecology, interactions of gorse with soils, and other ecosystem processes such as nutrient cycling in gorse stands. Very little information is available concerning the ecology of mature gorse plants, their chemical composition, or the biology of the associated fauna. Where relevant information is available it is discussed in the appropriate part of the text.
The aims of this study have therefore been:
(1) To describe the autecology of mature gorse, and in particular, the seasonal changes which occur in gorse foliage, both physically and
chemically.
(2) To describe the phytophagous insect fauna associated with gorse in
Southern Britain, both to identify potential control agents and to
find out more about the life histories of the insects involved.
(3) To examine the interactions between gorse and its phytophagous insect
fauna, particularly the influence of the plant on the timing and
performance of folivorous insect species.
Section 2 describes the seasonal variation of foliage growth and maturation, and the pattern of flowering and fruiting in U. europaeus and
U. minor. Section 3 follows the changes in foliage chemistry which occur during spring and summer. In Section 4, the phytophagous insect fauna is listed, and seasonal variation in the abundance and timing of major or
"key" species is discussed in detail, and similarities between the seasonal patterns shown by phytophagous insects, and those of host-plant character- istics are indicated. Section 5 expands consideration of these inter- actions between gorse and its phytophagous fauna, especially in relation to recent theories about how plants influence the abundance and seasonality of insects. The effects of a number of plant-borne characteristics have now been demonstrated, and in Section 5 the following factors moulding the phytophagous insect fauna of gorse are discussed:
(1) Morphological and mechanical defenses against insects (e.g. Scriber &
Slansky, 1981).
(2) "Living space" offered by host-plants (Lawton, 1978).
(3) Foliage secondary chemistry (e.g. Lawton, 1976; Feeny, 1975; Rosenthal 18.
& Janzen, 1979).
(4) Nutritional quality of foliage (e.g. McNeill & Southwood, 1978; Lawton
& McNeill, 1979).
In addition, the role of predation in the gorse fauna is briefly considered
(Lawton & Strong, 1981). Discussion of the numerous theories which have recently been developed around these interactions is also presented in
Section 5.
Section 6 describes the effects of perturbation of the stable relationship between gorse and its herbivores by the application of inorganic fertiliser to the host-plant in the field.
Section 7 outlines another experiment aimed at assessing the effects of food quality on herbivore performance. The life history of Agonopter-ix uZiceteZIa was adjusted in the laboratory such that larvae fed at abnormal times of the year. The performance of these larvae when fed on natural gorse foliage is assessed.
Conclusions concerning the interaction between gorse and its phyto- phage community and the relevance of this study to the practice of biological control of weeds are discussed in Section 8.
Strong (1979), recently reviewed research into the application of island biogeography theory to the study of insect plant interactions.
Host-plant patch size can greatly influence the number of insect species which colonise a particular area. This has been demonstrated particularly well on Juniperus communis L., on which Ward & Lakhani (1977) analysed the relationship between patch-size and the colonising insect fauna. It has been assumed that the areas of gorse heathland involved in this study (see
Section 2.2) were each large enough to be independent of such species-area complications. 19.
Biological control of gorse can probably best be achieved by the establishment of insects attacking foliage (Girling, 1977) especially since seed control has largely been achieved (Miller, 1970). For this reason, the major emphasis of this study has fallen on describing the interactions between gorse foliage and the insects which attack it. The fauna attacking gorse roots was not sampled in the course of the study, though imagos of a number of species were encountered in the course of sampling amongst gorse foliage (see also Section 4). A :small amount of effort was expended in sampling amongst the reproductive structures of
Wlex spp (see Sections 2 and 4) but this was small compared to the time spent sampling gorse foliage-feeding insects and analysing the foliage itself.
Each section contains an introduction which summarises, and to some extent reviews, the literature relevant to each section. 20.
SECTION 2
SEASONAL CHANGES IN THE FORM AND STRUCTURE
OF GORSE PLANTS
2.1 Introduction
Numerous studies have now demonstrated how host-plant morphology, structure, and phenology can modify the abundance and variety of insects living on that host-plant. For example, host-plant biomass (Lawton, 1978";
Lawton & Schroder, 1977), host-plant form (Lawton & Schroder, 1977; Scriber
& Feeny, 1979), host-plant water content (Scriber, 1979), toughness (Wint,
1979) and host-plant phenology (Feeny, 1970) are all regarded as powerful factors in moulding phytophagous insect communities (Gilbert, 1979; Strong,
1979). Host-plant distribution and abundance are also extremely important
(Southwood, 1961; Strong, 1974, 1979; Ward, 1977; Ward & Lakhani, 1977), but their influences have not been considered here for reasons discussed later.
In a recent bibliography, Gaynor & MacCarter (1981) summarised and indexed all of the literature pertaining to Ulex europaeus published before 1977. The vast majority of the papers listed relate to control of gorse in various parts of the world, or to biological studies aimed at improving that control. Several other papers treat the taxonomy, biology and general ecology of Ulex spp. None of these papers adequately consider the seasonal changes in patterns of fruiting and flowering, or of growth in mature Ulex plants. There is even less known about the structure of the plants or their foliage. This section therefore describes the seasonal changes in a number of Ulex characteristics which previous authors have considered to be important influences on the phytophagous fauna of other plants. Skipper (1922) described the many different growth forms of Ulex spp.
which can be found in Britain. He could not distinguish "ordinary" from
"ericoid" growth forms in most cases, and no attempt was made to distinguish
the two types of foliage in this study. All samples were taken from "sun-
type" foliage of "non-cushion" plants of U. europaeus, and from "sun-type"
foliage of U. minor whether "erect" or "cushion-form" (Skipper, 1922).
2.2 Description of Field Sites
Samples of plant material and insects (see also Sections 3, 4 and 6)'
were collected at two sites:
(1) Yateley Common, Hampshire (abbreviated as YC) (Grid reference: SU
836 591) is a heathland .area of many square miles. Plants grow on Bagshot
Sands, and the common is part of the Surrey Heaths system. Calluna
vulgaris Salisb., Ulex europaeus and Ulex minor are the dominant plant
species in the association, while Erioa cinerea L., Festuoa rubra L.,
Molinia caerulea Moench., and Deschampia • flexuosa (L.) are also common.
Portions of the common are frequently burnt, and contain patches of heath-
land of all ages.
An area (100 m x 50 m) 2 km west of Blackwater, and 300 m south of
the A30 was chosen, and all sampling was carried out within this area.
The site was burnt in 1976, and gorse bushes were 3-6 years old (1 to 1.5 m
tall) during the course of this study.
(2) Windsor Great Park, Berkshire (abbreviated as WGP) (Grid reference:
SU 975 702) contain 20-30 ha of gorse at Smith's Lawn, growing on Bagshot
sand, and this area is at the northern extreme of the Surrey Heath system.
Ulex europaeus was the only gorse species present, and the understory was
almost exclusively Calluna vulgaris. Gorse bushes were 2 m tall, and were
estimated to be over 20 years old. An area of 100 m x 50 m between Guards
Polo Ground and Obelisk Pond was chosen, and all samples were taken from 22.
this area.
2.3 Materials and Methods
2.3.1 Ana_l^sis_of_ plant s_tru_cture_
Between 1200 and 1400 hours on each sampling occasion from May until
September, 3-15 samples, each of 3 shoots were chosen haphazardly from random co-ordinates. These were freeze-dried in an Edwards freeze-drier for two days. The length of each shoot was recorded, and the following measurements made:
(1) Vegetative buds or new shoots were removed, weighed, and sorted into size categories. From the numbers in each category, a median shoot length was determined for each sampling occasion.
In 1981, at YC, the shoots were individually measured as well. Agree- ment between these measurements and the estimated median was very close, as was the accuracy of median shoot length as a predictor of new shoot biomass (Figure 2.4). Median shoot length was therefore used as a measure of "living-space" for phytophagous insects (Lawton, 1979). Seasonal variation of "living-space" is described in Section 2.4.2.
(2) Reproductive structures were removed and counted. In order to describe the annual flowering and fruiting patterns, the proportions of each type of reproductive structure were recorded for each sampling occasion. The progression of reproductive activity in gorse is described in Section 2.4.1.
2.3.2 Foliage water content
In addition to the vegetation samples mentioned above, 5 further samples were collected randomly. Between 3 and 10 subsamples of new shoots were weighed, dried in an air oven at 80°C for 2 days, and reweighed.
Seasonal and morphological variation in foliage water content are discussed 23.
in Section 2.4.3. Differences of water content between different portions of individual shoots was also examined.
2.3.3 FoHag^ _to_ughne^s^
From the same 5 samples, 20 new shoots were chosen at random. For each shoot the tissue toughness of spines at 1 cm intervals from the apex was estimated by measuring the force required to shear the spine with a
29 S.W.G. wire made of stainless steel. The apparatus designed to measure this force is shown in Figure 2.1. The spine was removed from the stem and placed on the metal platform over a slit of 0.7 mm, and a pan of 25 g was suspended from it. The spine was held down by a weight, while weights were added to the pan with 20 g increments. The weight required to shear the gorse spine was recorded. Since the wire broke with weights in excess of 1.2 Kg, this was the upper limit to measurement. Similarly, 25 g was the lower limit of sensitivity. Because the wire stretched it was replaced after 5 measurements.
The aim of these measurements was to gauge the seasonal variation in resistance of gorse foliage to attack by mandibulate insects in particular.
This shearing method was therefore preferred to the needle penetrometer used by Prestidge (1980) and Wint (197 9). Measurements only began in mid- summer 1980, and early season data discussed in Section 2.4.4 was not obtained until 1981. In these later experiments, the toughness of new stems as well as spines was measured. The seasonal variation in toughness of gorse tissue is discussed in Section 2.4.4.
2.4 Results
2.4.1 Patterns_of_ flowering and fruiting
Reproductive buds formed in the axes of primary and secondary spines of Ulex europaeus from early August. Sporadic flowering occurred through- Figure 2.1 : (a) Apparatus for measuring foliage toughness.
B holding block
W wire
S gorse spine
(b) Foliage nomenclature,
fb flower bud
ps primary spine
sg secondary growth
pg primary growth
vb vegetative bud 24. 25.
out winter, but most buds remained dormant until late winter and early
spring. The flowering rate increased in March and reached its peak in late
April. Flowering ceased by mid-June, pods developed through June, and
dehisced in late June and July. A timetable for these events is given in
Appendix I, and shows that there was very little variation between years
in the onset of various developmental events. In fact, despite the disparate climatic conditions experienced between years, gorse life-history
coincided within 7-10 days.
Figure 2.2 shows the change in the proportion of each type of Ulex europaeus reproductive structure through spring and summer. Unfortunately the sampling programme was not complete in 1979, and the results presented
in Figure 2.2 were augmented by further sampling 1980. The slight discrepancies between patterns at each site seem to relate to the high proportion of flowers in early May at YC, and the more rapid maturation of flowers at WGP in 1979. Figure 2.2 shows clearly that each type of repro- ductive structure (bud, flower, pod) is present for an almost constant, though very short period of time in each year. These structures therefore present a temporary though predictable resource to those insects which are
specialist feeders on gorse reproductive structures. The importance of this predictable pattern to the insect fauna attacking gorse reproductive structures is discussed in Section 4. By comparison Figure 2.2 also shows a representation of changes in the reproductive structures of Ulex minor through its flowering period. The pattern of flowering and fruiting closely resembles that of Ulex europaeus, though Ulex minor flowers in late summer and autumn, while the fruits overwinter to dehisce in the following summer.
In this case, the associated insect fauna has not been closely examined.
2.4.2 Seasonal patterns of_grx>wth in mature^ Ulex_spp
Vegetative buds formed in the axils of primary spines with stems, Figure 2.2 : Patterns of flowering and fruiting in U. europaeus and U. minor.
Windsor Great Park U. europaeus
• • buds
x x flowers
o o old flowers and young pods
A A pods
Yateley Common U. europaeus
Yatel^y Common U. minor (over) 26.
/o reproductives
A M J J A 27.
% reproductives protected by leaves. Some buds also developed between secondary spines
and primary spines (Figure 2.1b). In early spring these buds began to
expand. Growth of Ulex europaeus occurred in two phases. Those branches
not bearing pods began to grow very slowly in late April. These included
branches growing in the shade, and all immature plants. Buds on all other
shoots did not burst until mid-May, and then growth was very slow. Figure
2.3 shows the increase in the median length of new U. europaeus shoots measured at WGP and YC in 1979 and 1980, and mean length in 1981. In all
cases, the growth rate (slope of the line) was small during the first weeks
after bud-burst, which was the period when seeds were produced by the plant. Rate of growth did not increase until mid-June, when flowering
ceased and pods began to dehisce. The onset and rate of new growth on any
branch or shoot appeared to be determined by the resources required to
develop the reproductive structures on that shoot. While the initiation of growth seemed to be affected by the pod load of a branch or shoot, there was no significant negative relationship between the number of pods per cm and either the length of new shoots or the number of new shoots per cm when measured in mid-June. Very similar observations were made by Hamilton
(1980) but she was not able to demonstrate this relationship statistically either. Despite this variation of developmental activity between individual
stems, the vast majority of new shoots develop together from mid-May.
Figure 2.4 shows the very close relationship between the median length of new shoots and the biomass of those shoots measured in May, June and early July, 1979. From this relationship it was assumed that median shoot length was a good predictor of biomass and shoot surface area during the period of greatest phytophagous insect activity (May-July). Further evidence that the median shoot length estimate presented here represents an accurate assessment of shoot length is given in Section 6. The in- Figure 2.3 : Patterns of foliage growth in Ulex europaeus and Ulex minor.
(Use of standard error bars indicates the use of the mean
shoot length rather than the median) 29.
1979
Ue WGP
Ue YC
Um
T
mean shoot length
cm.
• Ue YC 1980
x Ue YC 1981
T
M s Figure 2.4 : The relationship between shoot length and foliage biomass.
• • Ulex europaeus
x x Ulex minor
2 Statistics b t R
YC 18 May 1979 • 0.003 10.4 96.0
WGP 12 June 1979 0.094 8.4 89.0
YC 18 June 1979 0.009 7.8 92.2
WGP 16 July 1979 0.03 42.9 99.8 g.
dry wt.
of foliage / sample
Total length of new shoots per sample (cm.) 31.
fluence of available shoot biomass on the phytophagous insect fauna is considered further in the discussion, and again in Sections 5 and 6.
2.4.3 Season a l_ch an ge s in f o_l i age^ water^ conten t
There was no significant difference between the water contents of shoots of different length on a single sampling occasion. Figure 2.5 shows the seasonal change in the water content of whole shoots of Ulex europaeus foliage at two sites in 1979, one site in 1980, and the seasonal change in the water content of U. minor in 1979 and 1980 at YC. Data are presented in Appendix III. From the end of June, the water content of U. europaeus foliage declined steadily throughout summer from approximately
75% to approximately 607 . At this stage there was little variation in the ? foliage water content between years or between sites. The water content of foliage measured in mid-June was higher than that measured immediately after bud-burst. Highest water contents were found at the time of highest foliage growth rate (see Section 2.4.2). Ulex minor foliage showed a similar very stable pattern. Peak foliage water content occurred in late
June, followed by a steady decline through summer to a level of 50-60% water content. Throughout the season the water content of U. minor foliage was lower than that of U. europaeus, reaching a peak of less than
70% (Figure 2.5).
Figure 2.6 shows the variation in foliage water content within individual shoots of U. europaeus during 1980. The water content of the basal 2 cm of new shoots began to decline at the end of June. The next
2 cm portion of stem followed a similar pattern. The penultimate 2 cm portion remained succulent until mid-July, but then became tougher with a lower water content in late-July and August. The actively-growing terminal
2 cm of each shoot remained succulent until mid-August before water-content declined. Part of each shoot was succulent throughout the developmental Figure 2.5 : Seasonal variation of mean foliage water content in Ulex
euro-paeus and Ulex minor.
(Mean water content of whole shoots) 32.
U europaeus 1979
. WGP
80 * YC
70
60
50
U europaeus YC
% foliage water content
r 1 1 T - —T
U minor YC 80
70
60
50
M Figure 2.6 : Within shoot seasonal variation of foliage water content.
• • terminal 2 cm
o o next 2 cm
A A " 2 cm
x x basal 2 cm
Yateley Common 1981 % water content 80 J
70
60 34. period of folivorous insects (see Section 4).
2.4.4 Sea_sona^va_ria_tion of Ul^_eurapaeus_foliage toughness
Preliminary measurements of foliage toughness made in 1980 using the method described suggested that at least part of each shoot was succulent and soft through most of the summer period. In 1981 measurements of
foliage toughness were made throughout the season, and the results are
shown in Figure 2.7. The equipment only allowed exertion of force to a
limit of 1200 g, though toughness often exceeded this limit later in the *
season. Standard error bars and statistics relating to Figure 2.7 could
therefore only be applied where all results were less than 1200 g.
In the early stages of growth, all foliage was uniformly succulent.
By mid-June there was a toughness gradient along the shoot from base to apex, though the terminal 1 cm of the shoot remained soft. By July the actively growing terminal 2 cm of each shoot remained soft, though the remainder was already mature and tough. From July onwards, the mean
toughness of spines in the terminal 2 cm increased gradually until growth was completed in mid to late August when all spines where extremely tough
and resilient. Along with foliage water content, these results suggest that at least part of gorse foliage remains succulent and apparently edible throughout the developmental period of folivorous insects.
The method employed did not allow measurement of U. minor tissue hardness because spines were too small to handle.
2.5 Discussion
Southwood (1972) pointed out that the physical structure of a plant can have a strong influence on the ability of a phytophagous insect to
live on that plant, particularly in terms of:
(1) The ability to find a host Figure 2.7 : Seasonal variation of foliage toughness,Ulex europaeus.
• • toughness of spine 1 cm from shoot apex
x x " " " 2 cm " " "
M 11 o o " " 3 cm " " 35.
Shearing
force
(9)
1000 •
800 •
600 •
400 •
200 - 36.
(2) Potential desiccation
(3) Attachment and shelter
In defining his "host-finding hurdle", Southwood was particularly concerned
with the influence of host-plant abundance and patchiness, host-plant
apparency (Feeny, 1976), host-plant form, and their influence on the
success of insect dispersal. Even within a preferred host-plant however,
phytophagous insects are very often limited in their ability to exploit the
plant by tight requirements for particular host-plant tissue or feeding
position. For example, insects feeding in pods, or species galling shoot
tips. Southwood's "host-finding hurdle" concept can therefore be extended
to include the requirement for insects to find resources within the plant
that are very often limited in time and space. It seems likely, therefore,
that relative or absolute shortage of certain resources within a plant
plays an important part in the timing and success of phytophagous insect
attack. In this section the existence of possibly limiting resources has
been demonstrated, and their impact on the gorse fauna is discussed further
in Section 5.
The general principle that larger and therefore physically more
diverse plant-forms bear more insects has now been proposed by a number
of people (e.g. Lawton & Schroder, 1977; Lawton & Strong, 1981) and a number of mechanisms for this relationship have been suggested. In bracken, a large part of the seasonal variation of phytophagous species
diversity was attributed to the expansion of what Lawton (1978) called
"living-space" through the growing season. Bracken is a perennial species, with no aerial parts in winter and early spring. Frond area and hence
"living-space" increases rapidly from mid-May to reach a maximum by mid-
summer. The "living-space" concept is more difficult to apply to Ulex europaeus. Gorse is an evergreen species, though only the most recent 37.
years' growth is green. Foliage produced in one year senesces and thickens very rapidly in early July of the following year. New shoots attain their maximum length several weeks later. Unlike bracken therefore, the green foliage of Ulex spp presents an almost constant suitable frame- work for shelter and attachment of phytophagous insects throughout the year, though modified by the presence of reproductive structures in winter and spring. The structural composition of the green foliage varies dramatically with the season however. Between the onset of new growth in mid-May and completion of senescence of old shoots at the beginning of
July, gorse foliage comprises a mixture of new and old growth in varying proportions. Both Ulex europaeus and U. minor lack true leaves, and the modified stems which make up the foliage of both species are necessarily tough, fibrous and rigid for most of the year. This foliage appears to be highly resistant to insect feeding, and indeed damage of mature tissue by insects was almost never observed. New growth however, is succulent, and presumably highly edible. Figure 2.8 shows the proportion of new growth amongst the green foliage of gorse in spring. During the first month of development (mid-May to mid-June), new growth accounts for approximately
5-10% of total green foliage biomass, but rises quickly after that to reach 100% as old foliage senesces in late June and July. The influence of this apparent rarity of new foliage in early spring on the phytophagous fauna is considered again in Section 5.
Patterns of flowering and fruiting in U. europaeus were similar be- tween years and between sites. There was some variation in the speed of development of reproductive parts, but the different types of tissue i.e. buds, flowers, pods etc., occurred at the same time of year in all cases.
In this case, resources for phytophagous insects are undoubtedly limited by being rare in time rather than in space. Each tissue type exists for Figure 2.8 : Dry weight of new growth as a percentage of total green
biomass.
(Bar denotes the period of senescence of old growth) % 100 4
50 39.
a limited time span, and insects can only exploit each tissue-type during
that time. The impact of host-plant phenology on the insect fauna is
therefore self-evident in this case, and is considered further in Section
5.
The increase in foliage toughness through the season described in
this section is the result of two complementary processes:
(1) Decreasing foliage water content
(2) Increasing tissue density
Recent studies suggest that foliage water content has far greater import- ance in modifying the feeding performance of insects than was previously
thought. Scriber (1977). showed that Hyalophora cecvopia L. larvae fed on
Prunus foliage in which water content was high, utilised plant biomass, energy, and nitrogen better than larvae fed on leaves with low leaf water but identical in other respects. In 1979, Scriber showed that the larval feeding performance of chewing insects, especially tree-feeding species, could be improved by supplementation of leaf water content.
The foliage water content of forbs is normally between 69 and 91%, whereas the water content of trees and shrubs is between 51 and 75%
(Scriber & Feeny, 1979). New foliage of tree species normally have a water content of 70-75%, but the content of individual leaves normally declines through the season to 50-60% by late summer (Scriber & Slansky,
1981; Wint, 1979; Schroeder & Maimer, 1980). Seasonal variation in the foliage water content of Ulex spp therefore closely resembles changes in the same measure in most trees, despite the extreme difference in foliage growth forms. As Wint (1979) found in various trees, there was some small variation in gorse foliage water content between areas and between years.
Despite the general decline in foliage water content through the summer, it has been shown that a proportion of the new foliage remained succulent until early August. This proportion declined from 100% of new
foliage in early spring to approximately 15% in late July when the terminal
1 cm of each shoot was succulent but the remaining 5.5 cm of the mean
6.5 cm long shoot had matured. It is therefore possible that phytophagous
insects on gorse face an increasing relative shortage of foliage with
sufficient water content, though the absolute amount of such foliage changes little through summer. How this might affect individual insect
species is impossible to predict without some knowledge of the feeding biology of each species. The published information discussed here is almost entirely concerned with mandibulate species, though the principles involved must also relate to mesophyll-feeders.
As with foliage water content, the role of foliage toughness in modifying the larval performance of phytophagous insects is known (e.g.
Tanton, 1962). The mode of action appears to be a reduction in the
"approximate digestibility" (AD) and consumption rate (CR) of foliage
(Waldbauer, 1968; Scriber & Slansky, 1981) with increasing fibre, lignin, and other structural components which contribute to foliage toughness.
Toughness is often assessed using proximate analyses of such structural components (e.g. Jobson & Thomas, 1964; Lawton, 1976), while actual measurement of tissue toughness is more rare (e.g. Tanton, 1962; Wint,
1979; Prestidge, 1980). The measurements made in this study allowed comparisons to be made between the foliage of U. europaeus at different sites and in different years though patterns were very similar in each case. Comparison of different portions of gorse shoots at different times of year showed that the region immediately behind the active terminal growing point of each shoot remained very soft throughout the growing season, i.e. until early August. Spine bases at 3 cm from the apex were always tougher than more terminal portions of the shoot. This pattern is almost identical to that shown by the seasonal variation of water content in different portions of the shoot. Since toughness could only be measured to an upper limit of 1200 g, the close relationship between water content and foliage toughness could not be tested, but comparison of Figures 2.6 and 2.7 shows the similarity very clearly.
As with water content, soft tissue became relatively more scarce through the season, but the absolute amount of active soft tissue remained very much the same from early spring until August.
The influence of foliage toughness on the larval performance of insects is impossible to assess, as it was for water content, without detailed biological information regarding the species involved. Such measurements give an indication of how handling time or consumption rate might be influenced by changes in foliage toughness. Its influence on digestibility is considered in more detail in Sections 3, 5 and 7.
The inextricable relationship between foliage water content and foliage toughness is recognised in the literature (e.g. Scriber, 1977,
1979; Scriber & Feeny, 1979; Scriber & Slansky, 1981; Matt son, 1980; Feeny,
1970; Wint, 1979; Schroeder & Maimer, 1980), and in experimental studies concerning the performance of phytophages with varying food quality, efforts are often made to exclude them altogether as variables (e.g. Fox
& Maca.uley, 1977; and see Section 7). Their relevance to the structure of the gorse phytophage community is discussed again in Section 5.
Results presented in this section show that there are wide seasonal variations in the form and structure of gorse plants. Each of the factors assessed are known to affect the phenology and performance of phytophagous insects in other insect host-plant systems. Further consideration of such possible interactions is given in Section 5. 42.
2.6 Summary
1. Ulex euvopaeus sets reproductive buds in autumn, and these produce the
large bulk of their flowers in April and May. Large buds, flowers and
pods are present on gorse bushes for relatively short but predictable
periods. Well developed synchrony with host parts is therefore essential
to potential herbivores.
2. New growth begins in mid-May and ceases in August. In early July
% previous season's growth senesces, leaving current growth as the only
green parts of gorse. For the first month only 7.5% of green biomass
is succulent new growth and may be effectively hidden from potential
herbivores. Between^mid-June and mid-July this figure rises from 7.5%
to 100%.
3. Foliage water content of gorse follows similar seasonal trends to that
of trees. Contents of whole shoots fall as low as 50%, but only in
very late sunnier. Terminal 1-2 cm of growing shoots remain very
jsucculent throughout summer, so that the absolute amount of succulent
tissue remains constant, though the amount relative to non-succulent
tissue drops steadily. There may therefore be increasing difficulty
for insects in finding appropriate edible food.
4. Basal portions of new shoots mature and toughen within one month of bud
burst. Growing tips and spines up to 2 cm from the apex remain soft
and tender until late in the growing season, while tissue further away
from the tip hardens progressively. As with water content, the absolute
amount of soft tissue remains constant until late in the season, but
the amount relative to inedible foliage drops progressively as shoots
grow. Southwood's (1972) "host-finding hurdle" concept can be logically extended to include the ability of insects to find food within host- plant foliage. Escape of reproductive parts in time, escape of new foliage in space, and the seasonal changes in foliage toughness and water content may all contribute to moulding the seasonal pattern of utilisation of gorse by its phytophagous insects. 44.
SECTION 3
THE PRIMARY AND SECONDARY CHEMISTRY OF
GORSE FOLIAGE
3.1 Introduction
It is becoming increasingly obvious that host-plant constituents have a profound impact on the performance of herbivorous insects (Van Emden &
Way, 1973). Southwood (1972) first reviewed the problem, referring to the
"nutritional hurdle" to be overcome by insects evolving to feed on a new host-plant. The two components of such a hurdle are:
(1) Quality of the host-plant as a food source (primary plant
chemistry)
(2) Host-plant protection by toxic or anti-feedant substances
(secondary plant chemistry)
McNeill & Southwood (1978) showed that nitrogenous compounds rather than energy content or carbohydrate content were the components of host- plants most likely to limit insect performance. This conclusion was based on the early work of McNeill (1973), Van Emden & Bashford (1971), Hill
(1976), and the observation that the nitrogen content of all phytophagous insects far exceeded the nitrogen content of their food. Since then numerous studies have demonstrated that the nitrogen content of insect food often modify the performance of phytophagous insect species (Lawton, 1976;
Mattson, 1980; Prestidge, 1980; Hill, 1982; McNeill & Prestidge, 1982;
Scriber & Slansky, 1981). Among these studies, Lawton (1976), Prestidge
(1980) and Hill (1982) have also considered how the quality or quantity of nitrogenous compounds in host-plants can affect the species composition of the phytophagous fauna of that plant in natural habitats. In this section, the quality of gorse foliage as food for phytophagous insects is examined, and further consideration of the effect of food quality on the fauna can be found in Section 5.
Secondary compounds are those which appear to have no primary role in the metabolism of the plant in which they are found, and which can modify
insect behaviour or performance. Secondary compounds are of numerous chemical types, and their effects on insects can take numerous forms
(Rosenthal & Janzen, 1979). In this study, the role of secondary compounds in modifying feeding and food utilisation by insects was of interest. It was not possible to consider the full range of known compounds in gorse foliage, but the seasonal variation in foliage of levels of the majority of the more important compounds was measured; i.e. alkaloids, isoflavones, silica, unusual amino acids, cyanogenic compounds, and phenolic compounds.
These groups were chosen because in general foliage of species of the
Leguminosae are particularly rich in these compounds.
In the search for new alkaloids of medical importance, a considerable amount of preliminary identification of alkaloid content has been carried out in many plant species, especially in the Leguminosae (e.g. Earle &
Jones, 1962; Faugeras et al., 1962; Smolenski et al., 1972, 1973, 1974a, b).
In Ulex europaeus 4 quinolizidine alkaloids, sparteine, cytisine, N- methylcytisine and anagyrine, have been recorded (Clemo & Raper, 1935;
Faugeras et al., 1962). Cytisine appears to be absent in all parts except flowers and seeds. In seeds, it reaches concentrations of approximately
0.82% by dry weight (White, 1943).
The isoflavones of the Leguminosae have also been extensively studied
(Harborne, 1969) and in Ulex europaeus appear to be particularly associated with flowers and fruits (Harborne, 1969).
The apparently fibrous nature of gorse led to the inclusion of silica in the analysis of foliage composition. Silica content can reach high
levels in some plant tissues, and is generally regarded as a feeding modifier for folivorous insects (see Lawton, 1976).
Though their role in foliage has not been examined closely before, the
toxic properties of "unusual" amino acids in the seeds of the Leguminosae has been demonstrated many times (e.g. Rehr et at., 1973). Recently it has been shown that one of these amino acids, L-Dopa, is present in the foliage of Cytzsus sooparzus (Kohlmunzer et at. 1975) and can also contribute to 9
seasonal changes in the food quality of grasses for phloem-feeding insects
(Prestidge, 1980; McNeill & Prestidge, 1982).
Many members of the Leguminosae are capable of producing HCN from cyanogenic systems in damaged foliage. Perhaps the best known example is the cyanogenic properties of Lotus comiculatus (Jones et at., 1978). The precise role of Cyanogenesis in the performance of phytophagous insects is open to some discussion (Bernays, 1982) but it is almost certainly a deterrent, at least for some insects.
The effects of phenolic compounds such as tannins on insect performance and seasonality were first pointed out by Feeny (1969, 1970) who attributed the spring-feeding of winter moth to the relatively low tannin content in foliage at that time.
Feeny's observations that oak-leaf tannins inhibit enzyme activity led
Wint (1979, 1982) to develop a proximate analysis which assessed the ability of foliage extracts to adversely affect insect nutrition. He used the standard starch/amylase reaction to mimic a living system, and invest- igated the affects of exposing the amylase to aqueous extracts of leaf tissue from 5 species of tree.
Most of the published information regarding the chemistry of plants is of limited use for two reasons. Very few studies take any account of the large seasonal changes in the chemical composition of plants. Often the presence or absence of a compound is recorded, but samples are taken on only one occasion. Often the date of that sample is not recorded.
Where sufficient information concerning seasonal variation is available, the information is often inadequate because insufficient information is provided concerning the type of plant tissue used for the analysis.
0*Donovan et al (1959) provided a useful estimate of the seasonal variation of carotenoid levels in Ulex europaeus foliage but made no distinction between new growth and old foliage, proportions of which change radically through the year (see Section 2). This is also true of Jobson & Thomas
(1964) who otherwise provide very important background information concerning the chemistry of gorse foliage.
Zabkiewicz & Gaskin (1978) described the seasonal variation of foliage surface wax and trichome concentration, and ultimately this is the only paper which adequately summarises such changes in the chemistry of gorse foliage. This section therefore describes the quantitative variation of 6 types of plant secondary compound in the new foliage of Ulex europaeus through the season. The effects of changes in concentrations of secondary compounds on the insect fauna of gorse are discussed in Section 5.
3.2 Sampling and Storage Methods
Samples of Ulex europaeus foliage were taken at approximately weekly intervals at YC during spring and summer 1979-81, and at WGP during 1979-80.
Samples of Ulex minor foliage were collected at YC at approximately weekly intervals during spring and summer 1979-80. On each sampling occasion in spring, 3 stems bearing many new shoots were chosen haphazardly from each of 3 sets of random co-ordinates. These were stored in the dark, and placed in an Edwards freeze-drier within 40 minutes. After drying to
0.05 mm Hg, the new shoots were removed, ground to powder in a Glen Creston 48. ball-mill and stored dry in a deep-freeze. Later in the season as current growth grew longer the sample consisted of 3 randomly chosen new shoots.
This change in sampling procedure did not appear to significantly affect the results of any analyses.
Some analyses of older foliage were also carried out, and this material was treated in a similar fashion.
On several occasions U. gaU'L'L foliage was also collected, freeze- dried, and ground to provide material for nitrogen content analysis.
Sporadic analyses of the nitrogen content of other parts of gorse plants were also carried out. This material was sampled and stored in a similar fashion to that used for gorse foliage.
Dried material was used for all analyses except for cyanide and polyphenol estimation. For these tests fresh material was collected from plants growing at Silwood Park and tests were carried out within minutes of collection. Results were checked using material collected from YC, but no significant difference was apparent.
3.3 Analytical Methods
3.3.1 Analy_sis_of_ nitrogen_conterit
(a) Total nitrogen
1. Weigh an amount (approximately 0.03 g) of powdered gorse foliage into
a kjeldahl boiling flask.
2. Add 2 ml of concentrated "nitrogen-free" H^SO^.
3. Add 1 kjeldahl catalyst tablet (1 g Na2S0^ and 0.05 g Selenium powder).
4. Heat the mixture in the tube gently for an hour using kjeldahl
apparatus (Bradstreet, 1965).
5. As the mixture clears, heat more and more until boiling. Shake
frequently. 49.
6. When mixture remains straw-coloured on shaking, remove from heat and
cool.
7. Transfer digest to a volumetric flask and make up to 50 mis with
Distilled water.
8. Store a 10 ml subsample, and discard remainder.
9. Measure concentration of ammonium ions (in ppm) using a Technicon
autoanalyser equiped for the indo-phenol technique described in
detail by Varley (1966). Standards are derived from a solution of
(NH ) SO . 4 2 4
4.7162 g (NH ) S0 /£ = 1000 ppm of nitrogen 4 2 4
10. Digest 2 blanks comprising catalyst tablet and acid only, and subtract
from results where necessary.
11. Calculation:
total nitrogen content = ppm x 1000 x 10 (mg/g) sample wt. 50 (mg)
(b) Soluble nitrogen
1. Transfer a known amount (approximately 0.1 g) of dry, powdered gorse
foliage to a 5 x 2.5 cm stoppered tube.
2. Add 2 mis of 2.5% trichloroacetic acid containing 0.02% phenol.
3. Shake mixture for 8 hours.
4. Centrifuge for 3 minutes in a Quickfit microcentrifuge at 5000 r.p.m.
5. Transfer 1 ml of supernatant to a kjeldahl boiling flask.
6. Continue as for total nitrogen (see 2 above).
7. Digest 2 blanks including 1 ml 2.5% trichloroacetic acid, and subtract
from results where necessary.
8. Calculation:
soluble nitrogen content = ppm x 1000 x 20 (mg/g) sample wt. 50 50.
3.3.2 Ana.l^sis_of_ foliage caloirific^ content^
1. Weigh a known amount (approximately 0.2 g) of dry, powdered gorse
foliage.
2. Form into a pellet using a Gallenkamp CB 340 briquette press, with
0.1 g benzoic acid (BCS 190h) as binding agent.
3. Determine the galvanometer deflection caused by ignition of the pellet
using a Gallenkamp CB 370 ballistic bomb calorimeter following the
technique laid down in the accompanying manual (issue 2).
4. Determine calorific value from a calibration curve obtained by ignition
of known amounts of benzoic acid (26.47 KJ/g).
5. Correct the value obtained to account for the calorific content of the
added 0.1 g of benzoic acid and other intrinsic heat sources described
in the manual.
3.3.3 An a_Tys i_s_of soluble c_ar^b^hy_dra_te_con_terit
This procedure closely follows that used by Allen (1974).
1. Weigh 50 mg of dry powdered gorse foliage into a 100 ml conical flask.
2. Add 30 ml of distilled water, cover neck with a marble, and simmer
very gently on a hotplate for 2 hours. Maintain level at approximately
30 ml during heating.
3. Cool slightly, and filter through No. 44 filter paper into a 50 ml
volumetric flask. Dilute when cool.
4. Into separate boiling tubes pipette 2 ml aliquots of each standard,
each extract, and 2 water blanks.
5. Add 10 ml anthrone reagent with tube immersed in cold water, and mix.
6. Place tubes in beaker with boiling water, and boil for 10 minutes.
7. Allow to cool in a cold water bath in the dark.
8. Measure the optical density at 625 run with a red filter, using water
as a reference. 51.
9. Draw calibration curve from readings of standards, and then obtain
sample determinations from the curve. Subtract blank determinations
where necessary.
10. Calculation:
soluble carbohydrate = Sample determination x extract volume (ml) (% of dry wt.) 10 x aliquot (ml) x sample wt. (g)
11. Reagents:
Stock solution of glucose. Dissolve 0.25 g dry D-glucose and dilute
to 1 £ in water (1 ml = 0.25 mg glucose). Prepare daily standards
to give 0 to 0.2 mg glucose per 2 ml aliquot.
Anthrone reagent. Add 760 ml conc. H^SO^ dropwise to 330 ml water
in a boiling flask .in running water with mixing. Add 1 g anthrone
and 1 g thiourea and dissolve using a magnetic stirrer. Transfer to
dark bottle and store in fridge. Use after 2 hours. Reagent can be
used for several days.
3.3.4 Anal£si_s_of alkaLoid_s
(a) Extraction
1. Carefully add a known amount (approximately 1 g) of dry powdered gorse
foliage to 50 ml of boiling 70% ethanol in a 150 ml conical flask and
leave overnight.
2. Carefully decant supernatant and store. Add 50 ml cold 70% ethanol
and leave overnight. Repeat until 5 extractions have been made at
daily intervals. Merge extracts.
3. Evaporate to 10 ml under vacuum at 38°C using a rotary film evaporator.
H S and leave over 4. Acidify concentrated extract to pH 2.5 with dil. °4 ~ 2
night.
5. Centrifuge at 5000 r.p.m. for 10 minutes and transfer supernatant to i a separating funnel. Discard precipitate. 52.
6. Partition 3 times with approximately 25 ml of dichloromethane to
remove lipid. Discard heavy fraction.
7. Adjust pH to 9.0-9.5 with dil. NaOH and extract 3 times with approx-
imately 20 ml'of analar Chloroform. Gently run chloroform fraction
through a filter funnel filled with anhydrous Na^SO^ to remove any
water.
8. Adjust pH to 10.5-11.0 and repeat 7.
9. Elute Na„S0, with 30 ml of analar chloroform and retain combined 2 4 chloroform fractions. Discard Na S0, after each extraction. 2o 4 10. Evaporate with care to dryness under vacuum at 38°C using a rotary
film evaporator.
11. Redissolve using minimum amount of analar chloroform, and transfer to
a stoppered tube.
12. Evaporate under a stream of warm air and redissolve in 0.5 ml of analar
chloroform or preferably 0.5 ml analar methanol.
This extraction was developed by Dr. Jill Harrison of the Agricultural
Botany Department, University of Reading.
(b) Thin-layer chromatography
1. Spot 10 yl of each sample on Silica gel G thin layer plates, along with
samples of available quinolizidine alkaloids at 0.1% by volume. (In
this case, cytisine and sparteine)
2. Run for 11 cm in a tank lined with chromatography paper and containing
1.5 cm of a chloroform-methanol mixture (80 + 20).
3. Remove plate and air dry. Visualise alkaloids by UV irradiation or
particularly by application of a fine spray of Drogendorff reagent.
Alkaloids visualise as orange-brown spots on a yellow background.
4. Determine Rf as distance of spot front from origin divided by distance 53.
of solvent front from origin,times 100.
Reagents:
Dragendorff reagent. See Harborne (1973)
This method is based on those of Santavy (1969) and Harborne (1973).
(c) Semi-quantitative alkaloid estimation (Planimetry)
1. Carefully spot 50 yl of each sample produced in (a) above onto
chromatography paper. Spot should be approximately 1 cm in diameter.
2. Make up 10 solutions of an available alkaloid (in this case cytisine)
ranging in concentration from 0.01% to 0.2% and spot onto chromatography
paper as above. Take care that all spots are 1 cm in diameter.
3. Dry paper, and visualise alkaloids using a fine spray of Dragendorff
reagent (see (b) above).
4. Using alkaloid spots of known composition as standards, compare the
intensity of sample spots and assign an approximate alkaloid
concentration to each sample.
5. Correct results for any differences in intensity due to spot size.
6. Calculate the amount of alkaloid in the original solution, and hence
alkaloid content of gorse foliage.
7. Results obtained are only approximate, but can be used to compare
relative changes in alkaloid content. In this case, results are
expressed as mg cytisine equivalents/g foliage dry weight.
3.3.5 Anjalysi_s_of_ i_s_of^avories^
1. Weigh accurately approx. 0.4 g of ground sample into a test-tube.
2. Hydrolyse for 30 mins at 100°C with 2 ml 2N HC1. Allow to cool.
3. Extract with ethyl acetate, make ethyl acetate extract up to 10 ml in
volumetric flask.
4. Take 2 mis of this extract (pipette), put in 5 ml beaker, allow solvent 54.
to evaporate. Take up residue in a few drops of 70% EtOH and apply as
small streak (5 cm in length) to a fluorescent Sigel TLC plate. Spot
markers alongside (genistein and 5 Me genistein) .
5. Develop plate in 11% MeOH in chloroform. Dry and observe in short-
wave U.V. light. Mark dark absorbing buds corresponding to markers
in Rf value.
6. Scrape off areas of plate marked. Elute with 5 mis EtOH.
7. Place 3 mis of eluate in spectrophotometer cell and scan over U.V.
wavelengths 200-300 nm against blank EtOH. Measure values of absorbance
at peaks (A genistein = 262 nm, A 5 Me genistein = 256 nm). mEX max 8. Make calibration curve by dissolving known amounts of genistein and
5 Me genistein in EtOH and making dilution series of these solutions.
This method was developed by M. Boardley and Professor J.B. Harborne at the Agricultural Botany Department, University of Reading.
3.3.6 Anal^is_o_f s^i H ca__c on tent
The procedure described here is from Allen (1974).
1. Weigh an amount (approximately 1 g) of dry powdered gorse foliage into
a weighed 100 ml conical flask.
2. Ignite at 550°C for 4 hours in a muffle furnace.
3. Add 5 ml conc. HC1, 5 ml distilled water, cover with a watch glass,
simmer gently for a few minutes on a heated sand bath, remove watch
glass and evaporate to dryness. Bake for 15 minutes.
4. Repeat, but do not evaporate to dryness.
5. Filter through a small ashless filter paper, wash filter paper with
hot distilled water.
6. Return filter paper plus residue to the flask, dry, and ignite at 550°C
for 4 hours. 55.
7. Cool and weigh flask and residue. Residue is regarded as silica.
3.3.7 AminjD acid_analysis
1. Extract soluble amino acids by shaking a weighed amount (approximately
0.1 g) of dry powdered gorse with 2 ml of pH 2.2 phosphate buffer for
at least 6 hours.
2. Analyse the amino acids contain in solution using a Locarte amino acid
analyser based on the automated liquid chromatography systems of Moore
et al (1958) and Spackman et al (1958).
3. Compare resulting record with trace from a mixture of amino-acids of
known composition and concentration.
3.3.8 An ail^si^s_o f^ fo_liar_cyan_ogeiiej^ij^
The details of this method are given in Tantisewie et al (1969).
1. Mix 5 ml of 1% tetrabase (Di - (4 - Dimethylaminophenyl) methane) in
chloroform with 5 ml of 1% copper ethylacetate in chloroform.
2. Dip strips of filter paper in mixture, dry, and store.
3* Crush fresh leaf material in 2 drops of chloroform in a stoppered
tube. Suspend a strip of test-paper in tube, and leave for one hour.
4. Intense-blue colour denotes the presence of HCN in the atmosphere.
5,. Foliage of cherry-laurel, Prunus laurocerasus is strongly cyanogenic,
and was used as a positive control for the presence of HCN. Negative
controls comprised drop of chloroform alone in a stoppered tube with
a test paper.
3.3.9 Ana_l£sis_of^ fol_ijir_erizyme_ inhibitors
This method was developed by Wint (1979, 1982).
1. Prepare 4 aqueous solutions of a - amylase (Type III-A, from Bacillus
subtilis, Sigma London Chemical Company Ltd) at concentrations of 0.4,
0.3, 0.2, 0.1 mg/ml (g/£). Prepare daily. 56.
2. Dilute 5 ml of 0.2% Iin KI solution to 250 ml with distilled water.
This is the indicator.
3. Prepare a phosphate buffer solution of pH 6.6 by mixing solution 1
(2.269 g KH P0 in 250 ml water) and solution 2 (4.75 g Na HP0 .12H 0 2 4 2 4 2
in 250 ml water) in the ratio 3:2.
4. Gently warm 1 g of soluble starch in 500 ml water on a magnetic
stirrer until the starch dissolves.
5. Mix 50 ml of starch solution, 20 ml of phosphate buffer (pH 6.6) and
% 20 ml of 1% (w/v) NaCl solution. This is the starch reagent.
6. Add 9 ml of starch reagent to 1 ml of each enzyme solution in test-
tubes in a 20°C water bath. Every 20 seconds withdraw 0.25 ml of
reaction mixture and add to 4 ml of indicator until the end point is
reached, i.e. when the mixture is isocolourmetric with 4 ml of i odine +
0.25 ml of reagent blank. With practice, this can be assessed
accurately by eye in natural light against a white background. Record
reaction time. The 4 reactions can be carried out simultaneously if
the starting times for each is staggered by 20 seconds, beginning with
the 0.1 mg/ml enzyme test.
7. Plot standard reaction time against the inverse enzyme concentration
times 15.
8. The Assay. Macerate freshly collected foliage in pH 6.6 buffer to
give an extract concentration of 60 yg/ml. Centrifuge for a short
time to precipitate the largest debris. Add 0.25 ml of the super-
natant suspension to 1 ml of each enzyme solution in test-tubes in a
water bath at 20°C, and allow to "Complex" for exactly 10 minutes. Add
9 ml of starch to each tube at an interval of 20 seconds beginning with
the 0.1 mg/ml enzyme solution, and sample every 20 seconds as described
above. 0.25 ml of plant extract and 0.25 ml of reagent blank are added 57.
to the indicator blank before colour comparison.
9. Plot test reaction time against the inverse of enzyme concentration
times 15. The procedure normally continues with calculation of the
slope of the graph of reaction delay against the inverse of enzyme
concentration, and comparison of this with Wint's calibration curve
to give an activity measure in "oak leaf tannin" equivalents. As delay
in reaction time caused by gorse foliage enzyme inhibitors was
negligible, this calculation was not used. Details of the remainder
of the procedure can be found in Wint (1982) .
3.4 Results
3.4.1 Nitrogen content
The variation in nitrogen concentration of 4 2 cm portions along an
individual shoot, from base to apex, was measured on 5 occasions in 1980.
Oneway ANOVA showed that there was no significant difference in the •
concentration of nitrogenous compounds along each shoot. Subsequent
analyses, .were therefore carried out on whole shoots.
Similarly, there was no significant difference in the total and
soluble nitrogen contents of shoots of different lengths but of the same
age in 1980. Nitrogen analyses were therefore carried out irrespective of
shoot length.
Se^-^nal changes in the total nitrogen content of Ulex europaeus
foliage at YC in 1979, 1980 and 1981 are shown in Figure 3.1, while Figure
3.2 shows the seasonal variation at WGP in 1979 and 1980. Figure 3.3 shows
the seasonal variation of foliage soluble nitrogen content in U. europaeus.
Supporting data concerning nitrogen content in Ulex europaeus and also data
from U. minor U. galHi and the reproductive parts of gorse are given in 3
Appendix IV. Figure 3.1 : Seasonal variation of total foliage nitrogen content of
Ulex euvcrpaeus at Yateley Common.
(Lowest trace is for old foliage N content)
1979, 1980
1981 58.
U europaeus YC Figure 3.2 : Seasonal variation of total foliage nitrogen content of Ulex
europaeus at Windsor Great Park, 1979, 1980.
(Lowest trace is of old foliage N content) 59. Figure 3.3 : Seasonal variation of soluble foliage nitrogen content of
Ulex europaeus foliage. 60.
WGP 1979
• old foliage
x new foliage
m 9 N^g dry wt.
WGP 1980
T 1—r •nr
J A s The nitrogen content of old foliage was measured in early spring.
Levels appeared to be very stable, varying between 15 and 20 mg of nitrogen/ g foliage dry weight total nitrogen and approximately 2 mg/g soluble nitrogen. Closed vegetative buds contained approximately 40 mg/g of nitrogen including 6 mg/g soluble nitrogen. At bud burst the concentration rose slightly but immediately began to decline. The concentration of total nitrogen declined at approximately 1.5 mg/g/week to reach a constant level of approximately 20 mg/g within 6 to 8 weeks at the end of July. This level was maintained until the end of September. Though nitrogen content was not measured during the winter months, the similarity of foliage nitrogen concentrations in October and February suggests that this level was maintained throughout winter. The concentration of soluble nitrogen varied in a similar manner, falling from 6 mg/g dry wt. to a constant level of approximately 2 mg/g by the end of July.
Broadly, this pattern appeared to be very consistent in both YC and
WGP, in all 3 seasons, in Ulex minor, and preliminary results suggest that
Ulex gallii showed similar seasonal variations (Appendix IV). Figures
3.1, 3.2 and 3.3 show, however, that there were some differences.
At YC there was some variation between years in the initial total nitrogen content of the vegetative buds, and also in the level found in foliage in the autumn (Figure 3.1). The rate of decline of nitrogen content was very constant, especially during June. The pattern of foliage total nitrogen content at WGP was quite different between 1979 and 1980
(Figure 3.2). Initial concentrations of nitrogen were similar, but the decline in 1980 was completely arrested at the end of June. This anomaly appears to be the result of heavy and frequent application of lime and fertiliser to an adjacent polo field under development during spring and summer 1980 (The Secretary, Guards Polo Club, personal dommunication). The Figure 3.4 : Seasonal variation of U. minor foliage nitrogen content. 62.
40
mg N U minor total N Per g dry wt.
30
20 H
1 n— T-l
M A S 63.
impact of fertiliser application on Ulex europaeus is discussed in Section
6.
The seasonal pattern of total nitrogen content of Ulex europaeus
foliage at YC and WGP in 1979 was almost identical in every respect (cf.
Figures 3.1 and 3.2). Ulex minor nitrogen content in 1979 was also very
similar to that of Ulex europaeus at both YC and WGP (see Figure 3.4).
Seasonal variation of soluble nitrogen content was very similar between sites, years, gorse species and is shown in Figures 3.3 and 3.4.
Only few analyses of Ulex gallii foliage nitrogen content were carried
out in 1979 and 1980, but the results in Appendix IV strongly suggest
similar seasonal patterns to those for the other Ulex spp in Britain. •
3.4.2 Foliage calorific^ _coiite_n_t
The calorific value of gorse foliage was almost constant throughout spring and summer, 1980 and 1981, at 24.5 KJ/g dry weight of foliage (see
Figure 3.5).
3.4.3 Soluble carbohydrate_con_tent
The concentration of soluble carbohydrates in two foliage samples was measured on several occasions in spring and summer of 1980 and 1981.
Concentrations were somewhat higher in early spring and declined slightly in early summer. The highest mean concentration was 105 mg soluble carbo- hydrate/g foliage dry weight, while the lowest was 56 mg/g. Concentration generally varied between 80-100 mg/g (Figure 3.6).
Seasonal variation of soluble carbohydrate content at YC was very similar from year to year, with the exception of one sampling occasion.
3.4.4. AlkaJLoid_content
In 1980 a preliminary analysis of the alkaloid content of Ulex europaeus was undertaken. Alkaloids were extracted and purified using the Figure 3.5 : Seasonal variation of foliage calorific value (Kilojoules/g
dry wt). 64.
Kj/g
X 1980
30 - • 1981
25 - I * * ** 2 2*. x 20 -
15 .
10 '
5 -
T"
M A Figure 3.6 : Seasonal variation of foliage soluble carbohydrate content
(% foliage dry weight). 65. methods described in Section 3.3.4. Since Sparteine sulphate was the only
standard available, it was not possible to undertake detailed analysis.
5 yl samples were run on a Pye-Unicam GLC (Jill Harrison, personal
communication) and the resulting trace was cut out. The area under the curve was weighed, and compared with the trace formed by a known amount of sparteine sulphate. This gave a very crude estimate of the seasonal variation of total alkaloid content in foliage, measured as "sparteine equivalents". This is shown in Figure 3.7a. This preliminary examination suggested that alkaloid levels were high in early spring but declined rapidly to a constant level by early summer.
In 1981, further samples were extracted and purified and semi- quantitative analysis was carried out using the planimetric technique described in Section 3.3.4. The seasonal variation of total foliage alkaloid content at YC in 1980 and 1981 is shown in Figure 3.7b.
Alkaloid concentration in new foliage was very high in early spring, but declined in early June to much less than 1 mg "cytisine equivalents'Vg foliags dry weight. Levels remained low throughout summer. Estimates of the alkaloid content of JJlex minor foliage in 1980 and U. europaeus foliage at WGP in 1980 also fitted the pattern described. One sample of U. europaaus foliage taken in September 1980 suggested that alkaloid levels may rise again later in the season, but the validity of this determination is uncertain. Figure 3.7 also suggests that the onset of the decline in alkaloid concentration may vary from site to site and from year to year, between mid-May and the end of June.
Thin layer chromatography showed that the alkaloid mixture was very simple. Only two components were resolved using the solvent system described earlier in the analytical methods. Rf values suggested that one component was sparteine, while the other was probably N-methylcytisine or Figure 3.7 : Seasonal variation of alkaloid concentration in foliage (mg
alkaloid equivalents/g dry wt).
A. 1979
B. 1980, 1981 67.
x Ue old foliage
A Um old • Ue new 3 - o Um new
mg/g of
sparteine equivalents
M 68.
B
WGP Ue 1979
YC Ue 1980 20 Um 1980 ®
Ue 1981 old *
Ue 1981 new
mg/g
of
Cytisine equivalents
10
0
* X
«o ^ o o© Xg M 69.
Table 3.1 : Seasonal variation of gorse foliage alkaloid composition as
shown by TLC.
? N-methylcytisine
Sample date Sparteine ? Anagyrine
15 April 81 (old foliage)
30 April 81 +
13 May 80 + +++ 14 May 81 +++ +
27 May 80 - ++
15 June 81 + +
23 June 80 ; - +++
9 July 81 - +
30 July 80 + -
22 Aug. 80 + -
12 Sept. 81 - -
19 Sept. 80 - - 70.
V j , anagyrme (Santavy, 1969). All three quinolizidine alkaloids are common amongst legumes, and are particularly associated with lupins and other members of the Genisteae (Harborne, 1973). Another very common alkaloid associated with this group, cytisine, was absent from foliage, which confirms the findings of White (1943) and Clemo & Raper (1935). Time did not allow further TLC work, and so alkaloid identification cannot be more posi tive.
Clemo & Raper (1935) reported that anagyrine appeared in new shoots of gorse from mid-May, peaked in early-June and declined to unmeasurable levels by the end of July. This is the pattern demonstrated by both TLC and semi-quantitative techniques in this study. White (1943) recorded no alkaloids in any part of gorse in November, but recorded information from the literature that concentrations of 1.85% of cytisine or a cytisine-like alkaloid could be found in gorse seeds. He suggested that high concentrations of alkaloids in other plant parts during seed-set could be linked to the accumulation of high seed alkaloid content. This has since been demonstrated in Cytisus scoparius (Smith, 1966). The high estimated alkaloid content of gorse foliage shown in this study coincided with the period of seed-set (see Section 2.2), and a similar process probably applies in Ulex spp. .
3.4.5 Is of lav one c^n_terit
Analysis of the content of gorse foliage was carried out at the Botany
Dept., University of Reading by Professor J.B. Harborne. Old and new Ulex euopaeus foliage collected at YC in 1980 were chosen for analysis. Some
Ulex minor samples were also used.
Levels of total isoflavone content were relatively high in early spring, declined rapidly at vegetative bud-burst (late-May) to low levels through summer and increased again in late summer and autumn (Figure 3.8). Figure 3.8 : Seasonal variation of total isoflavone content. 71.
8
U europaeus 7
• 1979
x 1980
Foliage
Isof lavone
content X
mg/g 0
2 •
1 • • • X X
r - "n 1— ~i—— r "
6
U minor 5
• 1979
4 x 1980
3
2
1 r_ 1 -T « 1— 1 1 J T" "
M J J A S 0 72.
Table 3.2 : Isoflavone content of Ulex europaeus and U. minor.
(Analyses by Prof. J.B. Harborne)
1979
Genistein 5 Me-Genistein Ulex sp Date (mg/g dry wt) (mg/g dry wt)
U. europaeus 17 April (old growth) 1.1 3.5 16 May 0.8 1.5 18 May (old growth) 0.9, 0.5 7.9, 8.1 31 May 0.8 1 June 0.7 1.6 12 June < 0.2 0.7 25 June 0.8 6 July <0.2 0.6 31 July 0.5 20 August 0.3 0.9
11 October 0.8 2.9
U. minor 18 May (old growth) •2.2 2.7 28 June 0.3 0.5 5 August 0.2 0.2
1980
U. europaeus 8 May 1.0 3.7 2 June 0.2 1.2 23 June 0.1 0.5 3 July 0.2 0.7 15 July 0.1 0.5 22 August 0.9 0.5
19 September 0.2 1.3
U. minor 21 May 0.2 0.7 3 June 0.3 0.7 23 June 0.3 0.5 3 July 0.3 0.9 22 August 0.3 0.1 73.
Two isoflavones were isolated from the foliage, genistein and methyl
genistein. Table 2 gives the seasonal variation in each of the components
in U. europaeus and V. minor.
3. A. 6 j>ilica_content
The silica content of new gorse foliage was measured on only 6
occasions in 1980 and 1981, and these results are presented in Table 3.
Silica content rose to a relatively high level, but only very late in
summer. Levels during the period of greatest insect activity, May-July, *
were approximately 0.5% of foliage dry weight. Lawton (1976) regarded
0.5% as a low silicate concentration, unlikely to affect insect nutritional
performance.
Jobson & Thomas (1964) examined the silica content of gorse foliage
at monthly intervals, but failed to separate new shoots from old foliage.
Their results showed that silica content of mixed foliage remained
approximately 0.5% throughout the year. Coupled with the data presented
here, the silica content of new and mature foliage must be similar.
Jobson & Thomas also measured % ash content (including silica) of dry
foliage and found that ash content peaked in June and July. This pattern
has been confirmed in this study, but nothing is known about
the composition of this ash apart from its silica content.
3.4.7 Unusual amino acids_
The water soluble amino acids in 25 samples of gorse foliage collected
in 1979 and 1980 were analysed. The composition of the samples was
expressed in graphical form, and comparison of these sample traces with
traces produced by known standards showed that all sample amino acids could be identified as essential metabolic amino acids with the exception of
L - Dopa. This amino acid has been implicated as a toxin of frugivorous 74.
Table 3.3 : % silica content of new, dry, Ulex europaeus foliage.
%
21 May 81 0.23
10 June 81 0.67
23 June 81 0.25
0.45
30 June 81 0.45
30 July 81 0.29
0.28
0.57
15 Aug. 81 0.60
22 Aug. 81 1.30 insects in legume seeds (Janzen, 1969) L - Dopa was only present in very small amounts, even in seeds, and appeared to be the only potential anti- herbivore secondary chemical of this group found in gorse. The effect of the balance between growth promoting and growth inhibiting amino acids on the performance of phloem-feeding insects has recently been recognised
(Prestidge, 1980; McNeill & Prestidge, 1982). Time did not allow detailed analysis of the composition of gorse foliage in this detail.
3.4.8 Foliage cyanogenesis
The cyanogenic properties of 10 Ulex europaeus foliage samples from
5 plants collected at Silwood Park were tested monthly from April to
September 1981 using the method of Tantisewie et al (1969).
No cyanogenesis was ever detected in Ulex europaeus foliage.
3.4.9 Fo^iar_en_z^me^ inh_ibi_tor^ conterit
The activity of enzyme inhibitory substances in Ulex europaeus foliage at Silwood Park was assessed at monthly intervals between May and August
1981..... In Figure 3.9 the reaction time of the starch/amylase reaction is plotted against the inverse of 4 enzyme concentrations, as described in the methods above. Each monthly graph shows the variation in reaction time with and without added plant extract. The difference between the slopes of the two lines represents the delay due to enzyme inhibitory activity in plant extracts. Such activity was negligible, if not absent, in all 4 months. The activity of an equivalent concentration of oak
(Quercus robur) extract is shown for comparison. Oak contains large amounts of both condensed and soluble tannins, which are highly active enzyme inhibitors (Wint, 1979, 1982). Simultaneous studies on the foliage of Erica cinerea also showed very high levels of inhibition of enzyme activity (A. Power, personal communication; McNeill & Prestidge, ,1982). Figure 3.9 : Enzyme inhibition activity in gorse foliage. 76.
JUN »i »
• without extract
x with gorse extract
• with oak extract
37.5 50 150 -1 [Enzyme] X 15 3.5 Discussion
Published information concerning the chemical composition of Ulex foliage proved highly inadequate for the purposes of this study. Although useful in identifying the actual constituents of gorse foliage in many cases, information regarding seasonal variation of the chemical components was unreliable either because the sampling dates were not recorded, or because the plant part sampled was not identified in sufficient detail. In this section it has therefore been necessary to re-examine the seasonal % variation of the chemical constitutents of gorse foliage. In some cases, e.g. nitrogen content, this has been achieved in depth, but for many chemical groups, these results can only be regarded as a preliminary examination of seasonal trends.
Gorse foliage contained a relatively high concentration of nitrogenous compounds for only 10% of the year, but for the remainder of the year levels were low compared with the nitrogen content of other angiosperms
(Scriber & Slansky, 1981; Mattson, 1980). In addition, Ulex spp are capable of fixing nitrogen, an ability which usually compensates for low foliage nitrogen content (e.g. in broom, J. Riggall, personal communication).
For this reason, the pattern of nitrogen use in gorse foliage is rather unusual. Southwood (1972) pointed out that artificial diets for phyto- phagous insects usually contain 25-40% protein. Mattson (1980) suggested that phytophagous species need at least 1% nitrogen in their diet in order to grow. It seems likely therefore that the nitrogen content of gorse foliage for 90% of the year (1.8% nitrogen, or 11.3% protein) is sub- optimal for phytophagous insects (see also Section 7).
Similar patterns of stable host-plant food quality decline have been demonstrated in several tree species (Wint, 1979) in oak (Feeny, 1970) and in bracken by Lawton (1976). The most detailed information regarding such patterns comes from studies of insects in acid grasslands (McNeill, 1973;
Hill, 1976; Prestidge, 1980; McNeill & Prestidge, 1982).
In these grasslands, very high levels of soluble nitrogen in spring are
followed by generally lower food quality through summer, with smaller peaks of concentration due to floristic events, such as flowering, later in the year. All of these studies confirm the pattern observed in gorse,
that food quality is highest in spring and generally declines in summer.
These studies also consider the impact of such changes on the performance of phytophagous insects, and are discussed again in Section 5.
McNeill & Southwood (1978) suggested that insects are rarely limited by an absolute shortage of either energy content or carbohydrate content in their food. This is almost certainly true of Utex europaeus, where levels of both were relatively constant and relatively high throughout the year.
No cyanogenic compounds were discovered in gorse foliage. Only one unusual amino acid, L - Dopa, was found and then only in trace amounts.
The absence of both groups of chemicals is not unusual, despite the fact that they are widespread amongst other species of the Leguminosae.
Amylase was not inhibited by aqueous extracts of gorse foliage, which suggrrts that this foliage contains little or no phenolic compounds, or that phenolic compounds present in gorse foliage do not complex amylase.
T he biological activity of phenolic compounds in vitro is now very well known (Feeny, 1969; Harborne, 1978; Swain, 1979; Bernays, 1981), though there is some controversy regarding the effect of foliage tannin on the performance of insect herbivores (e.g. Feeny, 1970; Fox & Macauley,
1977; Bernays, 1981). The relationship between phytophage and host plant tannin content varies greatly from species to species and on the type of tannin material present. Tannins can be phagostimulants (Bernays, 1981) / 79.
feeding deterrents (Rhoades, 1977), adversely affect feeding efficiency
(Feeny, 1970), improve feeding efficiency (Bernays, 1981) or can be
apparently neutral in their effects, even at high concentrations (Fox &
Macauley, 1977). This diversity of effects has led Bernays (1981) to urge
caution in negatively correlating tannin content with phytophage performance
in an ecological context (e.g. Lawton, 1976; Wint, 1982; Feeny, 1970),
though there is no doubt that they are of considerable importance in one way or another.
The role of alkaloids and isoflavones in gorse foliage is far from
clear. Both types of chemical appeared in very high concentration in vegetative buds and in old gorse foliage very early in spring. These
levels declined extremely rapidly and were very low throughout late spring and summer. The concentration of isoflavones rose again in late autumn.
The toxic nature of alkaloids is well known, and their role in the protection of plant tissue against herbivore attack is well established
(Levin, 1976; Waller & Nowacki, 1978; Robinson, 1979). High alkaloid c. orient rat ions in vegetative buds of gorse may protect these structures
from attack by generalist insects, but the fact that levels of alkaloid concentration are low during the remaining period of greatest phytophagous insect activity suggests that this is not the case. Such a role can be ascribed to alkaloids in broom foliage, but here levels are much higher, and more stable through the year (J. Riggall, personal communication).
White (1943), Faugeras et al (1962) and Smith (1966) have all recorded mobility of alkaloids in vegetative parts of various members of the
Genisteae during accumulation of high alkaloid levels in seeds. Coincidence of peak alkaloid concentrations in vegetative parts of gorse with the period of seed-filling reinforce this opinion (see Section 2).
Isoflavones are biologically active substances, and their anti- herbivore capabilities are well known. All isoflavones are estrogenic when given to mammals by parenteral injection, and high concentrations (up to
5%) of genistein in leguminous fodder plants can pose agricultural problems when ingested by stock (Harborne, 1979). The concentrations of genistein and 5-methyl geriistein in gorse foliage during very early spring, and in autumn were very high (J.B. Harborne, personal communication), but it is difficult to ascribe an antiherbivore function to them since they also declined to low levels during the period of greatest insect activity. High concentrations in foliage coincided with the end of flowering in spring and the formation of new flower buds in autumn.
The role of isoflavones in gorse foliage may therefore resemble that of alkaloids. Isoflavone concentrations were not measured in the winter months, nor in any other plant structures. Isoflavones have high enzyme- binding activity. Lack of inhibition of amylase by gorse foliage extract suggests that have little effect on insect feeding efficiency during the sunnier months.
Jobson & Thomas (1964) recorded a seasonal mean foliage silica content of J.31% of dry matter. They compared this with the silica content of i^e-fure at 2.79%. The content of new foliage determined in this study was approximately 0.5%. At these levels, it is unlikely that silica affects gorse phytophages in any way.
Another major group of secondary compounds, Phytohaemagglutiriin or phytolectin, is known to occur in gorse, but has not been measured in the course of this study. The role of phytolectins in plants is obscure, but they can make up between 2 and 10% of plant proteins (Liener, 1979).
Their role as antiherbivore chemicals has been suggested by Janzen et al
(1976) who showed that the lectin of Phaseolus Vulgaris seeds was toxic to Callosobruchus maculatus. Two phytohaemagglutinins have been .isolated in large amounts from seeds of Ulex europaeus (see Liener, 1979, for
references), and are used as blood-typing reagents. Though mostly found
in seeds, Lalaurie et al (1966) have shown that agglutinins can also occur
in what they called "spines and secondary stems" of gorse. As with many
such studies no seasonal variation was measured, though the term secondary
stems suggests that levels were higher in old foliage. These compounds may influence the performance and seasonality of phytophagous insects on gorse, and will be studied more closely in the future.
% The secondary compounds measured in this study and discussed here, all have well-recorded anti-herbivore activities in other plants, and in various plant structures. With the possible exception of foliage alkaloid content none of these compounds occur in sufficient quantity to be regarded as effective anti-herbivore compounds at any time of the year. Rhoades'
(1979) "optimal defense theory" proposes, amongst other things, that plant defenses against herbivores are allocated in direct proportion to the risk of the particular tissue, and the value of the tissue. In this sense, buds and young shoots of gorse which are attractive to herbivores becaubw of high nitrogen content would appear to be at high risk. It seems therefore, that the foliage of Ulex spp is not protected from ; herbivore attack by secondary plant substances in the sense of Rhoades
(1979).
Further discussion of the role of secondary plant substances can be found in Section 5.
3.6 Summary
1. Total and soluble nitrogen content of foliage was relatively high (25%
protein) for 10% of the year, but very low thereafter. The stable low
level of 11.3% protein is almost certainly sub-optimal for insect growth
and development. 82.
2. Total calorific value of foliage was almost constant throughout the
season at 25.4 KJ/g dry weight.
3. Though slightly higher in spring, levels of soluble carbohydrate in
gorse foliage were almost constant through the growing season at a
level unlikely to hinder insect development.
4. Gorse foliage contained only two alkaloids, sparteine and N methyl-
cytisine or anagyrine. Levels were high in very early spring, but
declined to a low level by late spring. High levels in spring may be
related to seed production.
5. Gorse foliage contained 2 isoflavones, genistein and 5^methyl genistein.
Total isoflavone content was high in vegetative buds, but fell to a
low level over summer. Levels rose again in autumn. The role of
isoflavones in gorse ecology is unknown.
6. Silica content appeared to rise late in the season, but too few
analyses were carried out to confirm this. Generally, levels were
lower than those associated with anti-herbivore activity.
7. L - Dopa was the only unusual amino acid identified in gorse foliage,
and was found only in trace quantities.
8. No cyanogenesis was ever shown in gorse foliage.
Gorse foliage showed very little enzyme inhibitory activity at any time
of the year. This suggests that phenolic compounds such as tannins
and flavenoids were present in only very low concentrations in the
summer.
10. Despite the fact that in early spring foliage was succulent, highly 83. nutritious, and therefore susceptible to insect attack, there was no evidence of protection by antiherbivore substances with the possible exception of alkaloids. Concentrations of secondary chemicals
remained low throughout the active feeding period of phytophagous
insects. SECTION 4
THE PHYTOPHAGOUS INSECT FAUNA OF GORSE
4.1 Introduction
Attempts to assemble a faunal list for Ulex spp began in the 1920's when Chater (1931) and Davies (1928) both undertook studies to identify potential control agents for Ulex europaeus, a serious weed in many temperate parts of the world (Gaynor & MacCarter, 1981). A similar invest- igation in the early 1960's led to a review of the available continental
literature, and extensive collecting in Western Europe (Zwolfer, 1963;
Schroder & Zwolfer, 1970). This study has formed the basis for subsequent work. Apart from these 3 studies, no concerted attempt has been made to determine the extent of the gorse fauna in Britain or in Europe.
In addition to the continental literature which was well reviewed by
Zwolfer (1963) and Schroder & Zwolfer (1970), there are numerous works which provide information about the insects attacking gorse in Britain.
The faunal lists presented and discussed in this section are derived from the sources listed in Table 4.1.
In addition to the standard literature, the faunal lists discussed here also include personal records of insects associated with gorse which were obtained from systematic sampling of the gorse fauna at two sites in
Southern England between 1979 and 1981. Descriptions of the sampling areas can be found in Section 2.2, and sampling procedures are described below.
The degree of specialism or generalism in feeding habits amongst the members of the gorse fauna is examined in this section, and compared with recent studies by Lawton & Schroder (1977) and McNeill & Prestidge (1982).
The faunas of the British members of the tribe Genisteae feature quite prominently in the entomological literature. In particular, the fauna of 85.
Table 4.1 : Sources of information concerning the insect fauna of gorse in
Britain.
General IMMS, A.D. 1977. General Textbook of Entomology. (2 vols)
Chapman & Hall, London.
KLOET, G.S. & W.D. Hincks 1945. A Check List of British
Insects. 483 pp.
Coleoptera FOWLER, W.W. 1887-1913. The Coleoptera of the British
Islands. (5 vols) London.
FREUDE, H. ; HARDE, K.W. & G.A. LOHSE 1979. Die Kafer
Mitteleuropeaus. Goecke & Evers, Krefeld.
Band 4 Staphylinidae. 263 pp.
Band 6 Diversicornia. 367 pp.
Band 7 Clavicornia. 310 pp.
HOFFMAN, A. 1950, 1954, 1958. Coleopteres - Curculionides.
(3 vols) Faune de France No. 52. Paul Lechevalier,
Paris.
JOY, N.H. 1932. A Practical Handbook of British Beetles.
(2 vols) Witherby.
SCHERF, H. 1964. Die Entwicklungsstadien der mitteleurop-
aischen Curculioniden (Morphologie Bionomie^ Okologie). 3
Abhandlungen Der Senckenbergischen Naturforschenden
Gesellschaft 506^: 1-335.
WALSH, G.B. & J.R. DIBB (Eds) 1954. A Coleopterists Hand-
book. Amateur Entomologists Society.
Diptera BARNES, H.F. 1946. Gall Midges of Economic Importance.
(Vol. II) London. 86.
Table 4.1 : Continued.
Heteroptera BUTLER, E.A. 1923. Biology of the British Eemiptera:
Eeteroptera. H.F. & G. Witherby, London. 682 pp.
SOUTHWOOD, T.R.E. & D. LEST ON 1959. Land and Water Bugs
of the British Isles. Warne & Co., London.
Homoptera DAVIDSON, J. 1925. A List of British Aphids. Longmans,
London.
NEWSTEAD, R. 1901. Monograph of the Coocidae of the
British Isles. (2 vols) Royal Society.
Lepidoptera CARTER, D.J. 1981. The Observers Book of Caterpillars.
Frederick Warne & Co., London.
EMMETT, A.M. (Ed) 1979. A Field Guide to the Smaller
British Lepidoptera. British Entomological and
Natural History Society, London. 271 pp.
SOUTH, R. 1906. Butterflies of the British Isles. Warne,
London.
SOUTH, R. 1961. The Moths of the British Isles. (2 vols)
Warne, Lond on.
STOKOE, W.J. 1944. The Caterpillars of British Butterflies.
Warne, London.
STOKOE, W.J. 1948. The Caterpillars of British Moths.
(2 vols) Warne, London.
Orthoptera RAGGE, D. 1965. Gras shoppers> Crickets, and Cockroaches of
the British Isles. Warne, London 87.
Table 4.1 : Continued.
Thysanoptera MORISON, G.D. 1949. Thysanoptera of the London Area.
London Naturalist, reprint 59.
MOUND, L.A.; MORISON, G.D.; PITKIN, B.R. & J.M. PALMER
1976. Handbook for the Identification of British
Insects. Vol. 1. part 11 : 1-79. Thysanoptera. Cytisus scoparius in the south of England is extremely well known (e.g.
Waloff, 1968). The composition of the fauna of 2 gorse species is compared and contrasted with that of 3 other closely related leguminous shrubs.
Greatest emphasis in this section, however, is placed on analysis of
the seasonal occurrence and abundance of each of the phytophagous insect
species which use gorse as a host-plant. Quantitative estimates of the
fauna were obtained using the sampling methods discussed in Section A.2.
Relationships between the occurrence of phytophagous insects and the
% developmental patterns of their host-plant are discussed, but more detailed consideration of these interactions can be found in Section 5.
Emphasis has been given to a description of the fauna which attacks gorse foliage, and particularly those species which complete the whole of their development on gorse foliage. Rather less consideration has been given to species inhabiting reproductive organs and gorse roots. Predatory insect species have been listed but the influence of predators on the structure of the phytophagous insect fauna of gorse is discussed in detail in Section 5.
4.2 Sampling Methods
Preliminary sampling in autumn 1978 showed that all gorse insects were mature by September, and that the abundance of all species was very low.
Samples were therefore taken between April and early September in 1979,
1980 and 1981.
Sampling sites chosen have been described in Section 2.2. Insect samples were taken at approximately weekly intervals. Five techniques for the quantitative estimation of the foliage-dwelling insect fauna were tested. Sweep nets could not be used because of the thorny nature of Utex spp. A Dempster box (Dempster, 1961) used with a pyrethroid insecticide gave high accuracy, but the method was extremely time-consuming and only small amounts of foliage could be sampled on each occasion. Bibby (1977) cut and examined whole shoots to assess insect numbers, but this was also too time-consuming because of the large number of shoots required to obtain sufficient insects for quantitative analysis. Bibby (1977) and
P. Hopkins (personal communication) both rejected suction sampling as a reliable technique and so it was not considered for this study. The most reliable method for obtaining repeatable sampling data was found to be beating. For each sample, a known quantity of gorse foliage was beaten heavily with a stick, and the insects dislodged were collected on a white
2 calico beating tray (0.85 m ) held beneath. Insects were either collected for later study or were counted in the field.
The foliage to be sampled was chosen at arms length from a random co- ordinate within the sample site (see Section 2.2). The sample sizes were
200 g wet weight of foliage for Ulex europaeus, and 100 g wet weight of foliage for Ulex minor, and in both cases occupied approximately 1 cubic foot of naturally occurring green foliage. The samples could be estimated visually with an accuracy of approximately 90%, and this estimate was checked regularly. Results from U. minor were doubled for ease of comparison.
Until mid-July in each year, green gorse foliage comprised mature growth from the previous growing season as well as new growth. Insect samples were therefore taken from both types of foliage combined, and it was not possible to distinguish which type of foliage each insect species used. After senescence of older foliage, all insects were sampled from new foliage (see Section 2.A.2).
The seasonal variation in the efficiency with which this method sampled the insect fauna was determined. After the sampling procedure was carried out, the foliage from which insects had been dislodged was cut into bags, returned to the laboratory, and carefully examined for remaining insects. The efficiency with which different stages of each insect species
(and spiders) was collected was determined, and sampling results were
corrected accordingly. Most groups such as beetles and spiders were
consistently sampled with 100% accuracy, while others, such as heteropteran
nymphs, were not.
The sampling programme carried out in 1979 was used largely to
identify the fauna and to develop sampling procedures, since nothing was
previously known about the relative abundance of the insect species on % gorse. The size and number of samples was therefore not consistent
through the season, and so confidence intervals have not been provided for
abundance estimates in 1979. In 1980 and 1981, 15 equivalent samples were
taken on each sampling occasion. Preliminary studies in 1979 suggested
that 15 samples contained representatives of over 90% of the phytophagous
insect species present.
The method described above did not accurately sample sedentary foliage-
feeding insects such as scale insects and gall-forming species, or those
.speri.feeding amongst the reproductive parts of gorse. During 1979,
weekly samples of 45 whole shoots were taken using the method described in
Section 2. Though species such as Phanococcus aceris (Homoptera: Pseudo-
coccidae), Apion souteVlare (Curculionidae: Apioninae) and Dasyneura sp
(Diptera: Cecidomyidae) (as larvae in galls) had been recorded in both
sai^p? ""ng areas, they were so rare that even samples of this size failed to
yiel^ 'neasurable levels of abundance. This sampling method was therefore
discontinued.
Species feeding in the reproductive parts of gorse were sampled in
late spring and summer 1979. In 1980 buds and flowers of Ulex europaeus
were sampled in late winter and early spring only, to cover gaps in know-
ledge from the previous year. All buds, flowers and pods were opened and infestations were recorded as percentages. The fauna associated with gorse
reproductive parts is listed in Table 4.2. The insect fauna attacking U. minor reproductives was not sampled.
The fauna feeding on roots was not sampled though the literature record
is summarised in Table 4.2. Imagines of root-feeding species were recorded
regularly, and are considered along with foliage-feeding species.
Data storage and manipulation was carried out using the package SIR
(Scientific Information Retrieval) available at the Imperial College
% computer centre. This package enabled storage of data concerning insect abundance and biology in a heirarchical fashion and hence selective data retrieval could be carried out according to specified criteria (e.g.
feeding site and insect family). The abundance data obtained was often non-normal, but normalised by application of a log (abundance + 1) trans- formation. Comparisons of insect abundance between sites, and between host-plants were made using the two-way analysis of variance programme of
the GENSTAT statistical package. Comparisons of insect abundance between y^a.rs were not made. Bars on figures represent standard errors. Time axes on figures show initials for month of the year, and smaller divisions represent day of year (see Appendix VIII).
4.3 The Fauna of Gorse Roots
A list of the species recorded feeding on the roots of Ulex spp in previous studies can be seen in Table 4.2. Zwolfer (1963) found records of
8 species feeding in roots in Europe, and 6 of these have been recorded in
Britain. No direct estimates of the gorse root fauna were made in the present study, though adults of only 4 species were collected in foliage.
Cydia lathyrana (Hb.) was not collected in this study, but is distributed very locally in Southern England. Zwolfer (1963) recorded this species as a root-feeder, but more recently Emmet (1979) has suggested that 92.
Table 4.2 : Feeding sites of arthropod species attacking gorse in Europe (European records from Zwolfer, 1964; British
records from Zwolfer, the present study; and sources listed in Table 4.1).
Plant part Family Continental Europe Britain Present study attacked Roots Coleoptera Cerambycidae Chlorophorua trifaaoiatua Curculionidae Polydruaus oonfluena Sitona erinaoeus S. regensteinensia tibialis Stropho8omus melanogrammus Scolytidae Hylaatinus obscurua Lepidoptera Tortricidae Cydia lathyrana Stems and Coleoptera Anobiidae Gastrallus sp wood Bupestridae Acmaeodera adspersula Anthaxia funerula Cerambycidae Chlorophorus trifasciatus Deilus fugax Scolytidae Hylastinu8 obscurus Phloeophthorus rhododaatylis Lepidoptera Gracillariidae Lithocolletis ulioiaolella Shoots and Coleoptera Chrysomelidae Chrysolina americana shoot tips Luperus circumfusus x Luperua longicornis / * Phytodeata olivacea P. variabilis x Coccinellidae / Subcooainella 24-punctata • Curculionidae Apion sautellare • Hypera venusta • x Peritelus 8 en ex X x P. prolixua X X Pleurodirua aquisextanus X X Polydru8ue aonfluena / • Sitona erinaoeus X X x S. lateralis • * S. regenateinenaia • • S. tibialis • / Diptera Agromyzidae Agromyza sp. X Cecidomyidae x x Da8yneura sp Heteroptera Miridae Aaciodema obaoletum / / Pachylop8 tricolor • / Pentatomidae Piezodoru8 lituratus • • Tingidae x Diotyonota strichnocera • Homoptera Aphididae Aphis ulicis x x Euceraphis punctipermis Membracidae Centrotus cornutus / Gargara genistae / Pseudococcidae Icerya purohasi / x Phanococcus aceris Psyllidae Arytaina genistae • Lepidoptera Gelechiidae Anar8ia spartiella • Geometridae CheaiaB rufata • x Ematurga atomaria Is turgia limbaria / x Ortholitha luridata Operophtera brumata / Ortholitha mucronata / x Peribatodes rhomboidaria Pseudoterpna pruinata / Sootopteryx peribolata Lasiocampidae Malaco8oma neustria / 93.
Table 4.2 : Continued.
Plant part attacked Family Continental Europe Britain Present study • Callophrys rubi Lycaenidae Lyaaena aegon / L. argiades • L. argiohiB L. boetiouB • x ? L. telicanus • Lymantriidae Euproctis chrysorrhoea Noctuidae Antitype argillaceago / chi x Ceramica pisi Heliothia peltigera • Oecophoridae Agonopterix ulioetella / Pyralidae Meoyna polygonalis x Nephoteryx genistella / Fcythrididae Scythris gallicella S. grandipennia Tortricidae Archip8 xyloateona Bat odea anguatorianu8 Tortrix pronubana Orthoptera Tettigoniidae • ? Leptophyea punctatissima Thysanoptera Thripoidea / ? Sericothrip8 staphylinus Acari Eriophyidae* Aceria genistae Tetranychidae Tetranychu8 lintearius / • Buds Diptera Cecidomyidae Asphondylia uliois Lepidoptera Gelechiidae Mirificarma mulinella / Oecophoridae Agonopterix nervosa / • ? Flowers Coleoptera Cryptophagidae Corticaria crenulata / ? C. serrata / ? Micrambe vini Curculionidae Apicm striatum / Staphylinidae Philorinum sordidum / Gelechiidae Agonopterix nervosa • Anarsia spartiella / Mirificarma mulinella / Geometridae Gymnoscelis rufifasciata / Thysanoptera Thripoidea Odontotkrips ulicis • Thripa flavua / Pr s Coleoptera Curculionidae Apian difficile A. lemovicinum A. paeudogallaecianum A. squamigerum A. uliciperda A. ulicie Bruchidae Bruchidiua lividimanue Bruchus affinis Callosobruchua Lepidoptera Coleophoridae Coleophora albicoeta Tortricidae Cydia internana C. succedana
* denotes species regarded as incidental record it feeds in flower buds of Genista spp, overwintering in a cocoon near the
roots. Strophosomus melanogrammus Forst. was collected occasionally. Its
close association with Ulex spp has not been demonstrated, though it is a
very polyphagous species as an adult and as a larva (Scherf, 1964).
Zwolfer (1963) recorded it damaging gorse foliage in Southern France.
Polydrusus confluens Steph. has been recorded attacking the roots of
broom, Cytisus sooparius, and larvae presumably feed freely on the
roots of other species in the tribe Genisteae since imagines are common
on all such species (Hoffman, 1958). Imagines were collected commonly in
gorse foliage, and their seasonal distribution in Ulex europaeus and Ulex minor for 1980 and 1981 is shown in Figure 4.1.
The pattern of abundance for adults of this species was extremely
variable between years, sites and hosts. Peak populations appear in late
June, which concurs with the records of Scherf (1964). More adults were
collected in Ulex minor foliage than in Ulex europaeus foliage in 1979 and
1980, while the numbers collected at WGP (where U. minor was absent) were
CALtClUC ly low. This may reflect an adult preference for low-growing plants or may reflect a true preference for U. minor.
Sitona regensteinensis Herbst has been recorded feeding in the roots of several plant species belonging to the tribe Genisteae and is particularly
common on broom (Zwolfer, 1963; Dantharayana, 1969). Adult weevils over- wintei^i, laid eggs in early spring, and declined in number through June.
Larvae developed in the roots and nodules of the host plant, emerging to
overwinter in October. The abundance of S. regensteinensis adults was low in comparison to S. tibialis Herbst., though it appears that peak pop- ulations were not sampled (Figures 4.2 and 4.3). The decline in adult numbers occurred much earlier on gorse than recorded on broom, which may have been the result of increased mortality, migration (Dantharayana, Figure 4.1 : Seasonal variation in the abundance of Polydrusus confluens
Steph. adults on U. europaeus and U. minor. 95.
WGP
• 1979
x 1980
0.2
•f-
M Figure 4.2 : Seasonal variation in the abundance of Sitona regensteinensis
Herbst adults on Ulex europaeus.
• • Yateley Common U. europaeus 1980
x x Yateley Common U. europaeus 1981
A A Windsor Great Park U. europaeus 1980
Figure 4.3 : Seasonal variation in the abundance of Sitona tibialis Herbst
adults on Ulex europaeus and Utex minor.
• • Yateley Common U. europaeus 1980
x x Yateley Common U. eviropaues 1981
A A Windsor Great Park U. europaeus 1980
A A Yateley Common U. minor 1980 96.
insects
A M J J A 1970), or simply low reproductive success 011 Ulex spp.
The most abundant root-feeding weevil collected in gorse was S.
tibialis. Adults of this species emerged from the ground in spring and
summer, and larvae fed in the roots of gorse in autumn and winter (Freude
et al., 1979).
There was no significant difference between the numbers of adult weevils collected in Ulex europaeus as compared to Ulex minor (Table 4.3),
though the unusual alternating pattern of abundance shown in Figure 4.3 may
represent movement between low Ulex minor and taller Ulex europaeus
according to weather conditions, particularly temperature. Such vertical movements have been recorded for Sitona regensteinensis on broom (Danth-
arayana, 1970). The abundance of weevils at YC was generally lower in 1980
than in 1981. S. tibialis was extremely rare at WGP in 1980, and as with
P. confluens, this difference may reflect a preference for younger gorse or
for Ulex minor, which was absent from WGP. Such large differences in
relative abundance were not observed in S. regensteinensis.
It was difficult to infer the importance of either species as a
component of the gorse fauna from consideration of adult biology alone,
and it was not possible to investigate their larval biology on Ulex species.
The relevance of the adult populations to the structure of the gorse phyto-
phagous fauna is discussed later.
4.4 The Fauna of Reproductive Structures
Table 4.2 gives a list of the insect species collected from buds,
flowers, and pods of Ulex europaeus from 1979 and 1980. The reproductives 98.
Table 4.3 : Differences in the abundance of insects on Ulex europaeus and
U. minor, 1980 (expressed as log (abundance + 1), analysis by
two way ANOVA).
Grand mean Grand mean F DF P Species Ulex europaeus Ulex minor
Sitona regensteinensis 0.18 0.09 5.1 1; 308 <0.05
S. tibialis 0.58 0.62 0.3 1; 308 NS
Asciodema obsoletim 0.74 0.43 14.0 1; 224 < 0-.01
Pachylops bicolor 1.19 0.99 2.9 1; 168 NS
Dictyonota striohnocera 1.26 1.24 0.04 1; 180 NS
- Piezodorus lituratus - - - -
Agonopterix ulicetella 0.20 0.13 2.6 1; 124 NS
Sericothrips staphylinus 2.40 2.42 0.02 1; 280 NS 99.
Table 4.4 : Differences in the abundance of insects on Ulex europaeus at
Yateley Common and Windsor Great Park, 1980 (expressed as log
(abundance + 1), analysis by two-way ANOVA).
Grand mean Grand mean
Sitona regensteinensis
S. tibialis 0.66 0.03 113.9 1; 252 < 0. 001
Asoiodema obsoletum 0.70 0.30 23.0 1; 224 < 0. 001
Paohylops bicolor 1.04 0.76 5.3 1; 140 < 0. 05
Dictyonota strichnooera 1.34 1.15 4.3 1; 224 < 0. 05
Piezodorus lituratus
Agonopterix ulicetella
Sericothrips stccphylinus 100.
of Ulex minor and Ulex gallii were not examined closely, but both species provide host material for a second generation in late summer and autumr^ of species which attack U. europaeus in spring. 16 species of insect were collected from Ulex europaeus though some were extremely rare, or of doubt- ful association. Asphondylia ulicis Ver., while locally abundant in
Southern England, was only observed once in samples taken between 1979-1981 at YC. Corticaria crenulata (Gyllenhal) and Corticaria serrata (Paykull) were both collected frequently as adults, but since they are both normally associated with compost and wrack, they were probably detritivorous on senescent petals. Similarly, the role of the common cryptophagid Micrambe vini (Panzer) in flowers was never determined. Thrips flavus was only recorded in extremely low numbers in comparison with Odontothrips ulicis which was very abundant. The role of Philorinum sordidum (Stephens) in gorse flowers was far from clear. It was often encountered as an adult, but whether predatory on thrips or feeding on gorse pollen was not deter- mined. Gymnoscelis rufifasciata is a polyphagous, multivoltine, flower- feeding geometrid, which was encountered on a number of occasions.
Coleophora albicosta Hw. was present at both Yateley Common and Windsor
Great Park, but was never common enough to appear in the samples of gorse flowers and pods taken in spring.
Apart from recording these relatively rare species, the abundance of a number of true gorse insects feeding in reproductive parts was measured.
In Table 4.5 the infestation of Ulex europaeus reproductives by a number of insect species is summarised. Sampling was first carried out at WGP in late spring 1979, but additional information was obtained in 1980 to reinforce this data. At Yateley Common, sampling was carried out over 3 seasons to provide a fuller description of the flower fauna.
Mirificarma mulinella (Z.) only rarely attacked U. europaeus buds at Table 4.5 : Infestation of reproductive structures of Ulex europaeus in spring and summer (* = species present).
Site : Windsor Great Park
Meail % of r<'product ^ res as No. of No. of Mirificarma Anarsia Agonopterix Odontothrips Micrambe Apion Cydia Apion Philorinum Date reproductives samples Immature Mature mulinella spartiella nervosa ulicis vini striatum spp ulicis sordidum collected Buds Flowers pods pods
18 Mar. 80 15 1530 91.4 7.8 0.8 0 * 0 0 * * 0 0 0 0
11 Apr. 80 15 920 82.9 15.6 1.5 0 0 0 0 0.6 0 0 0 0 0
3 May 80 4 513 51.1 25.6 23.2 0 0 0 0 0 0 0.4 0.2 0
31 May 79 7 279 14.3 23.7 60.9 0 0 0.03 0.06 7.9 7.5 2.2 0.03 2.2 0.03
12 June 79 10 209 1.0 21.1 54.0 23.9 1.5 0 4.3 28.2 13.4 0.5 4.8 18.7 0
25 June 79 8 128 0 0 22.6 77.3 0 0 0.08 3.9 4.9 0 23.4 45.3 0
6 July 79 8 139 0 0 13.7 86.3 0 0 0 3.6 1.4 0 25.9 33.1 0
20 July 79 10 131 0 0 0 100 0 0 0 0 0.7 0 5.3 30.5 0 Table 4.5 : Continued.
Site : Yateley Common
Meaii % of r<;producti >/es as No. of No. of Mirificarma Anarsia Agonopterix Odontothrips Micrambe Apion Apion Date reproductives Cydia Philorinum samples Immature Mature Mulinella spartiella nervosa ulicis , vini striatum spp ulicis sordidum collected Buds Flowers pods pods
2 Apr. 80 14 982 92.2 4.5 3.4 0 * 0 0 * 0 0 0 0 0
* 0 * 3 Apr. 81 - - 92.6 7.4 0 0 0 0 0 O 0 0
23 Apr. 80 5 186 31.2 59.1 9.7 0 0.5 1.6 0.5 22.0 0.5 0 0 0 0
1 June 79 2 44 15.9 59.1 25.0 0 0 0 0 15.9 11.4 0 0 2.3 0
18 June 80 5 84 0 0 28.5 71.4 1.2 0 4.8 3.6 2.4 0 27.4 64.3 0
28 June 80 5 26 0 0 0 100 0 0 0 0 0 0 34.6 57.6 0
9 July 79 3 17 0 0 0 100 0 0 0 0 0 0 41.1 35.3 0
23 July 79 5 12 0 0 0 100 0 0 0 0 0 0 16.7 16.7 0
Flowers 20 Mar. 81 239 0.9 0 0 6.7 0 0 0 0 0 only
15 Apr. 81 it 224 1.0 0 0 4.7 .2-5 0.7 0 0 0 it 13 May 81 161 0 1.2 1.2 12.4 1.2 3.1 0 0 0 it 21 May 81 160 0 0.6 1.9 29.5 2.5 2.5 0 0 0
1 June 81 " 200 0 0 0.5 7.0 3.5 2.0 0 0 0 103.
both Yateley Common and WGP. It occurred during April, May and the first half of June, the spring period during which buds were present on gorse
(see Figure 2.2). Bibby (1977) found that M. mulinella was abundant in gorse buds in Dorset, and provided a significant early spring food supply for Dartford Warbler, Sylvia undata.
The flower-feeding gelechiid species Anarsia spartiella Schr. was collected during May, June and early July. This species was mainly found feeding in flowers, though it completed its development feeding on new gorse foliage. Both Chater (1931) and Emmet (1979) recorded it feeding solely on new shoots of gorse. Its seasonal abundance in samples beaten from gorse is shown in Figure 4.4.
By contrast, Figure 4.4 also shows the seasonal abundance of the commonest flower-feeding lepidopteran, Agonopterix nervosa Hw. Peak pop- ulations coincided with peak flower production (Figure 2.2), though pop- ulations appeared to develop a little late in 1980. In both years develop- ment was complete by mid-June when flowering ceased. There was no signi- ficant difference between the abundance of Agonopterix nervosa in the treated and untreated areas at YC in 1981 (see Section 6 for details).
The commonest species encountered in flowers was the host-specific thysanopteran Odontothrips ulicis. Peak abundance of this species was also highly coincident with peak flower production (Table 4.5). Mound et al
(1976) recorded that 0. ulicis bred in the months of May to July in gorse flowers.
During 1979, random samples of gorse seed pods were taken at both YC and WGP at 7-10 day intervals, returned to the laboratory and dissected to determine percentage infestation by insects.
Three species were encountered, Apion ulicis Forst., and two olethreutid species, Cydia succedana (Schiff.) and C. internana (Gue.). Larvae of the Figure 4.4 : Seasonal variation in abundance of Agonopterix nervosa
and Anopsia spartieZla in samples beaten from gorse.
• • Yateley Common 1980
x x Yateley Common 1981
a a Windsor Great Park 1980 104.
insects per sample
1.0 A. spartiella
0.5
« x
i
M lepidopteran species could not be distinguished and the results presented
here combine both species.
Abundance of both Apion ulicis and Cydia spp was lower in WGP than
YC. Up to 18.5% of pods contained both Cydia spp and Apion ulicis larvae,
though the competitive or predatory interactions between them were not measured. Cydia larvae consumed the contents of more than one pod in the
course of their development, and the pods used could be identified by the
characteristic exit hole. By late July just before pods dehisced, Cydia,
or Cydia and Apion together, had destroyed 66.7% of all pods formed at YC
(Figure 4.5). Abundance of Apion ulicis larvae reached a peak in mid-June
when 64.3% of pods contained larvae (Figure 4.5).
As with the flower fauna, the occurrence of insects in pods was
strictly co-ordinated with host-plant phenology. In 1979 50% of gorse
reproductives were pods by approximately day 168 at WGP and approximately
day 164 at YC. The peak infestation by Apion ulicis measured in 1979
occurred within 8 days of this point at WGP, within 5 days at YC. The
same pattern was probably true of Cydia succedana though this pattern was
obscured by inability to distinguish the Cydia spp. Infestation by Cydia
intemana occurs from early July (Emmet, 1979), and the skewness in Figure
4.5c probably reflects later invasion by this species.
Adult Apion ulicis were common on gorse foliage throughout each year
of this study. They appeared to feed only lightly on flowers in spring,
and did not appear to feed on gorse foliage at all.
4.5 The Fauna Attacking Gorse Foliage
Apart from the weevils, some of which have been considered in Section
4.3, the dominant phytophagous species which occurred on gorse foliage were
various Heteroptera, particularly Dictyonota strichnocera Fieb., Asciodema
obsoletum Pachylops bicolor and Piezodorus lituratus L. A list of all 3 Figure 4,5 : Infestation of Ulex europaeus pods.
x x Yateley Common 1979
• • Windsor Great Park 1979
A. % of pods containing Apion ulicis and Cydia spp.
B. % of pods containing Apion ulicis.
C. % of pods containing Cydia spp, and total pod destruction
by Cydia spp (dotted line).
107.
folivorous species attacking gorse in Britain is shown in Table 4.2.
Of the species recorded attacking gorse bark or wood, only Phloeoph- thorus rhododaotylis Marsh was beaten from gorse in this study. No attempt was made to specifically sample the fauna attacking woody stems. Adult P. rhododactylis were collected on 9 occasions at both YC and WGP.
46 British species have been recorded attacking the green foliage of gorse, though a number of these records are almost certainly spurious. 25 species were recorded in the present study, but again, some of those were incidental records of little ecological significance, and have been marked as such in Table 4.2. Many species were very rare or local, and though recorded' from the study areas were not encountered in samples beaten from gorse foliage. Attempts to assess their abundance by other means also failed (see Section 4.2). The seasonal variation in abundance of 13 folivorous species is presented here, and in Table 4.6, the relative importance of these species compared to the remainder of the fauna collected is given.
The seasonal abundance of Sitona tibialis; S. regensteinensis 3
Strop!Hj&ormis melanogrammus and Polydrusus confluens adults has been discussed in Section 4.3. Zwolfer (1963) recorded S. melanograrmrus adults damagiz-g gorse foliage in France, but recorded no noticeable damage from
Sitona adults. The feeding ecology of adult weevils in gorse is very obscure. On several occasions damage to spines and buds was observed which could possibly be attributed to weevil adults, but in general neither
Sitona spp nor Polydrusus confluens adults caused visible damage to gorse foliage. S. melanogrammus only occurred in low numbers. No adult weevils have therefore been included in consideration of the foliage-feeding fauna of gorse.
The role and importance of Anarsia spartiella as a folivorous species 108.
Table 4.6 : The relative importance of phytophagous insects collected from
Ulex europaeus foliage at YC and WGP in two years.
("A" denotes adult weevil; * denotes that this species is
considered in more detail in Section 4.5)
WGP YC YC Species 1980 1980 1981
*Sericothrips staphylinus 2126 2837 3580 Wictyonota strichnocera 581 769 794 Apion ulicis (A) 645 322 283 *Asciodema obsoletum 94 268 327 *Pachylops bicolor 151 367 225 *Sitona tibialis (A) 4 186 61 *Agonopterix ulicetella 4 43 35 *Aphis ulicis 45 85 94 *Piezodorus lituratus 53 16 17 *Sitona regensteinensis (A) 23 53 8 *Polydrusus confluens (A) 6 33 6 *Strophosomas melanogrammus (A) 1 6 13 *Anarsia spartiella 2 8 6 *Pseudoterpna pruinata 0 4 6 Peribatodes rhomboidaria 5 5 0 Euceraphis punctipennis 15 8 0
Apion scutellare (A) 0 9 16
PKloeophthorus rhododactylis 10 0 0 Teptophyes punctitissima 5 0 0 Cerarnica pi si 0 0 3 Callophrys rubi 0 1 0 Geometrid (1) 1 0 0
(2) 1 0 0 Ematurga atomaria 0 0 1 Dasineura sp 0 1 0
(9 sampling occasions) (11) (6) was discussed in Section 4.4 (Figure 4.4).
Pseudoterpna pruinata (grass emerald) overwintered as LII - LIV larvae and completed development at the end of June. Too few larvae were collected in samples to consider detailed analysis of relative abundance between sites or between host-plant species.
Agonopterix ulicetella (Stnt.) was the only other lepidopterous species which occurred in measurable numbers in samples beaten from gorse.
This is a univoltine oecophorid which overwintered as an adult, and laid eggs during April and May. Eggs hatched in close synchrony with vegetative bud burst in early June and larvae developed to pupation by the end of
July. It is highly host-specific and was recently introduced into New
Zealand as a potential biological control agent for Ulex europaeus. Its seasonal pattern of occurrence on Ulex europaeus and Ulex minor for
1980-81 is summarised in Figure 4.6. Analysis of variance suggested that there was no significant difference between Ulex europaeus and Ulex minor as Irusts for A. ulicetella. Insufficient larvae were recorded at WGP to allsv-statistical comparison of A. ulicetella populations between sites.
Phanococcus aceris and Aphis ulicis (Walk.) proved to be the only phloem feeding insects on gorse at either site. Phanococcus aceris was too rar? £o sample by any practical method. Aphis ulicis colonies were also r^r^-but aphids could be beaten from gorse foliage. Peak numbers occurred in July and August but individuals could be found as late as September
1 (F" ' ^yre 4.7). The seasonal biology of Aphis ulicis is unknown.
Piezodorus lituratus (Pentatomidae) is an oligophagous species which has been recorded feeding on gorse pods (Southwood & Leston, 1959) and also may be partially predaceous (Butler, 1923). Its seasonal occurrence is summarised in Figure 4.7. This species overwintered as late instar nymphs and adults, and laid eggs in early spring. Eggs hatched in early June, at Figure 4.6 : Seasonal variation in the abundance of Agonopterix ulicetella
beaten from gorse.
• • Yateley Common U. europaeus 1980
x x Yateley Common U. europaeus 1981
A A Yateley Common U. minor 1980
A. The difference in abundance between years.
B. The difference in abundance between host-plants. 110.
insects per sample
M J J A Figure 4.7 : Seasonal occurrence of Aphis ulicis and Piezodorus lituratus.
• Yateley Common Ulex europaeus 1979
o Yateley Common Ulex minor 1979
a Windsor Great Park Ulex europaeus 1979
• Yateley Common Ulex europaeus 1980
A Yateley Common Ulex minor 1980
© Windsor Great Park Ulex europaeus 1980
x Yateley Common Ulex europaeus 1981 111.
A. ulicis
oa
* g>., fi)
insects per
sample
1.5 P. lituratus
1.0
0.5
x©
M S 112.
the same time as vegetative bud-burst in gorse, and a single generation or partial generation was completed during summer and autumn. This species was not encountered often in samples, except in early June when young nymphs were highly aggregated immediately after hatching. Numbers were
always insufficient to allow statistical comparison of populations on the
two gorse species, or between populations on Ulex europaeus at YC and WGP.
Two mirids were very common on the two species of gorse. Both
Asciodema obsoletum and Pachylops bicolor were univoltine, overwintering
%
as eggs. Both feed on leaf mesophylls though there is some evidence that
Pachylops bicolor is facultatively predaceous (G. McGavin, personal
communication).
The abundance of Asciodema obsoletum collected during three sampling
seasons is shown in Figure 4.8. As with most of the foliage-feeding fauna,
eggs hatched in late May or early June, at the same time as vegetative bud- burst in Ulex europaeus, and nymphal development was largely completed by
the end of July (day 210). Asciodema obsoletum appeared to prefer Ulex
oitropaeus to Ulex minor in 1980 as seen in Table 4.3. Significantly more
A. obsoletum were collected from Ulex europaeus at YC in 1980 (Table 4.4),
though Figure 4.8 suggests that this difference probably did not occur in
1979.
Peak abundance of Pachylops bicolor occurred in mid to late June.
Unlike A. obsoletum Ulex europaeus did not appear to be preferred over 3
U. minor as a host-plant, but again, significantly more of this species were collected at YC than at WGP in 1980 (Table 4.4).
Dictyonota strichnocera is a host-specific tingid which is univoltine
and feeds on leaf mesophyll. Along with Agonopterix ulicetella this
species has recently been recommended for introduction to New Zealand as
a potential control agent for gorse (Hill, 1981). The life history of this Figure 4.8 : Seasonal variation in the abundance ofDictyonot a striehnocera.
o —_ o 1979
• • 1980
x x 1981
A. Yateley Common Ulex europaeus.
B. Windsor Great Park Ulex europaeus.
C. Yateley Common Ulex minor 8
4
10
insects
per sample
10
8
6
4 Figure 4.9 : Seasonal variation in the abundance of Dictyonota striehnocera.
o o 1979
• • 1980
x x 1981
A. Yateley Common Ulex europaeus.
B. Windsor Great Park UZex europaeus.
C. Yateley Common Ulex minor.
Figure 4.10 : Seasonal variation in the abundance of Dictyonota striehnocera.
o o 1979
• • 1980
x x 1981
A. Yateley Common ZJlex europaeus.
B. Windsor Great Park Ulex europaeus.
C. Yateley Common Ulex minor.
116.
species is very similar to that of Asciodema obsoletum described earlier.
Brown (1981), incorporating some of the data represented here, has described the life history, and has calculated life-tables for the species at WGP and YC in 1981. He found no significant differences between pop- ulations on U. europaeus and U. minor, but populations on U. europaeus at
YC were considerably larger than those at WGP. In the present study, no significant differences were found between the abundance of D. strichnocera nymphs on U. europaeus and U. minor in 1980, though abundance on U.
% europaeus at YC was just significantly higher than at WGP (Table 4.4;
Figure 4.10).
The commonest phytophagous species on either gorse species was the thysanopteran Sericothrips staphylinus Hal. Larvae were collected from
June until September. Population numbers reached a peak in July and
August, but the numbers collected were extremely variable between each sampling occasion, each site, and especially between years.
The other insect species inhabiting gorse foliage were detritivorous or predaceous species. These have been listed in Table 4.7.
4.6 Discussion
4 b , 1 Differences^ in_f auria_of_ U_._eurc^a e w s^andj^ minor_
Most species of phytophagous insects collected during the period
1979-1981 were found on both Ulex europaeus and Ulex minor, and the fauna attacking gorse roots appeared to be similar on both species. Sitona tibialis was found in only very low numbers at Windsor Great Park where
Ulex minor was absent, and this may represent a degree of host-preference for Ulex minor. Since no larval collections were made this could not be confirmed. The abundance of Sitona regensteinensis was significantly higher in U. europaeus than U. minor in 1980, but the difference between 117.
Table 4.7 : Detritivorous and predaceous insect species encountered in gorse
foliage.
Detritivores
Psocoptera
Trogiidae
Trogium pulsatorium (L.)
Ectopsocidae
Eotopsoous petevsi Smithers
Caeciliidae
CaeciHus ? burmeisteri Brauer
Caecitius sp.
Psocidae
Trichadenotecnum (Loensia) fascicctum (L.)
Collembolla
Entomobryidae
Entomobryia multifasciata (Tullberg) All sites
E. nivalis (Lubbock) "
Ovohesella cinota (L.) "
Tomocerus longicomis (Muller) "
Tomocerus sp.
Lepidooyrtus sp. 118.
Table 4.7 : Continued.
Predators
Coleoptera
Carabidae
Dromius linearis (Olivier)
D. melanocephalus Dejean "
Elateridae
Dalopius marginatus (L.)
Staphylinidae
Anotylus tetracarinatus (Block)
Taohyporus hypnorum (F.)
Diptera
Syrphidae
2 unidentified species
Heteroptera
Anthocoridae
Anthocoris sp.
Orius niger Wolff.
Miridae
Phytocoris ? varipes (Boheman)
Nabidae
Nabis rugosus (L.)
Neididae
Berytinus minor (Herrich-Scheffer)
All predaceous insects were rare, though N. rugo^us and P. varipes occurred more frequently than other species. With the possible exceptions of these two species, all were regarded as vagrants. 119. sites was not significant.
Ulex minor and Ulex gallii both flowered in autumn whereas Ulex europaeus flowered in spring. Though no formal sampling of U. minor repro- ductives was carried out, the literature shows that many bud, flower and pod feeding species are bivoltine, completing one generation in the repro- ductives of each host species. On the other hand, univoltine species use only one host species. Similarities and differences between the faunas are summarised in Table 4.8.
Many of the folivorous insects were encountered in numbers too small to allow statistical comparison between U. europaeus and U. minor as host- plants. Of the common species, only Asciodema obsoletum showed a host- plant preference. Brown (1981) showed that Dictycnota strichnocera exhibited almost identical population characteristics on the two Ulex spp.
Of the rarer species, Apion scutellare may have a preference for Ulex minor since it was never collected at WGP and is found more commonly on low- growing vegetation (Hill, 1981).
Apart from the exceptions discussed, the faunas attacking foliage of each host species were very similar in composition, phenology, and abundance.
4.6.2 Faunal_di^fferences_between_Y£ and WGP
Results suggested very marked differences between the number and species richness of insects collected from U. europaeus at the two sites, though biological interpretation of these results is difficult.
Three features distinguished the YC site from WGP:
(1) Presence of U. minor.
(2) Host-plant age (6 yrs compared to c. 20 years, see Section 2).
(3) Host-plant height (1 m compared to 2 m) . 120.
Table 4.8 : Life histories of fauna associated with reproductives of Ulex
europaeus and Ulex minor.
Months Larva Ulex europaeus Ulex minor
Mirificarma mulinella 4-5
Agonopterix nervosa 5-6
Anarsia spartiella 5-6
Gymnoscelis rufifasoiata 4-5 8-9
Apion striatum 5
Odontothrips ulicis 5-7 9
0. ignobilis 9
Thrips flavus 7-9
Coleophora albicosta 1 7-4
Cydia internccna 7 7-3
C. succedana 6 9-4
Apion ulicis 5-6
Asphondylia ulicis 4-5 7-8 121.
Any one or more of these characteristics might explain the significant differences observed. The absence of Apion scutellare from Windsor Great
Park was particularly striking, as was the virtual absence of Sitona tibialis. Apion scutellare showed a preference for low growing gorse bushes for oviposition (Hill, 1981) but this was not an essential requirement since Apion -galls were frequently collected high on 1 metre bushes. The distribution of S. tibialis adults at Yateley Common (Figure 4.3) suggests that the height of gorse bushes cannot explain the difference in this species either. There appears to be little evidence from Section 3 that the quality of gorse as food varied with plant age. Both weevils may therefore show a degree of host-preference for U. minor over U. europaeus, though this was not demonstrated at Yateley Common (Table 4.3).
The abundances of A. obsoletum> P. bicolor and D. strichnocera were also significantly greater at Yateley Common. This could not be attributed to a preference for U. minor as host-plant, and is difficult to explain.
YC and WGP were not sampled on the same day, and it is possible that the differences detected by ANOVA which have been presented here may reflect the effect of sampling date discrepancies rather than properties of the sites themselves. This is particularly true of those differences at the 5% significant level.
4.6.3 Seas_ona.l_pa_t terns_ jji_the_gor s_e_fa_una
Several general patterns in the seasonal occurrence of the gorse fauna were observed. In Table 4.9 the 22 species which commonly attacked Ulex europaeus and Ulex minor have been grouped according to their life-history 122.
Table 4.9 : Seasonal patterns in gorse insects.
Type of Development Overwintering No. of Feeding site Voltinism pattern period stage species
1 Reproductives Uni- early spring adult 5
2 n Bi- ii larva 4
ii ii ti 3 adult 4
it 4 Foliage Uni- egg 4
it ii it 5 larva '1
ii it 6 ii adult 3
ii 7 Multi- summer 1 1
22 characteristics.
Earlier in this discussion the close correspondence between the life-
histories of the insect species attacking reproductive parts of gorse and
the seasonal occurrence of those parts was discussed. Table 4.9 shows
that univoltine species overwintered as adults whereas those species feeding
on both Ulex species overwintered as adults or larvae. All species co-
occurred as immatures with reproductive parts, and all development
activity ceased with seed dispersal in late spring (Figure 4.11).
Similarly strong seasonal patterns were observed amongst folivorous
species. All species were univoltine, with the exception of Aphis utieis which underwent an unknown number of generations through the summer months.
89% of folivorous species began and completed nymphal or larval development
in early spring, and no species began development on gorse foliage after
June. All folivorous species overwintered as adults or eggs except Pseudo-
terpna pruinata which overwintered as a larva and completed the major part
of its development in early spring (Figure 4.11).
Development of almost all common species attacking gorse was
restricted to early spring, and this appears to be the most consistent
generalisation which can be made concerning the life histories of the
fauna of Ulex europaeus. In most folivorous species, hatching of eggs
coincided extremely closely with vegetative bud-burst in early June. In
Section 2 it was shown that gorse had a long growing season, and abundant
succulent food appeared to be present throughout most of summer. The
reason for a preponderance of univoltinism and restriction of development period in gorse folivorous insects is therefore not immediately obvious, and this question is considered more closely in Section 5. The major modes of overwintering in all gorse insect species appeared to be as adults or as eggs, both strategies which allow rapid response to spring conditions Figure 4.11 : Patterns of occurrence of gorse insects in relation to host-
plant development. 124.
buds
flowers
young pods
pods
Asphondylia ulicis
> Mirificarma mulinella
Agonopterix nervosa
Gyrrtnoscelis rufifasciata
Apion striatum
Micrambe vini
Anarsia spartiella
Odontothrips ulicis
Apion ulicis
r Cydia intemana
Cydia succedana
growth
Dictyonota strichnocera
Asciodema obsoletum
Agonopterix ulicetella
Pachylops bicolor
Piezodorus tituratus
Aphis ulicis
T 1 1 1 r
A M J J AS and consequent synchrony with the physiology of the host-plant.
4.6.4 Feeding generalism and_spe£ia.l_ism of__the gorse fauna
The feeding strategies employed by phytophagous insects can be
defined as specialist or generalist. In this study, specialist species were defined as those restricted to the genus Ulex or several closely
related genera (i.e. monophagous or oligophagous). The degree of feeding
specialisation recorded in the literature concerning gorse phytophages was examined and compared with the degree of specialisation of species
collected over the three year period of the present study.
The literature records a very high proportion of generalists among
gorse phytophages. Such records are notoriously misleading however, and
the true number as reflected in the present 3 year study is much smaller.
Table 4.10 summarises the fauna recorded from continental Europe by
Zwolfer (1963), British records from Zwolfer's study augmented by further
records from the British literature (see Table 4.1), and records from the present study. Where two life stages attacked different parts of gorse,
they were counted twice' (there are 49 records in Table 4.10 from 41 phyto- phagous species).
With the exception of the Coleoptera, the European fauna is well represented in Britain (the missing species are mostly Apion spp which
attack gorse pods on the continent), and the proportions of specialists to generalists are similar. The British fauna was well represented in the present study, with the exception of 3 specialist Lepidoptera (which are extremely rare in southern Britain), and the large discrepancy between the number of generalist Lepidoptera recorded in British literature and in the present study. This study, which was carried out over a 3 year period, should have recorded most of the generalists which use Ulex spp as a host plant. It seems likely therefore that in this case literature records do TABLE ^.iQSummarised records of U. europaeus phytophages with proportions of specialists and generalists.
(Literature records from Zwolfer, 1963. British records include present study)
COLLECTED IN LITERATURE RECORDS THIS STUDY
Continental British (Spec : Gen) (Spec : Gen) (Spec : Gen) LEPIDOPTERA 37 35 15 (11 : 26) (10 : 25) (7 : 8) COLEOPTERA 17 17 25 (9 : 8) (9 : 8) HOMOPTERA (12 : 13) 6 4 9 (2 : 4) (2 : 2) HETEROPTERA (3 : 6) 6 6
DIPTERA 6 (4 : 2) (4 : 2)
(4 : 2) 2 (2 2: 0) OTHERS 5 2 (2 : 0) (5 : 0) (2.: 0) (5 5: 0) FOLIAGE FEEDERS 62 53 32 (5 5: 0) (21 : 41) (16 : 37) (12 : 20) REPRODUCTIVE FEEDERS 22 18 17
TOTAL (16 : 6) (16 : 2) (16 : 1) (37 8:4 47) (32 7:1 39) (28 4:9 21) 127.
not represent a true picture of the gorse fauna. It is also interesting the the spurious records all appear to be from gorse foliage as opposed to reproductive structures, and probably represent records of itinerant larvae not strongly associated with gorse at all. The few generalist species which were collected in the present study were rare, and therefore contri- buted little to the overall structure of the phytophagous community.
Seasonal patterns were dominated by the more specialist species.
Rhoades & Cates (1977) proposed that the impact of grazing by generalists on widespread and long-lived plants such as woody shrubs should be less than the pressure on more ephemeral species. Lawton & Schroder
(1979) predicted from this that woody shrubs should support a smaller proportion of generalist insect species than annual plants, but found from the literature record that the opposite was true. The literature record shows that 63% of the species associated with JJtex are generalists, which confirms the findings of Lawton & Schroder that woody shrubs bear more polyphagous herbivores than theory would predict. These species were all idie, however, and since their contribution to overall grazing pressure is small in comparison to that of the more numerous monophages and oligophages,
Rhoades' & Cates' hypothesis cannot be negated on this evidence alone. As
Lawton & Schroder point out, closer consideration of oligophagous herbivores would add much to our understanding of feeding specialism, but this inform- ation must come from detailed survey information (such as this study) rather than the often misleading literature record.
4.6.5 Richnej3s__of^ the £ors£ _fauna_
The number of British insect species associated with several host plants in the tribe Genisteae were obtained from 12 works of the standard literature. These "literature record samples" were used to represent the richness of each fauna, and 128.
have been summarised in Table 4.11. The number of species attacking each
plant did not appear to be related to the relative abundance of the host-
plant measured as the number of 10 km squares in which the host-plant was
found in Great Britain (Strong, 1979; Perring & Walters, 1962) (Table
4.11). It was also assumed that equal collecting effort was afforded
each species through the years. The fauna of Cytisus scoparius appears
to be much richer than that of other species in the tribe, with 30% more
species than Genista tinctoria and almost 70% more than Ulex europaeus.
Ulex europaeus appeared to carry more species than Ulex minor, and Genista
anglica seemed to harbour the least species of any plant in the tribe.
The faunas associated with host species other than Ulex europaeus and
Cytisus scoparius have probably works quoted,
but such large differences in the number of species between host plants
probably reflect true differences in faunal species richness. The differ-
ences shown in Table 4.11 mostly involve the Lepidoptera associated with
each host-plant.
Lawton & Schroder (1979) analysed the faunal composition of several
different growth forms of host-plant, and found that approximately 65% of
the phytophagous insect species attacking woody shrubs were Lepidoptera.
Table 4.10 shows that in the present study, only 31% of the species recorded
were Lepidoptera, while only 49% of the British gorse fauna were Lepidoptera.
Some of the difference shown in the present study can be attributed to the misleading literature record, but the British list which is based on that
record also shows that Lepidoptera are underrepresented on gorse. Emmet
(1979) records almost twice as many lepidoptera species on both C.
scoparius and G. tinctoria than on either Ulex spp. In fact, only 3 species of microlepidoptera attack gorse foliage. The reason for the differences
between host-plants is not known but some possibilities are discussed in Table 4.11 : Species richness of phytophagous insects on 5 host-plant species (Tribe: Genisteae) estimated from some
standard references.
(The number of 10 Km squares in which each host-plant is found is given in brackets, Perring & Walter, 1954)
No. of insects associated with host-plant Authority Insect group Ulex Ulex Cytisus Genista Genista (see Table 4.1) europaeus minor scoparius tinctoria anglica
(2167) (132) (1864) (463) (376)
Heteroptera 6 6 10 2 0 Southwood & Leston, 1959 Macrolepidoptera 5 3 5 1 2 South, 1961 Carter, D.J., 1981 Stokoe, 1944, 1948
Microlepidoptera 8 3 14 20 7 Emmet, 1979
Aphids 1 1 4 5 3 Davidson, 1925
Coleoptera minus 5 5 6 4 4 Walsh & Dibb, 1954 weevils
13 Fowler, 1887-1913 Hoffman, 1950, 1954, 1958 Curculionidae Scherf, 1964
TOTAL 31 24 52 39 21 130.
Section 5.
4.7 Summary
1. The faunas of U. europaeus and U. minor were very similar. Some uni-
voltine species feeding on reproductive structures specialised on one
species or the other, though bivoltine species used both host-plants.
Asciodema obsoletum was the only folivorous species which seemed to
prefer U. minor, otherwise the faunas were very similar.
2. The virtual absence of Sitona tibialis from WGP suggested a preference
of this species for U. minor, as did the absence of Apion soutellare,
though other factors may be responsible for this. Differences in
abundance of other phytophagous insects between YC and WGP may be a
result of discrepancies in sample dates.
3. The seasonal pattern of occurrence of insect species attacking gorse
reproductive structures was closely tied to the phenology of the host-
plant structure which they attacked. Most folivorous species hatched
and developed very near the time of vegetative bud-burst, but since the
resource on which they fed was available throughout the summer, the
reason for this early spring development is not immediately obvious.
89% of common folivores were univoltine.
4. Feeding generalists were far less common than the literature implied.
All common species attacking either reproductive structures or foliage
attacked Ulex spp only, or occasionally one other genus of the tribe
Genisteae.
5. The gorse fauna was poor compared to that of other related species.
Fewer Lepidoptera attacked Ulex spp than current theory would predict. 131.
SECTION 5
THE EFFECTS OF HOST-PLANT QUALITY
ON THE INSECT FAUNA OF GORSE
5.1 Introduction
The structure of the phytophagous insect community living on a host- plant is a patchwork based on the phenology and population dynamics of each member species of that community. Much of the research concerning the relationship between insects and plants is aimed at the control of insect populations by biological or other means. White (1978) has recently pointed out, that while pressure can be exerted on insects from above through predation and parasitism etc., it is becoming increasingly evident that equally strong pressures are exerted from below by the action of the plant on the insect populations feeding on it. Recently 4 theories have been proposed to explain the observed pattern of phytophagous insect communities based on the influence of host-plants on their insect fauna in ecological time.
(1) Species-area effects
(2) "Living-space" effects
(3) Defense strategies in plants
(4) Food-quality effects
The expansion of island biogeography theory to the field of insect- plant relationships has led to a number of ideas based on the predictability of host-plant material for phytophagous insects in time and space. This area has recently been reviewed by Strong (1979). This theory has not been tested in the present study for reasons outlined in Section 1.
In 1978, Lawton proposed that the number of insect species attacking 132.
a frond of Vtevidvum aquiUnwn was closely related to the area of the frond
on which they lived, because as the frond expanded it became architecturally
more complex and could accommodate more insect species as the number of
different niches increased. This theory arose as a logical extension to
the suggestion that the number of insects attacking plants of different
life-forms could be related to host-plant complexity (Lawton & Schroder,
1977). He admitted that factors other than complexity could account for
the high correlation but was unable to bring any further direct evidence
to bear, though he quoted a number of studies which seemed to bear this
out. There have been very few faunal studies which provide data to test
this theory. In the present work, the amount of living space available to
insects was measured (Section 2.4.2) and compared with the number and
abundance of the insects attacking gorse (Section 4).
The role of secondary plant compounds as modifiers of insect behaviour
and feeding efficiency is well known and has recently been well summarised
by Rosenthal & Janzen (1979). Lawton (1976), using the bracken system
^dc3cri-bed above assessed the importance of such chemicals in determining
the way in which herbivores attacked that host-plant. Feeny (1970) also
considered the ecological significance of secondary compounds, namely
tar~ins, in his study of the oak folivore community. This work was
extruded to other tree species by Wint (1979). Rhoades & Cates (1976)
app >-^ched this problem from a study of the responses of a generalist
herbivore to a range of plants exhibiting different secondary chemistry.
Using these two approaches, Feeny (1976) and Rhoades & Cates (1976)
independently recognised two kinds of chemical defenses in plants which
Feeny termed "qualitative" and "quantitative" and Rhoades & Cates called
"toxic" and "digestibility reducing" defenses. These two studies were
reconciled recently by Rhoades (1979) and Feeny's terms are used here. 133.
Qualitative defenses are present in small quantities in ephemeral or cryptic plants or plant parts, and are highly toxic or repugnant in small quantities. They are metabolically economical to produce. Quantitative defenses are those present in abundant, large plants or plant parts prone to exploitation by specialist insects in evolutionary time. Such defense chemicals are present in large amounts, reduce the performance of insects which use the plant, and are metabolically costly to produce. Tannins provide the best known example of quantitative defenses, but structural
* defenses such as foliage toughness can also be classed as such. These two types of defense form the ends of a continuum from "unapparent" annual herbs to "apparent" trees Feeny (1976). Prediction of the secondary chemical composition of a woody shrub such as gorse in these terms is impossible since it falls in the middle of that continuum. Rhoades (1979) has recently formulated a general theory which incorporates the features described above, but can be used as a framework to consider other cases.
Evolutionary theory predicts that animals forage for food in a manner which will maximise their inclusive fitness. This is a concept which has been widely accepted and used in many types of ecological research, and has become known as optimal foraging theory. Fitness is a very difficult characteristic to measure, and no plant/herbivore system has ever been studied with precisely this aim in mind. Many of those studies already quoted in earlier Sections, and lin fact most studies of insect/plant relationships demonstrate the systematic use of plant resources by phyto- phagous insects which are probably optimal (e.g. Lawton, 1976; Feeny, 1970).
Prestidge (1980) has shown that leafhoppers actively migrate to grasses which provide an optimal diet, and this is reflected in their reproductive success. McNeill (1973) showed that the reproductive success of Leptotema dolobrata was determined by the success of life history synchronisation 134.
with an annual nutrient flush in its host-plant. These studies both seem
to demonstrate optimal foraging by phytophagous insect species in the
strict sense of the definition. It is difficult to apply optimal foraging
theory to insect/plant interactions however, without detailed knowledge
concerning the influence of the host-plant defensive system on the phyto-
phagous fauna, especially its array of defensive capabilities.
Rhoades (1979) has pointed out the need for plants to maximise fitness
in just the same way that foraging insects do, and has proposed that an
"optimal defense strategy" can apply to the interaction between a host-
plant and its herbivores. This theory is based on the following
hypotheses-:
(1) Organisms evolve and allocate defenses so as to maximise individual
inclusive fitness.
(2) Defense is costly in terms of fitness because it diverts nutrients and
energy from other needs, particularly growth and reproduction.
(3) In general, organisms evolve defenses in direct proportion to their
risk from herbivores, and in inverse proportion to the cost of defense.
(4) Within a plant, defenses are allocated according to the risk and value
attached to each tissue type.
-
(5) Since defenses are costly, they should be reduced in the absence and
increased in the presence of herbivore attack.
(6) In a particular individual, the resources available for defense are
those surplus to maintenance. Stressed individuals should therefore
be less well defended than unstressed individuals.
This theory assumes optimal foraging by the herbivores involved. He presents evidence to support each of these hypotheses.
Coevolution between optimally foraging insects and optimally defended plants should result in a regular and logical pattern of use by insects determined by the various defensive strategies of the plant. The secondary chemistry of gorse foliage was discussed in Section 3, and only two classes
of compound, alkaloids and isoflavones varied in a manner which would
suggest that they act in a protective capacity. In addition, two
structural defensive mechanisms, foliage toughness and water content
(succulence) were measured. In this section, the relationship between the pattern of use of gorse foliage by insects and the defensive strategies of
gorse are examined.
McNeill & Southwood (1978) outlined the importance of insect nutrition, and especially the availability of nitrogenous compounds in the food, to
the performance and seasonality of phytophagous insects. The dominance of nutritional or primary plant chemistry in determining the phenology and
reproductive potential of insects has now been demonstrated in many insect/
•host-plant systems (e.g. McNeill, 1973; Hill, 1976; Van Emden, 1977;
Lawton & McNeill, 1979; Prestidge, 1980; Hill, 1982; McNeill & Prestidge,
1982). White (1976, 1978) has used the detailed published information concerning the effects of food quality on herbivores to suggest that herbivores are limited by a relative shortage of appropriate food, especially for the very young. He also suggested (White, 1978) that the reaction of foliage nutritional quality (particularly nitrogen content), mi^^t be a strategy by which plants could avoid destruction by their predators. A similar effect could be achieved by making nutrient rich plant parts relatively rare by dispersion, "flushing", or by the evolution
of defensive mechanisms.
Apparently independently of White's influence, Moran & Hamilton (1980) 136.
have also examined the proposition that poor nutritive quality of foliage could evolve as an adaptation to insect herbivory and thus improve the fitness of the host-plant. Logically, decreased nutritive quality should lead to greater consumption of tissue, and hence reduced fitness in the host-plant. There are a number of circumstances vhen the opposite is true.
If successive herbivore generations tend to feed on the same host individual, then low nutritive quality will act to prevent further buildup of herbivore numbers, thus increasing plant fitness. This would be part- icularly true if neighbouring plants were relatives in which case some mobility between neighbours could occur. The gorse fauna appears to have very limited dispersal capabilities (McNeill & Prestidge, 1982), and such circumstances may very well apply. If prolonged development of an insect because of low food quality led to increased mortality, this too could lead to selection for decreased nutritive quality. Moran & Hamilton conclude that this strategy is widely possible but has never been demon- strated .
To look more closely at the ideas presented above, the structural defenses, living space, chemical defenses, and nutritive quality of gorse foliage have all been measured in the present study, along with the structure of the insect community and the phenology and abundance of individual species attacking gorse foliage. Seasonal changes in all of the~2 variables have been recorded at two sites for two years and the results have already been discussed in detail in Sections 2-4. In this section the resulting patterns of plant use and plant phenology are contrasted and compared. In addition, the relationship between the phyto- phagous fauna of gorse and their predators is considered.
5.2 Methods
Storage and retrieval methods for all insect sampling data have been 137.
described in Section 4.2. The diversity of the phytophagous insect fauna was calculated as the Simpson-Yule index,
using a sorting and retrieval programme within SIR (Scientific Information
Retrieval; see Section 4.2).
Spiders were sampled along with the insects using the method described in Section 4.2. The abdominal length of each spider was estimated in the field, and ranked in the 4 categories 0-2, 4-6, 6-8 and 8-10 mm.
The sum of the abdominal diameters was calculated using the median for each rank. This was used as a spider biomass index. The accuracy of this index in predicting spider biomass was determined by weighing 15 dry samples of spiders ranked as described above.
Measures of plant structure and morphological adaptations for defense against herbivores are described in Section 2. Measures of foliage primary and secondary chemistry are described in Section 3.
Statistical analyses in this section have been carried out using pooled data collected from Ulex europaeus at YC in 1980 and 1981, and WGP in 1980.
This was necessary to obtain sufficient data points for regression analysis.
Pooled results appear to be reliable, since floristic events occurred at very similar times between years and between sites (Appendix II).
Correlation, regression and multiple regression analyses were carried out using the statistical package MINITAB (Ryan et al., 1981). All transformed variables were normally distributed.
5.3 The Effect of Predators
Figure 5.1 shows the relationship between log dry weight of spiders in each of 15 samples and the spider biomass index calculated for each of Figure 5.1 : Applicability of the spider biomass index.
Y = 0.30 + 0.79 X
t = 2.53 p < 0.05 138. 139. those samples. The index was a predictor of spider biomass (Figure 5.1).
Insect predators were extremely rare on gorse foliage, as mentioned in Section 4, and their contribution to predation of the phytophagous insects found on gorse was considered to be negligible compared to that of the spider fauna. Spiders were extremely common, and late in summer probably outnumbered phytophagous insects in samples. Bibby (1977) also measured the number of arthropods on gorse, and found that the biomass of spiders peaked in August and September. It was therefore assumed that spider biomass effectively represented the total predator pressure exerted on the insect fauna of gorse. Very similar conclusions were drawn by
Bibby (1977) who considered that spiders formed a large part of the diet of the dartford waller (Sylvia undata (Boddaert)), which forages almost exclusively in gorse thickets.
The relationship between predator pressure and the seasonal variation of gorse insect abundance was examined. There was no significant relation- ship with the number of breeding phytophages nor with the total abundance of phytophages (i.e. including non-feeding adults etc) found on Ulex europaeus. Similarly there was no relationship between the spider biomass index and the number of phytophagous insect species found on gorse (Table
5.1).
In a recent paper which considered the role of competition in forming the observed community patterns of folivorous insects, Lawton & Strong
(1981) advanced the view that enemy-free space might be considered as a limiting resource for insects along with those factors more commonly considered, such as food quality and quantity. They proposed that co- evolution between natural enemies could modify the phenology of host species so as to minimise predator pressure on that species. (The inter- actions between such influences and plant-borne selection pressures has 140.
also been discussed by Lawton & McNeill, 1979). Given no such coevolution, one would predict a strong positive relationship between predator biomass and the number of prey on gorse foliage. Given strong selection for enemy- free space one might expect a negative relationship between predator biomass and prey. In fact, no relationship was found at all, which suggests either a dynamic equilibrium between the responses of gorse insects and their predators, or that there is no interaction at all. Detritivores such as Entomobryia spp are also prey for spiders, but have not been considered here.
In fact, it seems likely that spiders use gorse plants simply as a framework on which to live, and that itinerant insects provide the bulk of prey. This is supported by the fact that in New Zealand, spiders again form the dominant portion of anthropod biomass, despite the fact that very few indigenous insects have crossed over to gorse and that the fauna is much poorer than it is in Britain (Gaynor, 1977).
Despite the apparent lack of any relationship between the number of specics or individuals of gorse phytophages and spider predation pressure, the high numbers of spiders on gorse probably account for the low numbers of insects found in gorse foliage, especially in late summer.
5.4 Patterns of Foliage Use by Insects
Throughout Section 4 it was pointed out that hatching and early development of most insect species feeding on gorse foliage occurred immediately following vegetative bud-burst in mid-May to early June. In
Figure 5.2 this is reflected in the rapid rise in the number of gorse foliage-feeding species collected from gorse foliage in 1980-81. The number of species collected on gorse foliage peaked in late June, and no species began developing on gorse foliage after the end of June. When all phytophagous species collected on gorse were considered, the pattern was Figure 5.2 : The number of folivorous insect species collected on gorse
through the season.
• • 1980
x x 1981
A. Species which reproduce on gorse foliage.
B. Total phytophagous species beaten from gorse. 141.
No. of species
per B sample
20
10
M Figure 5.3 : The total abundance of folivorous insect species collected
Ulex europaeus at Yateley Common. 142. 143.
repeated, since most of the species on foliage were adult weevils which
could be found in foliage all year round.
Peak populations of all phytophagous species which breed on gorse also
occurred in June, shortly after vegetative bud-burst (Figure 5.3) and then
declined throughout the summer period as the insects developed. All
univoltine species were adult or had pupated by late July.
This early spring activity by the phytophagous insect fauna was
reflected in the sharp rise in species diversity at the end of May and the
beginning of June as new species appeared in relatively large numbers.
Diversity also declined throughout summer, and this was particularly
noticeable in 1981 (Figure 5.4).
Early spring activity coincided with a number of trends in host-plant
structure and chemistry, the effect of which are considered in Sections
5.5.1 and 5.5.2.
5.5 The Effects of Plant-Borne Factors
'5.5.1 Plant j3truc_tu_re^ and ]J.ving_S£ace
In Section 2 the seasonal variation of 3 variables which contribute to
the structure of gorse plants was presented. New growth began in mid-May
and shoots grew apically until August (Figure 2.3). As shoots grew the
water content of whole shoots declined, though the terminal 2 cm of each
shoot remained succulent throughout the growth period (Figure 2.5). The
mean toughness of spines on gorse shoots increased with shoot length,
though again the terminal 2 cm of each shoot was succulent and soft
throughout the summer. The general pattern of these changes is summarised
in Figure 5.5.
The seasonal variation in the number of insect species, the abundance of
those species and the diversity of the insect fauna is presented in Figures Figure 5.4 : The diversity of folivorous insect species through the season
on Ulex euvo-paeus at Yateley Common.
A. Diversity of folivores reproducing on gorse.
B. Diversity of all phytophagous insects on gorse foliage. 144. 5.2, 5.3 and 5.4 respectively. Initially, the number of insect species which bred on gorse increased with increasing shoot length. The number of
species dropped later in summer while shoot length continued to increase.
There was nevertheless a significant correlation between the number of
insect species and shoot length (Table 5.1). A similar trend was shown
when all phytophages were included in the analysis, but the relationship was not significant. The abundance of phytophagous insects breeding on
gorse was also significantly correlated with shoot length or "living space"
Lawton (1978) proposed that the number of species which used bracken
fronds through the season was related to increasing frond complexity. In
gorse foliage this also appears to be true, in that those species actually
breeding were strongly related to increasing shoot living space through the
season, whereas when all phytophagous species, including non-feeding adult
phytophages were added to the analysis, this relationship was lost.
Lawton (1978) predicted that mechanisms which protected foliage would
influence the season in which that foliage would be attacked. He was
largely concerned with chemical defenses, which are discussed further in
Section 5.5.2, but the seasonal variation of two structural protection mechanisms are relevant. As shoots grew, mean shoot toughness increased while water content, or succulence, decreased through the season. Lawton's ideas would suggest that the timing of heaviest attack would be negatively correlated with mean toughness and positively correlated with foliage water coif' ent. Peak period of attack is represented by the number of immature and breeding phytophages collected, and Table 5.1 shows that this was not positively correlated with water content, nor with mean shoot toughness.
These mechanical devices therefore appear to have no influence on when gorse foliage is attacked by phytophages, and confirm the apparent influenc of shoot length or living space. The same relationships were shown when Figure 5.5 : Summary of seasonal trends in folivorous insects and some
plant factors affecting those insects. 146. Table 5.1 : Correlation o^' faunal variables with 8 plant borne factors.
(S = number of species, n = abundance, D = diversity as the Simpson-Yule index)
For species which breed on For all phytophagous insects gorse foliage on gorse foliage
log S log(N+l) D log S log(N+l) D
Shoot length 0.529 0.493 - 0.058 0.049 0.440 - 0.371 * **
Toughness 0.466 0.415 - 0.150 - 0.030 0.372 - 0.405 * -O •vj
Water content 0.389 - 0.473 0.325 - 0.128 - 0.473 0.490 * . *
Nigrogen content - 0.261 - 0.522 0.238 0.100 - 0.473 0.604 * ** *
- 0.334 - 0.384 0.273 0.158 - 0.344 0.542 Alkaloid content **
0.717 0.524 - 0.386 - 0.426 0.429 Isoflavone content * 0.012 •kick *
Carbohydrate content 0.328 0.089 0.036 0.057 0.023 0.161
Spider biomass index 0.158 0.200 - 0.352 - 0.172 0.146 0.167 148.
all phytophagous insects were included in the analysis, largely because breeding species dominated insect abundance in early spring during peak
insect attack. The structure of the phytophagous insect community, as represented by the Simpson-Yule diversity index yielded little information about the interaction between phytophagous insects and the structure of their host-plant. The only significant relationship was between the diversity of all phytophages and foliage water content. This result was dominated by the negative correlation of phytophage abundance with foliage water content.
These results appear to strongly confirm the views of Lawton (1978) that the number of insects which attack the foliage of a plant is related to the living space available to those insects on the plant. Living-space also appears to be the dominant factor determining when insects attack the foliage, rather than the mechanical protective devices of the plant. When he considered plant defense in 1978, Lawton mainly had chemical defenses in mind, and their role is discussed in Section 5.4.
The demonstration of significant relationships between insects and host-plant factors cannot demonstrate causation, as Lawton (1978) freely admitted. This is particularly true when there is autocorrelation between the predictor variables used in correlation and regression analysis. In particular, this can give undue importance to the less important of auto- correlated variables (Butt & Royle, 1974). Table 5.2 clearly shows that
the physical plant parameters measured in this study and discussed in this
section are very strongly autocorrelated. Disentanglement of the individual effects of variables when so heavily autocorrelated is extremely difficult, but the relative importance of these three variables in determining the
structure of the gorse phytophagous fauna is discussed further in Section
5.5.6. In light of the reservations expressed, interpretations presented 149.
in this section should be regarded as tentative.
5.5.2 Plant_ chemistry
The seasonal variation of foliage primary and secondary chemistry were measured, and the detailed results have been presented in Section 3. The
concentration of nitrogenous compounds in the foliage was high in very
young new shoots, but declined to a low level by July. For 90% of the
year the foliage nitrogen level was suboptimal for insect growth and
performance (Mattson, 1980; Southwood, 1972). Other nutritional measures'
of foliage quality (including carbohydrate content), did not appear to be
limiting to insect performance.
Gorse foliage seemed relatively unprotected by the battery of
secondary chemicals often associated with woody plants (Rhoades & Cates,
1976; Feeny, 1976). Only two classes of compounds, alkaloids and iso-
flavones, were present in measurable quantities, and the seasonal variation in the concentration of both types of chemical have been
discussed in detail in Section 3.4. Both have also been included in this
analysis.
Isoflavone proved to be a good predictor of the number of species which inhabit gorse foliage, especially those species which completed their development on the foliage (Table 5.1; Figure 5.5). To a lesser extent
though still significant it was also negatively correlated with the number
of phytophagous insects collected from gorse (Table 5.1).
The ecological reason for this relationship is not immediately obvious. The isoflavone concentration in foliage fell very early in
spring, but rose again in autumn foliage. In Section 3.4.5 the argument was made that since isoflavones are often associated with flower pigments
(Harborne, 1961, 1969), the peaks in foliage concentration were associated with cessation of flowering in spring and flower bud formation in autumn. 150.
It seems very unlikely that these served a protective function for gorse
foliage against herbivores since foliage concentration was very low during peak insect activity, and no insects developed on gorse foliage in autumn.
The statistical relationship is strong, however, and this possibility
cannot be ruled out without more detailed knowledge of the role of iso-
flavones in plant foliage (see also Section 3.4.5).
The concentration of alkaloids in gorse foliage also fell rapidly at bud-burst but unlike isoflavone concentration remained low throughout
summer and autumn. Foliage alkaloid content was not significantly correlated with either the number or abundance of gorse phytophages, but was positively correlated at the 5% significance level with the diversity of all phytophagous insects associated with gorse foliage. Peak alkaloid
levels coincided with the emergence of non-feeding adult weevils from the
roots and from pods, resulting in high diversity. Since these weevil adults appeared not to feed (Section 4.5) this relationship was probably not of ecological significance to foliage herbivore activity.
The alkaloid concentrations used in this analysis were derived from the combination of data presented in Figure 3.7. There is some evidence from those results that the timing of the decline in alkaloid concentration may vary somewhat from year to year. This interyear variation must have a large effect on the degree of protection which alkaloids can impart to the foliage, and also change the relationship between alkaloid concentration and the measures of herbivore activity used in this study.
Two indicators of the quality of gorse foliage for food have been used in this analysis. The concentration of soluble carbohydrate in gorse foliage was measured as an indicator of simple assimilable carbohydrate content. Levels did not vary much through the year, and were maintained at a level which can adequately support insect growth and reproduction 151.
(Section 3.4.3) (Southwood, 1972). It was not surprising therefore that soluble carbohydrate content was not significantly related to any of the measures of insect occurrence presented in this section (Table 5.1).
Foliage nitrogen content, however, declined rapidly immediately after vegetative bud-burst from a high level of 25% protein to approximately 10% protein within 6 weeks. This very low concentration was maintained through the remainder of the year (see Section 3.4.1; Figures 3.1 and 3.2). In considering the phenology and abundance of the various phytophagous insects attacking gorse foliage (Section 4.5) it was pointed out that most species hatched immediately on appearance of new tissue at vegetative bud-burst.
Since nitrogen content declined rapidly at this time, a strong negative correlation should exist between the total nitrogen content of foliage, and phytophagous species number, abundance on diversity. Such relationships do occur, and are significant for abundance (which represents the timing of attack) and for the diversity of all phytophagous species on gorse foliage (Table 5.1). This last measure is again inflated by the emergence of non-feeding imagines as discussed earlier.
The negative correlation of peak abundance with food quality appears to be an anomaly at first sight, but is logical on close examination.
White (1978) has pointed out that the availability of high quality food is very important to young herbivores. In this case selection has acted to maximise the nutritional quality of the food available to young stages, while minimising the possibility of early hatching larvae or nymphs emerging to find no available food at all (i.e. before bud-burst). A significant negative relationship means a sharp response in insect numbers to the rapid decline in food quality at the earliest possible moment. The slight lag between the events may also be influenced by the high alkaloid levels in buds and small shoots as discussed earlier. Table 5.2 : Autocorrelations between independent variables used in regression analysis.
Shoot Water Nitrogen Alkaloid Isofl. Carbo. Spider Toughness length content content content content content index
Shoot length 0.946 - 0.664 - 0.812 - 0.903 - 0.800 - 0.523 0.048 •kick kkk kkk kkk kkk *
- 0.639 - 0.868' - 0.945 - 0.678 - 0.537 Toughness ** - 0.084 kkk •kick kkk kk
0.512 0.614 0.432 0.269 Water content ** * - 0.105 i 0.568 0.477 Nitrogen content 0.866 * kkk kk 0.186 •
0.563 0.570 Alkaloid .content ** ** 0.041
Isoflavone content 0.448 k 0.003
Carbohydrate content - 0.219
Spider biomass index 153.
As with the structural components of gorse, the concentration of some chemical components of gorse foliage are strongly autocorrelated (Table
5.2). Chemical components are also strongly correlated with the structural components discussed earlier, shoot length in particular. The inter- pretation of the effects of plant chemistry presented here must therefore also be regarded as tentative.
5.6 The Relative Importance of Plant-Borne Factors
As already mentioned, the autocorrelation of independent variables makes their value in predicting insect activity extremely difficult to assess (Butt & Royle, 1974). As shown in Table 5.2, autocorrelation be- tween different independent variables was large in this analysis. Only two variables,(spider biomass index/ foliage and/ soluble carbohydrate content could be considered sufficiently free of autocorrelates for the analyses presented earlier in this section to be accepted without modification.
Neither factor was related to insect species number, abundance or diversity.
Further analysis of the remaining variables was required.
The influence of individual autocorrelates can be examined by multiple regression techniques. The method chosen assessed the contribution of the mean square (MS) of the variable entered last in the multiple regression compared with the residual MS. If significant, the resulting F value
(with 1 and N - the number of independent variables - 1 degrees of freedom) showed that the variable contributed significantly to the regression in the presence of its autocorrelates. By putting each variable into the multiple regression model last, the contribution of each was assessed. A non-significant F value meant that the last variable was too strongly correlated with one or more variable already in the model to contribute any significant information. The F values can be ranked however, to give Table 5.3 : Assessment of the contribution of 8 independent variables to a multiple regression model (after Strong,
1974; see text for details; 1, 13 df).
F-value contributed by
Shoot Water N Carboh. Alkaloid Spider Isoflavone Toughness length content content content content index content
log S (breeding species) 0.50 0.00 1.05 2.85 0.75 0.19 2.15 3.12
log(n+l) (breeding species) 1.65 0.26 2.26 3.25 0.24 0.05 0.70 0.58
D (breeding species) 0.19 0.50 3.10 4.39 0.94 0.60 9.95 5.00 :k*
log S (all phytophages) 0.06 0.57 1.99 0.30 0.01 0.10 0.65 5.15
log(n+l) (all phytophages) 1.03 0.22 2.11 2.49 0.47 0.02 0.23 0.20
2.78 0.31 4.50 15.40 1.86 3.24 4.91 0.43 D (all phytophages) ** an indication of the importance of each variable in its complex of auto-
correlates. This method was employed by Strong (1974). Table 5.3 gives
a matrix of F values (with 1 and 13 degrees of freedom) for each variable
when entered last in the 6 multiple regression analyses.
The degree of multicollinearity was so high that only two factors
contributed significantly to the regression in the presence of their auto-
correlates. One was the spider biomass index which significantly explained
some variation in the diversity of phytophages breeding in gorse. Table
5.1 shows that this negative relationship approached a significant
correlation, and considering that spider biomass was not correlated with
any other variable, this result was not surprising. The contribution to
explaining variation in the diversity of all phytophages on gorse foliage
was also high, but not significant. Foliage nitrogen content contributed
significantly to explaining the diversity of all phytophages on gorse.
The role of foliage nitrogen is discussed again later.
Though not significant, isoflavone made the largest contribution to
„ the- explanation of variance in 4 of the 6 analyses, in keeping with the
relatively small degree of autocorrelation (Table 5.2). It seemed to
affect the species number more than phytophage abundance. The significance
of isnflavones has already been discussed.
Foliage nitrogen content made a larger contribution to the multiple
regression models than might have been predicted because it was very
strongly negatively correlated with shoot length, which proved such a good
predictor in Section 5.3.
Linear regression of species number and abundance of phytophages which
bred on gorse against shoot length yielded highly significant results
(Section 5.3; ). Having taken account of the strong auto-
correlations shown in Table 5.2, shoot length per se had much less influence 156.
on the models than it's correlates toughness, foliage water content, nitrogen content and alkaloid content. Of the 2 structural variables examined, water content appeared to be the dominant influence.
The Simpson-Yule index has been used throughout this section as a single figure to describe the interaction between the number of phyto- phagous species and their abundance, and so describe the structure of the phytophagous community. Of the factors which were considered, foliage nitrogen content, isoflavone content, and water content were adjudged to be the most dominant influences on insect community structure. This was only reflected in the Simpson-Yule measure incorporating phytophagous species not actively breeding on gorse, i.e. including adult weevils etc.
It seems likely that the small number of species involved (2-8) makes the
Simpson-Yule index statistically unreliable for use as a measure of structure for breeding species only. With 10 apparently irrelevant species added, the index for all phytophages shows similar trends to the other measures.
5.7 Discussion
Experimental investigations of biological problems allow control of experimental design and measurement of treatment variables independently.
Analysis of field-collected information is much more difficult because of the complex interrelations of variables and the existence of unknown influences on the dependent variable under investigation (Butt & Royle,
1974). In the case reported here, strong autocorrelation, between year and between site variation has made linear regression and correlation unreliable, and multiple regression analysis difficult to interpret.
Despite that, it has been possible to make some generalisations and to make some comment on existing theory.
Initial analysis suggested that Lawton's (1979) "living space" theory provided an adequate explanation of the observed pattern of gorse foliage use by insects. Multiple regression analysis showed this to be an artifact
of strong autocorrelation with several other measured variables including
foliage nitrogen content, foliage water content, and possibly foliage alkaloid concentration. Shoot length was a good predictor of the patterns but was not causally involved. Lawton's theory does not therefore apply to the insect fauna of Ulex europaeus. It should be pointed out however, that gorse growth is not analagous to bracken growth. The expansion of a bracken frond progresses geometrically, with the systematic exposure of new types of structure as the frond matures. Gorse shoots grow apically, and so the amount of foliage for colonisation increases in proportion to the length, while the available area per unit length of shoot remains practically constant. The seasonal increase in "living space" in bracken and gorse is not the same. As a logical extension of Lawton & Schroder's
(1977, 1979) ideas concerning the role of plant complexity in forming
observed patterns of phytophagous insects, Lawton's "living space" theory is very attractive, and there seems little doubt that in the case of bracken it provides a good predictor of insect occurrence. As in gorse, however, the expansion of fronds is closely tied to numerous other events such as falling food quality (Lawton, 1976), and there seems little direct evidence that "living space" per se is the dominant factor involved.
How do the structural and chemicals defenses of gorse foliage affect its use by insects? In the relatively few appropriate studies in the literature it appears that the food quality of most plants declines through the summer months, often as a result of increasing amounts of quantitative or digestibility reducing compounds in foliage (Feeny, 1970; Lawton, 1976).
Such compounds appear to be absent from gorse foliage, or appear in apparently inconsequential amounts. In some plants, highly susceptible
new growth is protected by qualitative defensive compounds which decline
in concentration in late late spring (Lawton, 1976). In gorse this role
appears to be taken by alkaloids which are present in relatively high
concentrations immediately after bud-burst and decline in concentration
along with nitrogen concentration as shoots expand. Such toxins are normally most effective against generalist herbivores (Rhoades, 1979) and
it is interesting that no generalist species appear to attack gorse during
early spring.
Perhaps the most obvious protective devices evolved by gorse as
protection against herbivores are tissue toughness, and spines. There can
be no doubt that spines were evolved in response to grazing pressure, but
by herbivores other than insects. It has been suggested that toughness
of gorse foliage does not form a barrier to foraging insects because the
terminal growing portion (approximately 2-3 cm) of each shoot remains
succulent almost throughout the summer. Such susceptible tissue is more
protected from vertebrate herbivores, however, because it is hidden amongst
the matured spines.
The insects which eat gorse foliage appear to optimise nitrogen uptake.
-This observation was confirmed by the fact that foliage nitrogen content
•appeared to be one of the most important contribution predicting the
observed structure of the community. The sharp decline in foliage nitrogen
content in late spring to a very low level is unusual for a nitrogen-
fixing plant (Mattson, 1980) and is very unlike its close relative broom ^
(J. Riggall, personal communication; see Section 3). As mentioned above
decline in food quality of plant foliage is normally caused by the presence
of digestibility-reducing compounds, but in gorse these are absent. In
this case, lowered food quality is a result of reduced nitrogen metabolism 159.
by the plant. It would be unwise to suggest that this has developed in response to grazing pressure by insects but the observation certainly fulfils the suggestions made firstly by White (1976, 1978) and then by
Moran & Hamilton (1980) that reduction in foliage nitrogen content could evolve by this means. Many features of the gorse fauna (optimal use of the nitrogen available, high degree of specialism and univoltinism, low number and abundance of associated insect species, poor dispersal ability), would all conform to such a view.
How does this fit with Rhoades' (1979) "optimal defense strategy" for
1 plants? Ulex spp conforms to Mattson s (1980) definition of stress-selected species. One of Rhoades' hypotheses was that since resources allocated to defense were those surplus to maintenance requirements, then stressed individuals should allocate fewer resources to defense (Section 5.1). If this is also true at the species level then defense of gorse foliage should be as economical as possible. Quantitative defenses are costly (Feeny,
1976) and these appear to be absent in gorse. Qualitative defenses are cheap, and in gorse foliage are used to protect susceptible and nutritious small growing shoots. This fulfils another of Rhoades' proposals, that defenses should be allocated to the plant parts most at risk, and of most value to the plant. Development of low nitrogen metabolism in foliage would also appear to conform to the concept of optimal defense in a stress-adapted species.
At the beginning of this discussion it was suggested that experiment- ation could be a better approach to isolating the importance of some of the factors mentioned in this section. In Sections 6 and 7 two such experiments are described.
5.8 Summary
1. Four current theories concerning how plants can influence the diversity 160.
and abundance of their folivoares are presented. The data from this study are summarised, general trends are discussed, the results are used to investigate 3 of these theories more closely.
Spider biomass does not appear to influence the structure of the insect community, but is probably partially responsible for low phytophage abundance.
Using linear regression and correlation, shoot length was the best predictor of the seasonal variation in the number of species on gorse
f foliage and for their combined abundance. This was very like Lawton s
(1978) bracken "living-space" theory.
Isoflavone content was the most important predictor amongst the
"chemical" variables. Isoflavone levels are probably associated with flowers and flower-buds, and this correlation was probably fortuitous.
Alkaloids and nitrogen content also contribute.
Massive autocorrelation between independent variables is demonstrated, and the correlation and regression results are re-examined using a multiple regression analysis technique. This showed that the predictive value of shoot length was a result of its many autocorrelates part- icularly nitrogen content, and that living-space per se made little contribution to the regression.
The significance of these results for current theory are discussed, especially the possibility that low foliage nitrogen content may be an adaptation to grazing pressure. SECTION 6
THE EFFECTS OF FERTILISER ON GORSE AND ITS FAUNA
6.1 Introduction
In the previous section it was suggested that the structure of the phytophagous insect community of Ulex europaeus was moulded by several factors, particularly the seasonal variation of foliage nitrogen content, and possibly the amount of new growth available to the fauna. In this section the relative importance of these two factors is investigated experimentally through the augmentation of foliage nitrogen by application of inorganic fertiliser.to gorse plants in a natural habitat.
Prestidge (1980; McNeill & Prestidge, 1982) recently investigated the effects of fertiliser application on the seasonal abundance and species composition of leafhoppers feeding in acidic grasslands. He found that various grasses responded to fertilisation with an increase in the quality of the food available to the leafhoppers, which subsequently increased in abundance. He also showed that fertilisation increased the biomass of food available to leafhoppers, and this also increased the capacity of areas to support large leafhopper populations, especially later in the season.
Finally he showed that each leafhopper species actively sought and utilised plant-parts, patches, or plant species bearing a nitrogen concentration most suited to its physiological requirements. In all three ways, he showed that fertilisation of plants can profoundly affect the species number, abundance, and diversity of the phytophagous fauna feeding on those plants.
Chapin (1980) has recently reviewed the literature concerning the mineral nutrition of wild plants. Whereas plant species adapted to fertile habitats respond to increased nutrient availability by increased growth, 162.
species from infertile sites (such as Ulex spp), respond more by increased nutrient concentration in plant tissue rather than increased growth. Such
"luxury consumption" of nutrients, coupled with low growth rate, appears to be an adaptation to the steady utilisation of limited resources available from the infertile habitat in which the plants grow.
In this experiment an attempt was made to change this stable relation- ship by the application of inorganic nitrogenous fertiliser to Ulex europaeus plants. Section 5 suggested that foliage nitrogen content and possibly plant biomass were important factors moulding the structure of the phytophagous insect fauna of gorse. This experiment was particularly designed to monitor changes in these two plant parameters with fertilisation, and to measure the effects of these changes on the phytophagous insect fauna of gorse.
As with most other legumes, Ulex europaeus has nitrogen-fixing symbiontsin its root nodules. These are particularly active in gorse
(Reid, 1973), and presumably provide the greatest proportion of gorse metabolic nitrogen. It was therefore difficult to predict whether gorse foliage nitrogen levels would rise when nitrogenous fertiliser was added, or whether this would lead to decreased symbiont activity and no change in foliage nitrogen content. In the event, two different fertiliser regimes were tried in successive years, as described in Section 6.2.
6.2 Methods
Two areas of heathland at Yateley Common were chosen (see Section 2 for site description). One was treated with fertiliser while the other acted as a control. The insect fauna and plant growth characteristics in the control area have already been described in Section 2. The treated area (25 m x 50 m) was situated within 10 m of the control plot, and was visually indistinguishable from it. Granular fertilisers were used, and 163.
were broadcast by hand over the treated area once in 1980 and twice in
1981, at the following rates: t 2 1980 5 May "Growmore" (NPK mix 7 :7:7) 30-40 g m"
2 1981 20 March NH.N0 15-20 g m" 4 o3
2 30 April NH.N0_ 15-20 g m~ 4 3
Such rates are commonly used in agricultural systems (Prestidge, 1980) and were considered low enough to minimise any toxic effects on such a loyr fertility system. In effect, 3 times as much nitrogen was applied in 1981 as in 1980. The reasons for this change in treatment are discussed later.
Foliage' samples for nitrogen content analysis were taken at intervals throughout the growing seasons in 1980 and 1981, using the sampling method described in Section 3. Nitrogen content was determined using the micro- kjeldahl technique described in Section 3. In 1981 equal numbers of samples were taken on the same day at each sampling occasion, allowing detailed statistical analysis of the data. Such an analysis was not possible for 1980 data because sample dates and size were not equivalent.
Results obtained are presented in Figures 6.1 and 6.2 and analysed in
Table 6.1.
30 mature gorse shoots were randomly chosen from each area in early spring of 1980 (prior to treatment), 1981 and 1982. These were measured, and the differences resulting from fertilisation are analysed in Table 6.2.
In addition, the growth of new shoots in each area was estimated throughout the growing season of 1980 and 1981, using the same method as that described in Section 2. In 1980, 9-15 samples were taken on each sampling occasion, but in 1981 10 samples were taken on each occasion. The results obtained are presented in Figure 6.3, and analysed in Table 6.3.
The insects occurring on gorse foliage in both areas were sampled at 164.
approximately fortnightly intervals in 1980 and 1981, using the methods already described in Section 4.
Seasonal changes in the abundance of some phytophagous species are presented in Figures 6.4 to 6.7, and an analysis of the differences between
the abundance of insects in the treated as opposed to the untreated area is given in Tables 6.4 and 6.5. The effect of artificial fertilisation on the diversity of the fauna in the two areas is also summarised in Tables
C 6.4 and 6.5. CO <«-{>/«.t>cot U eo^CVJ^cc •
6.3 Results
6.3.1 Effec_ts_ on_se_as_onal_ var^ijitiori _in_N_cont_eiit
The results obtained from analyses carried out in 1980 and 1981 are
shown in Figures 6.1 and 6.2, and comparisons between treated and control areas are made in Table 6.1. Although rigorous statistical comparison was difficult in 1980 because of differences in sampling time and intensity, significant differences in N content were caused by fertilisation in both years.
In Section 3 it was shown that the total and soluble nitrogen content of young foliage was greatest in mid-May, but declined rapidly to below
50% of this level by mid-July in most cases. Generally, this pattern was also seen in fertilised gorse foliage. In 1980, soluble nitrogen levels were vcr.y similar in foliage from both fertilised and unfertilised areas.
Later irs the season there was significantly more soluble nitrogen in fertilised gorse. This analysis was not repeated in 1981.
The seasonal changes in total nitrogen content of foliage on treated and control areas were different in 1980 compared to 1981. Seasonal changes in 1980 are shown in Figure 6.1 and Table 6.1. As with soluble nitrogen content, levels were very similar in early spring, but high levels 165.
Table 6.1 : A statistical comparison of the soluble and total nitrogen
contents found in fertilised and unfertilised gorse foliage in
1980.
Soluble nitrogen content
Unfertilised Fertilised
X SD n X SD n
21 May - - - 4.7 - - -
3 June 5.0 1.7 5 5.7 1.2 6 0.92 NS
15 June - - - 4.0 0.4 4 -
3 July 2.5 0.6 9 3.4 0.3 4 2.81
20 August 1.7 ' 0.4 9 3.3 1.1 8 4.10 ***
Total nitrogen content
Unfertilised Fertilised t
x SD n x SD n
21 May - - 40.3 - -
3 June 39.0 3.6 6 40.7 2.7 6 0.57 NS
15 Jv - - 34.3 2.1 4 - ?e
3 July 28.8 2.3 7 33.9 2.9 4 1.58 NS
20 An gust 20.3 1.6 9 23.8 2.6 8 3.40 ** Figure 6.1 : Seasonal variation of foliage soluble and total nitrogen
content in fertilised and unfertilised gorse, 1980.
(With significance of differences between fertilised and
unfertilised levels) 166.
Soluble nitrogen content
NS * ***
4
mg/g dry wt Total nitrogen content
NS NS **
40
30
20
10
M 167.
of total nitrogen content were maintained in the fertilised foliage until late summer. Since sampling dates and sizes were not equivalent, statistical analysis cannot be more rigorous than that shown in Table 6.1. In general, nitrogen concentration was not significantly higher in fertilised foliage during the period of greatest insect activity, i.e. May and June.
In an attempt to augment foliar nitrogen levels during this period, the fertiliser regime was changed in 1981. Highly soluble NH^ NO^ was applied in late winter, and again several weeks before bud-burst. In this case, the total nitrogen content of fertilised foliage was higher in spring.
The greatest difference between treated and untreated areas occurred in mid-June, but the effects of fertilisation were not carried through late summer as they were in 1980 (see Figures 6.1 and 6.2). Analysis of variance showed that the treatment exerted a highly significant effect on nitrogen content through the season (Table 6.2). t-tests for individual sampling occasion confirmed these differences, though the use of t-tests in this context cannot be regarded as conclusive evidence.
In Section 3 the effects of contamination by fertiliser on the nitrogen content of gorse foliage at WGP was described (see Figure 3.2).
Levels of nitrogen content did not decline in June as they did in other naturally occurring gorse plants, and the response was very similar to that obtained by intentional application of fertiliser in this experiment.
It has also been shown that seedlings of U. europaeus and U. galli contain higher total nitrogen levels in late summer when grown in soil enriched by nitrogenous fertiliser (V. Cowling, personal communication).
6.3.2 Ef_fe£ts on_the_growth of_new_shoots_
There was no significant difference between the lengths of shoots in the two areas prior to treatment (10.29 cm, 11.03 cm, t = 1.03, df = 78,
P = 0.3). After treatment in early spring 1980, new shoots grew faster in 168.
Table 6.2 : Statistical comparison of gorse foliage total nitrogen content
in fertilised and unfertilised plants.
Unfertilised Fertilised t P X SD n X SD n
1A May 32.9 1.9 5 39.7 5.3 5 2.7 *
21 May 37.5 1.6 5 AO. 9 3.0 5 2.2 c. 0.05
1 June 35.6 2.1 5 AO. 0 2.0 5 2.9 *
15 June 30.1 A.7 5 AO.2 2.6 5 A.2 **
9 July 23.3 1.6 5 26.8 A.3 5 1.7 NS
25 July 20.7 1.8 5 20.7 1.6 5 - NS
2 way ANOVA F =38 P < 0.001 Figure 6.2 : Seasonal variation of foliage total nitrogen content in
fertilised and unfertilised gorse, 1981.
(With significance of differences between fertilised and
unfertilised levels) 169.
Total nitrogen content 1981 mg/g dry wt
* 0.05 * # ti- ns ns
V
M 170.
the fertilised plot than in the unfertilised plot (Figure 6.3). Table 6.3 shows that this difference was not significant late in the growing season because of the large variability in shoot length, especially in fertilised shoots. Thirty fully-grown shoots from each area were measured before new growth began in early spring 1981. Shoots collected from the fertilised plot were 30% longer than those from untreated plants (10.68 cm, 14.41 cm, t = 2.47, df = 50, P < 0.05). Preliminary results also suggested that fertilised shoots were more dense than unfertilised shoots (0.099 g dry
1 1 wt cm" compared to 0.078 g dry wt cm" ; t = 2.1, df = 58, P < 0.05). This suggests that in 1980, Ulex europaeus grew for a longer period in the fertilised plot than in the unfertilised plot, finally producing longer shoots on the treated plants.
In 1981, when nitrogenous fertiliser alone was used, the difference in growth between fertilised and unfertilised foliage was not as pronounced.
Fertilised shoots were longer than untreated shoots at every sampling occasion (Figure 6.3), but Wilcoxon's sum of ranks test performed on each csiapling occasion showed that the differences were much less pronounced compared to 1980. In Table 6.3, shoot measurements obtained in 1981 are presented for comparison with the estimates made using the same shoots.
Agreement between estimates and measurements was close. In 1982, 30 fully- grown shoots produced in each area during 1981 were collected and measured.
Again, there was no significant difference between treated and untreated shooLa (13.7 cm, 14.5 cm, t = 0.41, df = 58, P = 0.6). It was assumed that spring addition of nitrogenous fertiliser did not extend the growing season in 1981.
6.3.3 Effect_of_ rt il i_sa_t io n £n__the_ins£ct_ faun£
There were no differences between the lists of species collected from each area. Fertilisation did not appear to attract additional species, and 171.
Table 6.3 : Statistical comparison of median shoot growth (cm) on fertilised
and unfertilised gorse (pooled median of 5 size categories;
1 differences analysed by VJilcoxon s sum of ranks test; 1981
assessment of mean shoot length by measurement also presented).
1980
Unfertilised Fertilised Date P median n median n
3 June 0.80 348 1.48 129 ***
17 June 1.87 306 2.52 118 ***
1 July 2.65 471 3.22 189 ***
15 July 3.56 450 6.00 125 •kick
31 July 5.70 7.35 -
20 August 7.13 8.09
1981
Unfertilised Fertilised
.Date P mean median mean median n n length length length length
14 May 0.50 100 1.78 126 -
21 May 0.78 0.73 214 1.05 0.98 353 •kkk
2*TJune 1.59 2.00 241 1.74 2.16 320 NS
1 5 ,.Iune 2.00 2.32 373 3.25 2.93 343 kk
4 July 4.16 4.12 366 4.56 4.57 372 kk
25 July 4.9 4.85 285 5.97 5.62 335 kkk
zl August 6.9 6.87 199 7.6 7.12 187 NS Figure 6.3 : Growth patterns of fertilised and unfertilised gorse 1980, 1981.
(Figures represent the percentage by which fertilised gorse is
longer than unfertilised gorse. The significance of this
difference by Wilcoxon sum of ranks test is also given)
At the completion of growth
Fertilised Unfertilised t df P
1979 11.03 10.29 1.03 78 0.03
1980 14.41 10.68 2.47 58 < 0.05
1981 14.5 13.7 0.41 58 0.60 172.
1980
10 *** *** *** ***
85 35 22 69 29 14
shoot 1981 length cm.
10 NS ** ** *** N5
34 8 26 11 16
• 4 •
T~
M
i 173.
there was 110 significant difference in the number of species at any stage of the experiment. These findings contrast with fertilisation experiments carried out on acidic grasslands (Prestidge, 1980). Prestidge found that even moderate applications of fertiliser increased the variety of species collected in the treated area.
Fertilisation affected the abundance of gorse insects in varying ways, depending on the fertiliser regime and the feeding characteristics of the insect concerned. Since Sitona regensteinensis overwintered as an adult and laid eggs in spring, too few adults were collected in spring and summer to enable statistical analysis of the response of this species to fertil- isation. The other common root-feeding species, Sitona tibialis was common during this period. The density of adult weevils in the untreated plots was higher, though not significantly different in either year.
Larval densities were not measured, and so no meaningful conclusions can be drawn regarding the performance of root-feeding species on fertilised gorse plants.
Four mesophy11-feeding species were present on sufficient sampling occasions to allow statistical comparison using analysis of variance. In
1980, significantly more A. obsoletum were present in the plot treated with
NPK fertiliser than in the control plot (Table 6.4), largely as a result of slightly higher populations in June and July (Figure 6.4). This difference was not found in 1981 when the numbers collected on the plot fertilised with NH^NO^ were very similar to the control population through- out the year (Figure 6.4). There were no significant differences between populations of the other mesophy11-feeders in either year of the experiment
(Figures 6.5 and 6.6; Table 6.4).
Of the lepidopterous species feeding on Ulex as larvae, only Agonopterix ulicetella was present in sufficient numbers to allow any sort of Table 6.4 : Statistical comparison of differences in abundance (as log (abundance + 1) per sample) between insect species
on fertilised £.nd unfertilised Ulex europaeus (ANOVA).
1980 1981
Grand Grand Grand Grand F attributed F attributed mean mean df P mean mean df P to treatment to treatment control treatment • control treatment
Sitona tibialis 0.52 0.38 3.47 1,140 NS 0.39 0.30 1.5 1,168 NS
Sericothrips stccphylinus 2.46 3.14 30.1 1,140 < 0.001 3.3 3.4 0.66 1,168 NS
Agonopterix ulicetella - - - - - 0.42 0.15 9.0 1,84 < 0.01
Asciodema obsoletum 0.48 0.67 7.9 1,140 < 0.05 1.22 1.24 0.01 1,140 NS
Pachylops bicolor 1.17 1.36 2.4 " 1,112 NS 1.0 0.99 0.01 1,112 NS
Piezodorus lituratus - - - - 0.44 0.82 7.3 1,112 < 0.05
Dictyonota strichnocera 1.17 1.35 2.8 1,140 NS - - - - - Figure 6.4 : Abundance of A. obsoletum in fertilised and unfertilised gorse
1980, 1981.
• • Unfertilised
x x Fertilised 175. Figure 6.5 : Abundance of Pachylops b-icolor in fertilised and unfertilised
gorse 1980, 1981.
• • Unfertilised
x x Fertilised 176.
M J J A S Figure 6.6 : Abundance of Diotyonota strichnoceva on fertilised and
unfertilised gorse 1980, 1981.
• • Unfertilised
x x Fertilised 177. 178.
statistical analysis, and then only in 1981. In this case, significantly more A. ulicetelta larvae were present in the unfertilised plot in 1981
(Table 6.4).
As explained in Section 4, larvae of Ser-icothrips staphylvnus were not recognised in 1980, and the numbers shown in Figure 6.7 represent estimates of adults only (larvae occurred from mid-June to mid-September).
The rise in numbers recorded in September-October represent the emergence of new adult thrips. ANOVA showed that there were significantly more adult thrips collected on fertilised gorse than on unfertilised gorse in 1980.
In fact, there were often twice as many thrips/sample in the fertilised area (Figure 6.7), and this is reflected in the treatment means for the
ANOVA (26.8, 15.0). This species overwinters as an adult, but it is not known whether it remains on gorse over this period, or whether it uses some other overwintering site. Mound et at (1976) recorded macropterous individuals late in the year, which suggests that dispersal to an over- wintering site may occur, while female macropters have been recorded from
May to September. Although no large-scale dispersal was ever observed, these facts suggest that dispersal of females in spring may occur. The observed difference in the density of adult thrips may be the result of host-plant selection in spring, especially since the fertilised plot bore significantly more new growth than the untreated plot by early June 1980.
In 1981, when there was no significant difference in the amount of new growth produced in the two plots, there was also no significant difference in the density of Sevicotbrips staphylinus collected.
None of the remaining foliage-feeding insect species were present in sufficient numbers to make either statistical presentation or pictorial presentation feasible. Instead, the abundance and phenology of all phyto- phagous species (including those described above) has been summarised using Figure 6.7 : Abundance of Serioothrips staphylinus on fertilised and
unfertilised gorse 1980, 1981.
• • Unfertilised
x x Fertilised 179.
insects per 180.
the Simpson-Yule index of diversity. Figure 6.8 depicts the seasonal change in the structure of the total community of phytophagous insects on fertilised and unfertilised gorse in both years. Figure 6.9 summarises only those species which bred on gorse in those years. No statistical analysis of the differences has been attempted, but from Figures 6.8 and
6.9 it is obvious that in 1980 the diversity of insects on unfertilised gorse was consistently less than on fertilised gorse, whereas in 1981 there was no apparent difference. There appeared to be no apparent difference between the total number of phytophagous insects collected in fertilised or unfertilised gorse in either year (Figure 6.10). The discrepancies in diversity shown in Figures 6.8(a) and 6.9(a) must therefore result from differences in the presence and/or abundance of rare species which were not recorded in sufficient numbers to allow more detailed analysis, or from the disproportionate dominance of Serioothriys staphyHnus in 1981 (Figure
6.7).
6.4 Discussion
The constant use of fertilisers in agricultural systems confirm their ability to raise the productivity and food quality of plants. While strongly influenced by the soil-plant milieu and the uptake mechanisms of the plant, application of either nitrogenous or balanced fertiliser to plants normally results in increased biomass through stimulation of cell division and elongation, as well as increased nitrogen concentration in plant tissues (Mattson, 1980). It might be expected that this response would be even more pronounced on very low fertility soils such as Bagshot
Sands. It is interesting therefore, that in both 1980 and 1981 gorse showed only slight responses to the applications of fertiliser in early spring. The fertiliser application rates chosen were of the same order as those used in agricultural systems. Using the same rate of nitrogenous Figure 6.8 : Seasonal changes in the community structure of all phyto-
phagous insects living on fertilised and unfertilised gorse
1980, 1981.
» 181. Figure 6.9 : Seasonal changes in the community structure of phytophagous
insects which reproduce on fertilised and unfertilised gorse
1980, 1981. 182. Figure 6.10 : The number of phytophagous insects per sample from fertilised
and unfertilised gorse 1980, 1981. 183.
YC Ue
Insects per sample fertiliser, Prestidge (1980) was able to raise total leaf nitrogen content in Holous lanatus by 39.7% and 17.9% in 1978 and 1979, while using an NPK fertiliser at a similar rate to that used in this experiment, N content rose by 45.9% and 22.1% (Table 6.5). Similarly, N fertilisation increased the growth rate of Hotcus lanatus and significantly increased the standing
1 crop. Prestidge s (1980) results suggested that the presence of phosphorus and potassium in a fertiliser mixture synergised the utilisation of the nitrogen component of an NPK fertiliser and resulted in greater nitrogen content in the plant. When such a mixture was applied to gorse in 1980, there was no immediate increase in foliage nitrogen concentration (see
Figure 6.1), but growth began earlier and was somewhat faster under this fertiliser regime. As seen from Figure 6.3, fertilised growth was between
20 and 70% longer in May, June and July. Despite the similarity in nitrogen concentration in the foliage, the total amount of nitrogen accumulated in new growth of gorse plants per unit area was therefore gneaLer in the fertilised area than in the unfertilised area. The rate of
in fertilised gorse slowed later in the season, and at this stage, the concentration of nitrogen in new foliage became significantly greater in fertilised foliage.
In 1981, a larger amount of N was added to the fertilised site, over a longer period of time, but without the addition of phosphorus or potassium. Gorse plants responded with significantly increased nitrogen content early in the season which declined to equality later. There was no appreciable difference in shoot length at any stage in the season (Table
6.3), as confirmed by measurement of fully grown shoots in spring 1982
(Table 6.3). In 1981 therefore, as in 1980, more Nitrogen was accumulated in the fertilised site, but in this case by virtue of increased concentration in the foliage rather than by increased biomass of new tissue. There are 185.
Table 6.5 : Comparison of fertilisation effects on Holous lanabus (Prestidge, 1980) and Ulex
europaeus.
(Figures in parentheses represent % increase over the control. Other figures are annual
me an s)
Foliage nitrogen content (mg g
Fertiliser treatment
Control N .NPK -1 300 Kg Ha -1 300 Kg Ha
Holcus lanatus 1978 19.6 27.4 (39.7) 28.6 (45.9) 1979 23.5 27.7 (17.9) 28.7 (22.1)
Ulex europaeus 1980 29.4 32.8 (11.6) 1981 30.0 34.7 (15.7)
2 Foliage biomass (g m or cm)
Fertiliser treatment
Control N NPK 300 Kg Ha 300 Kg Ha -1
Holcus lanatus 1979 709 907 (27.9) 1744 (146)
Ulex eruropaeus 1980 3.8 4.8 (26.3) 1981 3.1 3.4 (9.7)
Insects
2 Holcus leafhoppers 1978 (no. m~ ) 59.8 59.7 (0) 195.4 (227) 1979 283.1 260 (-8.2) 1143.9 (304)
Ulex phytophages 1980 (no./sampling occasion) (25-30) 1981 (0) 186.
no data available to calculate the actual amount of nitrogen accumulated per hectare after each of the treatments, and so this interpretation must remain untested.
The effects of fertilisation on the insect fauna of Ulex europaeus appear to be similar to the effects on the plant itself. At first glance, the effects appear to be minimal, with few significant differences in the population density of each insect species (Table 6.4). As with the plant data discussed earlier, consideration of insect abundance on an area basis can lead to a different interpretation.
The insect sampling method employed yielded results expressed as abundance per 200 g fresh weight of foliage. (This data can also be expressed as abundance per shoot cm.; Brown, 1981). Since the amount of green foliage on Ulex europaeus plants increased by approximately 25% in the fertilised area in 1980, the 200 g foliage sample represented a smaller proportion of the total amount of green foliage than the equivalent sample on the control area. If the fertilisation treatment had no effect on the total number of insects living in each area, then in 1980, dispersal of insects through the available green foliage would result in a reduction in the density of insects per sample in the fertilised area compared to the unfertilised area.
This could not be demonstrated in comparing the abundances per sample of the more common species, with the exception of S. tibialis
(Table 6.4). Similarly, the total number of phytophagous insects collected on each sampling occasion was quite similar (Figure 6.10). This suggests that the total number of phytophages inhabiting the fertilised area in 1980 was greater than the total number inhabiting the unfertilised area. Figures 6.8 and 6.9 show, however, that the diversity of the fauna was reduced in the fertilised plot. Whether this resulted from changes in 187.
the equitability of fauna, or through fewer species collected was not determined.
In 1981 there were few differences between the density of individual species in the fertilised area compared to the control area, the total numbers of phytophages caught (Figure 6.10), or the diversity of the fauna
(Figures 6.8 and 6.9). There was also no appreciable difference in the biomass of green foliage available to the phytophagous insects. In this case therefore, the insect samples were comparable, since they sampled the % same proportion of the available habitat.
As with plant biomass and foliage nitrogen content, the response of gorse insects to fertilisation of their host plant was minimal compared with the response of grassland leafhoppers to fertilisation of Holcus lanatus (Prestidge, 1980). Table 6.5 shows that the mean number of leaf- hoppers collected in the NPK fertilised areas on each sampling occasion were 2-3 times higher than the numbers collected in the control areas.
-1 Nitrogenous fertilisation had little effect at the rate of 300 Kg Ha .
In comparison, the gorse fauna was estimated to be only slightly higher in
NPK fertilised areas, while nitrogenous fertiliser had little effect on
1 insects at 300 Kg Ha" .
What makes Ulex europaeus less susceptible to manipulation by fert- ilisation than the acidic grassland system described by Prestidge (1980)?
In the first instance, Ulex spp have nitrogen-fixing root symbionts (Reid,
1973). Application of inorganic nitrogen (in 1981) may have inhibited fixation of atmospheric nitrogen by symbionts, thus maintaining the net nitrogen uptake by the plant at a similar level. Conversely, addition of phosphorus and potassium (in 1980) may have enhanced the activity of nitrogen-fixers, and this may account for the significant accumulation of gorse foliage nitrogen in late summer 1980 (see Table 6.1), and the growth response of the plant 188.
in that year.
Ulex europaeus and other species of the genus characteristically inhabit poor, acidic soils, and are highly calcifugous (Zwolfer, 1962).
Their highly infertile surroundings strongly suggest that Utex spp are'
"stress-selected" species, adapted to coping with harsh conditions (Mattson,
1980). Among the characteristics of such species are inherently slow growth rates, a relatively small growth response to flushes of higher nutrient availability (such as fertilisation), and low nutrient losses be- cause of evergreenness and slow rates of tissue production (Chapin, 1980).
It seems logical to assume that such plants support insects following comparable strategies. Thus phytophages can be characterised by feeding- specialism, univoltinism, low inherent rate of increase, low density, and demonstrating behavioural adaptations to optimal utilisation of scarce plant-borne resources. The characteristics of insects associated with
"stress-selected" and "non-stress-selected" plants have recently been discussed with particular reference to insects of acidic grasslands and acidic hp/rthland by McNeill & Prestidge (1982), and with gorse in particular by Hill (1982).
6.5 Summary
1. The effects of two fertiliser regimes on the growth and foliage nitrogen
content of Ulex europaeus were examined in two different years. In
1980 an area of gorse was treated with an NPK fertiliser, while in 1981
the same area was treated twice with ammonium nitrate.
2. Gorse responded to NPK fertiliser treatment by significantly increased
growth, but foliage nitrogen concentration was not appreciably greater
compared to the control plants. With ammonium nitrate fertilisation,
gorse foliage nitrogen content increased significantly, but growth did 189.
not. Iri both treatments added nitrogen was taken up by gorse plants,
but expressed itself as increased shoot growth in the presence of
phosphorus and potassium, but increased foliage nitrogen concentration
in their absence.
3. With few exceptions the abundance of common folivores when expressed as
insects per 200 g of foliage was not changed by either treatment. The
total number of phytophages also remained the same, though the diversity
of the fauna was reduced in the area fertilised by the NPK fertiliser.'
4. Interpreted as insects per unit area it follows that there were more
phytophagous insects in the NPK fertilised area than in the control area
because the amount of green foliage was significantly greater.
5. In general, gorse showed very little response to fertilisation, and
there was a correspondingly small response in the insect fauna to
increased "living space" in 1980 or foliage nitrogen content in 1981.
Results are compared with a similarly treated grassland/leafhopper
system. It is suggested that the response of the host-plant was
typical of a stress-selected plant, and that insects associated with it
seem closely tied to the life history strategy of the host-plant. 190.
SECTION 7
THE FEEDING CHARACTERISTICS OF ONE GORSE SPECIES,
AGONOPTERIX ULICETELLA
7.1 Introduction
In both Sections 5 and 6 it was shown that the community structure of
the phytophagous fauna attacking gorse foliage was correlated with the
nitrogen or protein content of the foliage through the season. It was
suggested that on gorse, which was not protein-rich, most phytophage
species used the only period of high foliage protein content for repro-
duction and growth. The experiment described in this section was designed
to test this hypothesis by looking at the performance of larvae of one
of those phytophages when fed on gorse foliage of different composition
from that normally encountered in the field.
The feeding performance of insects has been measured in a number of
ways (Waldbauer, 1964, 1968; Mattson, 1980; Scriber, 1979; Scriber &
Slansky, 1981), and the associated collection of definitions and terms
reflects this. In the following discussion of published information, these
are explained as they are encountered, and equivalent results from different
experiments are compared. The terms used in the experiments described here
are defined in Section 7.2.
Most of the literature relating to this field concerns the physio-
logical performance of individual species on various foods. Recent papers
however, have turned their attention more to the ecological significance
of phytophagy.
Slansky & Feeny (197 7) studied the performance of fifth instar Pieris vapae larvae on brassicas of different foliage nitrogen content. They measured feeding rates and rates of nitrogen accumulation (NAR) of larvae fed on the different plants, and proposed that herbivores adjust their
intake of food to the lowest rate which maintains the rate of nitrogen
accumulation at a maximum. This is achieved by such methods as variation
of development time or by variation of food consumption rate.
Scriber (1977) has pointed out many cases where the water content of
foliage can limit the availability and efficiency of utilisation of food, particularly nitrogenous components of food. Scriber & Feeny (1979) have
generalised this idea by relating the water content of foliage to the
growth form of the plants involved. They found that lepidopteran larvae
feeding on high-water content herbaceous plants were more efficient than
those feeding on shrubs or trees, though correlates of water content such
as leaf toughness and leaf nitrogen also contributed to the observed
difference.
Schroeder & Maimer (1980) studied the total hymenopterous and lepid-
opterous phytophagous fauna on black cherry. Since the efficiency of
conversion of digested material into larval biomass remained constant in
different species collected throughout the season, they postulated that
each species was temporally adapted to the food which it found at the time when it was feeding. What controlled the time at which each species was
feeding was not nitrogen quantity, could be affected by nitrogen quality,
but was probably mediated by numerous factors including abiotic and biotic mortality. A similar theory has been promoted by Lawton & McNeill (1979).
In his study of the effect of phenolic substances on the feeding of winter moth Qpevophtera brumata, Wint (1979) hatched larvae out of season
and compared their performance on mature leaves of 5 natural host-plants
as opposed to the new leaves which were the normal diet. In general he
showed that feeding LV_ larvae on mature leaves caused considerable
reduction in overall feeding efficiency, larval survival, and fitness as 192.
measured by pupal weight. He also showed differences in performance be- tween larvae fed on different tree species. From this information he confirmed that successful development of winter moth was closely dependent on the synchrony of hatching with the availability of new leaves on the
5 trees (Feeny, 1970).
From these studies it was possible to predict that given the rapid seasonal decline in foliage nitrogen content described in Section 3, gorse phytophages should perform best when fed their natural food from the correct time of year, since feeding at that time would optimise species fitness by one means or another.
The experiment described in this section was therefore designed to test whether the relationships described in Sections 4 and 5 between phytophage performance and seasonal variation in host-plant quality could be seen in the detailed feeding strategy of an individual species.
The gorse phytophage chosen was the oecophorid moth Agonopterix ulicetella the commonest lepidopteran on gorse. Field studies showed y that A. ulicetella hatched and developed at the time of year when nitrogen levels were at their peak, and pupated just as protein content reached its lowest concentration. Lepidoptera make good subjects for feeding trials of this type, and there were many similar studies with which to compare the results obtained (e.g. Scriber & Slansky, 1981).
A. ulicetella larvae were reared out of their normal season and the performance of fifth instar larvae fed on fresh, natural food was measured on 4 occasions at approximately 3-weekly intervals in spring and summer
1981. The performance of larvae was monitored in three ways:
(i) Individual fitness (e.g. larval and pupal peak weight, nitrogen
content and water content.
(ii) Relative daily measures of growth, food consumption, and 193.
nitrogen accumulation corrected for larval weight.
(iii) Standard feeding efficiency measurements as defined in Section
7.2.
7.2 Methods
Approximately 200 eggs laid by 20 Agonopterix ulicetella females in
one week were divided into 4 batches and stored at 10°C with 6:18 hours
short day photophase. At intervals, batches of eggs were removed from t storage and incubated. Storage and incubation details for each batch are
given in Table 7.1. Larvae hatched synchronously and were transferred to
a 30 x 20 cm plastic bag containing excess fresh gorse foliage. Every 4
days this food was replaced, until larvae reached late fourth instar when
they were transferred to individual petri-dishes lined with filter paper.
Petri-dishes were stored in plastic bags to minimise water loss, and fresh
food and drops of water were added daily. At the last moult, new fifth
instar larvae were weighed and transferred to petri-dishes with a weighed
amount of food as already described. At regular intervals (detailed
below) larvae were transferred to new petri-dishes with weighed food, and various measurements were made. All rearing was carried out at 20°C and
18:6 hours, long day photophase. All gorse foliage used in this experiment was obtained from a single 7 year old U. europaeus bush growing at Silwood
Park ( ) on sandy soil in a disused field near a public footpath.
To avoid any effects of shoot toughness or water content, only the terminal
3 cm of any shoot were used. It was shown in Sections 2 and 3 that these remained constant during the period of this experiment.
It was assumed that the length of cold storage did not affect perform-
ance in fifth instar, though mortality before LV_ was high in treatments 3 and 4. Treatment 4 eggs could not be retarded longer than July 8, and Table 7.1 : Incubation, storage, and rearing details for each treatment.
Approx. date Days in Pupal moult Treatment Hatched LV Moult eggs laid cold storage
26-30 May 1 13 April 0 23-24 April 15-18 May
2-6 July 2 4-7 May 15-18 31 May 23-27 June
20-23 July 30 July - 1 August 3 7-15 May 30-37 24 June
5-8 August 15-17 August 4 7-15 May 53-62 7-8 July hatched in cold store. In this case, early LIV larvae were reared at 10°C
for 5 days to retard development, and measures of larval duration etc.,
have been modified accordingly. Feeding and weighing of larvae, grass and
food were carried out at 3 or 4 day intervals in treatment 1, to minimise
disturbance of larvae. Much information regarding day to day variation in
the parameters measured was lost using this method, so in treatment 2 measurements were made every two days and corrected to give daily estimates.
In treatments 3 and 4, daily measurements were made.
At the beginning of each experiment, and at the intervals described
above; the fresh weight of each larva and the food offered to it were measured, remaining food and frass were freeze-dried and weighed, water
and nitrogen contents of all components were measured. The water content
of LV larvae was only determined once (87.4%) and this figure was used
universally thereafter. This figure agrees well with Scriber's figures
for lepidopterous larvae in general (Scriber, 1977). Fresh and dry weights
of pupae were also measured, along with pupal nitrogen content.
All material was dried using an Edwards freeze drier and all nitrogen
anal>oes using a micro-Kjeldahl technique (Bradstreet, 1965; Varley,
1966),. All weighing carried out on a Torbal electronic balance weighing
to O-lvmg.
The measurements described above allowed compilation or calculation
of the results shown in Table 7.2.
Measurement of consumption, assimilation and egestion for individual
larvae, and the N content of each component allowed the calculation of the
following dry weight efficiency coefficients for the fifth instar (Scriber,
1977; Wint, 1979).
Overall Assimilation _ Food ingested (mg dry wt) - Faeces (mg Efficiency AE . dry wt) Food ingested (mg dry wt) 196.
Efficiency of Conversion Peak dry wt biomass gained in LV (mg of Ingested Food EC1 dry wt) Food ingested (mg dry wt)
Efficiency of Conversion Peak dry wt biomass gained in LV^ (mg of Digested Food ECD dry wt) Food ingested (mg dry wt) - Faeces (mg dry wt)
Nitrogen Utilisation Efficiency N ingested (mg dry wt) - N in Faeces NUE dry wt) N ingested (mg dry wt)
EC1 AE x ECD
Ecological efficiencies for larvae in each treatment are shown in
Table 7.3.
In addition, the following measures were made on a daily basis.
Relative Consumption Rate Food ingested (mg dry wt)/mg larval RCR dry wt/day
Relative Growth Rate RGR Biomass gained (mg dry wt)/mg larval dry wt/day
Relative Nitrogen Accumulation N gained (mg dry wt)/mg larval dry Rate RNAR wt/day
Th.ese are summarised in Table 7.4 and Figure 7.1.
Some of the measurements were derived from treatment means rather than individual data points, and these proximate values are indicated by an psterisk.
7.3 Results
7.3.1 ^xpe^iment a_l_mon_it or inj*
During each of the trials certain common parameters were monitored to confirm consistency between treatments. The results obtained from some of 197.
Table 7.2 : Comparison of components in each treatment.
(Different letters denote significant difference by the GT2
Multiple Range Test)
Treatment
1 2 3 4
Nitrogen content of mean 29.9 a 29.5 a 27.9 a 30.9 a gorse foliage S.E. 1.6 0.7 0.9 0.7
n 5 5 10 14
Nitrogen content of mean 29.1 a 24.9 a 22.1 a 27.3 a frass S.E. 1.5 0.8 2.3 0.7
n 18 25 10 52
Water content of mean 75.9 72.6 a 72.7 a 72.9 a food S.E. 2.5 0.7 1.0
n 3 12 10 198.
these are shown in Table 7.2.
This experiment was designed to test the hypothesis that falling foliage nitrogen content affected insect performance, but on analysis, there was no significant difference in the nitrogen content of gorse foliage supplied to any of the treatments. Over the same period of time the nitrogen content of gorse foliage growing in a natural habitat at
Yateley Common declined by 50% (see Figure 3.1). The significance of this to the results obtained in this experiment is discussed later.
*
The nitrogen content of the frass produced from day to day was the same in each treatment. As expected, the water content of food provided was constant throughout, overcoming the potential difficulties discussed by Scriber (1977).
In all respects conditions provided in each treatment appeared s i Tii i. lair.
7.3.2 I^h^t^phaj|e_qu_a_lit_y
The quality or fitness of individual insects in each treatment was estimated using a number of measurements, including weight and protein content of larvae and pupae, and duration of larval stages (Table 7.3).
The duration of larval development in treatments 1 and 2 was signi- ficantly shorter than in treatments 3 and A, though there was no difference between treatments 1 and 2 or between 3 and A. There were no significant differences in the duration of the fifth instar between any treatments.
Larvae from treatments 3 and A were slightly heavier than those from
1 and 2 at the LIV/LV moult, but not significantly so. Weight changes within the fifth instar are shown in Figure 7.1. Larvae from later treat- ments approached pupation rate at a slow rate, while larvae from earlier treatments achieved this quite early in the instar.
Pupae produced from treatments 1 and 2 were significantly heavier than 199.
Table 7.3 : Measurements of parameters reflecting insect quality in each
treatment.
(Different letters denote significant difference by the GT2
Multiple Range Test)
Treatment
Duration of larval mean 31.9 a 31.9 a 37.3 b 37.0 b development (days) S.E. 0.4 0.2 0.2 0.3' n 23 25 14 14
Duration of LV mean 9.2 a 8.8 a 9.6 a 9.1 a S.E. 0.2 0.2 0.2 0.2 n 24 25 14 • 14
Fresh weight at LIV/LV mean 20.7 a 19.8 a 20.0 a 18.3 a S.E. 0.7 0.5 0.9 0. 6 n 18 30 14 15
Pupal dry weight mean 9.6 a 10.0 a 7.8 b 7.8 b S.E. 0.4 0.3 0.5 0.4 n 25 22 10 10
Water content of pupa mean 76.4 a 76.4 a 80 a 78.2 a
S.E. - - - - n 25 8 9 10
Protein content of LIV/LV mean 530.6 a 612.5 b 662 786.3 c
(mg/g dry wt) S.E. 20.0 23.1 - 13.1
n 3 3 — 4
Protein content of pupa mean 646.9 a 705.0 a 672.5 a 738.1 a (mg/g dry wt) S.E. 31.3 16.9 37.5 46.3 n 10 10 10 10 Figure 7.1 : Growth of LV_ Agonopter-ix ulicetella larvae - treatments 1-4.
(Bars represent standard errors) 200.
mg fresh
wt.
2 4 6 8
Day of fifth instar 201. those produced but the water contents of pupae were not significantly different from 3 and 4. There were no significant differences in pupal weight between treatments 1 and 2 or between treatments 3 and 4 .
There were no significant differences between the protein content of pupae in each treatment. In larvae moulting to LV however, those in treat- ment 4 contained a significantly higher proportion of protein than those in treatments 2 and 1. The level in treatment 2 was significantly higher than in larvae from treatment 1, and treatment 3 also fitted this pattern.
7.3.3 Dail^_ j^arva.l_p£rf_ormanc_e
From daily or interpolated measures of growth, consumption and egestion, daily changes .in relative growth rate (RGR), relative consumption rate (RCR), and relative nitrogen accumulation rate (RNAR), were calculated, and these results are summarised in Table 7.4 and Figure 7.2. Only treat- ments 2-4 can be considered here because measurements of treatment 1 larvae were only made at 4 day intervals.
Rates of consumption, growth and nitrogen accumulation were highest during days 1-3 of the fifth instar and declined towards the end of the instar. In treatment 4, consumption and growth were maintained for longer than in treatments 2 and 3, suggesting that this was a poorer diet.
Feeding in treatment 4 also appeared to be more erratic than in the other treatments.
On days one and two the RCR of larvae in treatment 3 was significantly lower than in the other two treatments, and this was reflected in the RNAR measurements for those larvae. Re-examination of the original data showed that ingestion figures for day one and day two were underestimated due to inefficient drying of the food remaining after larval feeding. This anomaly therefore has no biological significance.
Larvae in all treatments grew at a similar rate, though in treatment 202.
Table 7.4 : Daily comparison of larval performance during LW in Treatments
2-4.
(* denotes that results are derived from interpolated data)
Treatment
2 3 4
Relative consumption rate Day 1 7.10 3.21 5.5 (mg food consumed/mg mean dry wt 2 * 5.38 3.65 6.6 of LV/day) 3 4.17 3.54 3.9 4 * 3.67 2.85 4'. 82 5 2.56 2.39 2.27 6 * 1.69 2.33 2.17 7 0.78 0.11 0.76 8 0 0 0.8 9 0.02
Relative growth rate _ Day 1 0.51 0.44 0.31 (mg/mg mean dry wt of LV/day) 2 0.44 0.25 0.31 3 0.21 0.22 0.21 4 0.12 0.07 0.13 5 0.01 0.01 0.05
6 - 0.05 - 0.08 0.04
7 - 0.05 - 0.04 0.05 8 0 - 0.04 0.06 - 0.09
Relative nitrogen accumulation Day 1 130 160 120 rate 2 * 90 150 110 (mg/g mean dry wt of LV/day) 3 50 40 70 4 * 40 30 100 5 20 40 27 6 * 10 20 26 7 10 0 10 8 0 0 0 Figure 7.2 : Daily larval performance of IV Agonopterix ulicetella.
• • Treatment 2
x x " 3
o o " 4
A. Relative nitrogen accumulation rate,
(mg N/g larval dry wt/day)
RNAR
B. Relative consumption rate.
(mg dry wt/g larval dry wt/day)
RCR
C. Relative growth rate.
(mg dry wt/g larval dry wt/day)
RGR 203.
RNAR
RCR
RGR
2 4 6 8
Day of LV 204.
4 growth was significantly retarded in day 1, and larvae in treatment 2
grew significantly faster in day 2.
In general, however, the performance of larvae in all 3 treatments
from day to day were similar.
7.3.4 St ad iafeed in^ ef_f icji.encies
"Ecological efficiencies" measure the efficiency with which an
organism can convert ingested biomass to production.
Most of the efficiencies recorded here were based on measurements of'
total consumption and egestion for the fifth instar (Table 7.5). There were no differences between amounts of faeces produced by larvae in each
treatment, but larvae in treatment 3 consumed significantly less foliage
than those in treatments 1 and 2 or in treatment 4. This difference
probably resulted from the serious underestimation of consumption in days
1 and 2 of the experiment as already described. Fifth instar RGR was also
significantly different in treatment 3. Since no component of consumption
is involved in the calculation of RGR, it is possible that the observed
results for treatment 3 were valid. They are therefore discussed here.
It follows, however, that values for the results calculated using total
consumption in treatment 3 may be underestimated, i.e. AE, ECD, EC1, NUE,
RCR and RNAR (Table 7.5).
The assimilation efficiency of LV larvae in treatment 3 was signi-
ficantly lower than those of the other treatments. ECD was significantly higher in treatment 3 but EC1 was not. In all other respects AE, ECD and
EC1 for different treatments were similar. The NUE for treatment 3 was also lower than in the other 3 treatments, but not significantly so.
With the exception of treatment 3, there appears to be little difference between the overall efficiency with which larvae accumulate biomass and nitrogen from food at different times of the year. 205.
Table 7.5 : Measurement of ecological efficiencies for fifth instar in
treatments 2-4.
(Different letters denote significant differences by the GT2
Multiple Range Test)
ireatment
1 2 3 4
Food consumed in LV mean 94 .6 a 108.0 a 73.5 b 101.2 S.E. 4 .0 4.7 3.8 2.9 ' n 24 23 13 14
Weight of frass produced mean 48 .6 a 59.2 b 50.2 a 44.8 in LV S.E. 1 .6 1.1 1.2 1.8 n 23 21 10 12
Relative consumption mean - 2.49 a - 2.51
rate for LV S.E. - 0.11 - 0.21
(mg dry wt consumed/mg n - 22 - 13 mean LV dry wt/day)
Relative growth rate for mean - 0.095 a 0.087 b 0.093
LV S.E. - 0.003 0.001 0.002
(mg dr^ wt gained/mg n - 22 13 14 mean LV dry wt/day)
Relative nitrogen mean - 42.1 a 21.0 b 51.6
accumulation rate S.E. - 3.0 2.5 2.99
(mg N/g LV larval dry n - 20 10 13 wt/day)
Assimilation efficiency 47 .7 a 46.5 a 37.1 b 56.1 AE
Conversion efficiency 3.5 a 3.8 a 4.6 a 3.7 for ingested food EC1
Conversion efficiency 7.4 a 8.3 a 13.3 b 6.3 for digested food ECD
Nitrogen utilisation 51.8 a 54.9 a 45.8 a 61.3 efficiency NUE 206.
The relative activity rates shown in Table 7.4 were calculated from daily measures and so could not be obtained for treatment 1, where measure- ments were made at 4 daily intervals. Apart from treatment 3, where RGR and RNAR were significantly lower than in the other two treatments, all relative measures were similar. RNAR in treatment 3 was calculated from consumption figures, and therefore may have suffered from the bias already described. RGR was also significantly lower in treatment 3, and this had no component of consumption. This may suggest that other differences seen in treatment 3 were also valid. If this was so, the quality of gorse foliage presented to those larvae must have varied in some way for a short period of 3-4 weeks in summer. There was no evidence of this in measured parameters.
The values for relative activity rates and ecological efficiencies obtained in this experiment are directly compared with a number of other studies in the discussion.
7.4 Discussion
This experiment was designed to test the hypothesis that the need to optimise food and particularly nitrogen utilisation influenced the seasonal occurrence of Agonoptevix uHcetefla larvae, and by inference, the remainder of the gorse phytophagous fauna. The nitrogen content of the food presented to test larvae proved to be constant in the four treat- ments, despite the fact that the nitrogen content of foliage collected from natural gorse habitats over the same period declined by almost 50%
(Figure 3.1). Because nitrogen content did not decline in the course of the experiment, the original aim could not unfortunately be achieved. All foliage used in this experiment was obtained from an isolated bush growing in rough pasture near a footpath. The maintenance of 3% nitrogen content in the foliage was probably directly related to the relatively high 207.
fertility of the area, and possibly to fouling by dogs. A similar response can be seen in Figure 3.2 where the equilibrium nitrogen concentration of a natural gorse population was raised by the accidental application of a balanced fertiliser. This response was also seen in the fertilisation
experiment described in Section 6.
For comparison of ecological efficiencies and rates, the dubious results obtained from treatment 3 have been ignored for reasons mentioned
earlier.
Since the quality of the food as measured by nitrogen content appeared
to remain constant, it was not surprising that there were no significant differences between treatments 1, 2 or 4 in any ecological efficiency or rate term. It is generally accepted that spring foliage is of higher quality as a food than summer foliage. This has been the basis of a number of studies including those mentioned in the introduction. In most cases, decreasing food quality has resulted in lowered AE and ECD and an
increase in NUE (Mattson, 1980; Slansky & Feeny, 1979).
It is therefore tempting to suggest that when nitrogen content was constant, water content was high, and leaf toughness was low, then larval performance was identical. This was true for rates and efficiency of
feeding, but there were large differences in the quality of larvae and pupae in various treatments.
Those larvae fed foliage collected later than the normal larval period fed longer to achieve the weight required for the final moult, reached a lower peak weight in the fifth instar and produced lighter and therefore "less-fit" pupae (Wint, 1979). Early instar larvae contained
less nitrogen by dry weight at the LIV/LV moult when fed on early-season
foliage as compared to later season foliage, and yet the dry weight of
larvae did not vary significantly. There are two possible explanations 208. for this imbalance;
(1) relaxation of a block of nitrogen uptake with time, though this
is unlikely since NAR was not significantly different between
treatments 2 and 4;
(2) some other component of larval biomass, such as fat content, was
reduced with time, either by reduction in the absolute amount in
the food, or by an increase in assimilation inhibition through
the season.
These results suggest that the critical phase in the feeding of A. ulicetella may well be much earlier than the fifth instar. The develop- ment time between the LI and LV larval stages at 20°C was approximately
20% longer in treatments 3 and 4 than in earlier treatments which confirms this view.
Throughout the growing season, the nitrogen content of gorse foliage is low compared to many plants, especially herbs, but nevertheless falls within the normal bounds for angiosperm leaves. It is interesting there- fore to compare the feeding efficiencies df the gorse-feeding specialist
Agonopterix ulicetella with those of other Lepidoptera. Mattson (1980) has reviewed the recent literature. The AE of 40% reported in this experiment appears to be an average figure, since 20% AE is typical of nitrogen-impoverished foliage, and 60% is regarded as high.
In general most insects feeding on shrubs have an EC1 of between 10 and 20%. The EC1 of A, ulicetella is extremely low at 3.5-3.8% as is the
ECD at 6.3-8.3%. Gorse therefore appears to be a very difficult plant to utilise as food, even by such specialists as A. ulicetella. As a comparison,
Fox & Macauley (1977) recorded ECl's of 4-17% for Paropsis larvae on
Eucalyptus spp, and Wint (1979) recorded ECl's of 5-11% for Operophtera brumata larvae on 5 species of trees. Larvae of A. ulicetella consumed up 209. to 20 times their own peak weight during the fifth instar, but the recorded growth rates were very low (0.09 mg/mg/day). Nitrogen utilisation efficiency appeared to be relatively high (51.8-61.3%) compared to those found by Schroeder & Maimer (27-57%), by Slansky & Feeny (1979) for Pieris
larvae (32-59%) and even by Scriber & Feeny (1979) for papilionids and bombycoids (34-88%), NAR was also relatively high. The accumulation of nitrogen either appears to be a priority over the accumulation of biomass as measured by ECD, or a large throughput is required to obtain some unknown limiting nutrient.
The comparisons drawn above between different studies can only be regarded as approximate, -since authors use different methods for determining
the larval weight used to calculate their indices.
In conclusion, the performance and success of fifth instar Agonopterix ulicetella larvae appeared to be reduced when fed on more mature gorse foliage as compared with their performance on young foliage. The reason did not appear to be reduction in the absolute amount of nitrogen present in the-foliage, but may have related to its quality (McNeill & Southwood,
1978). Whatever the mechanism, food quality affects the.performance of
A. ulicetella larvae.
7.5 Summary
1. Though the aim of the experiment was to investigate the effects of food
nitrogen content on larval feeding, analysis of the food used at the
end of the experiment showed no significant difference between nitrogen
content of food in any treatment. Nitrogen content of frass and water
content of foliage used were also constant.
2. Larval development was significantly longer in treatments 3 and 4,
though the duration of the last instar was not. 210.
3. Percentage protein content of pupae was not significantly different be-
tween treatments, but the protein content of larvae at the LIV/LV
moult was much lower in treatment ascending the maximum level in treat-
ment 4. This rise in the proportion of protein may be associated with
a decline in another body component such as fat but the exact reason
was not determined.
4. Mean pupal dry weight, and hence fitness, was significantly reduced in
treatments 3 and 4.
5. Daily relative growth rate, relative consumption rate and relative
nitrogen accumulation rate were similar between treatments, though there
was an indication that larvae in treatment 4 accumulated N and biomass
for a longer period than larvae in the other treatments.
6. Efficiency of conversion of ingested food (3.5-3.8%) was very low
compared with other studies, as was the efficiency of conversion of
digested food (6.3-8.3%). Approximate digestibility was relatively
high (40%). Growth rates were also low (0.09-0.1 mg/mg/day). Nitrogen
utilisation efficiency was quite high (51.8-61.3%). There were no
significant differences between the ecological efficiencies measured in
different treatments.
7. Though there are some anomalies in the data which make interpretation
difficult, mature foliage does appear to be a less acceptable food than
new shoots. 211.
SECTION 8
CONCLUSIONS
The data collected in the course of this study have been presented and discussed at the end of each appropriate section, and in Section 5.6 its relevance to current theory has been considered in detail. The observed relationships between the insect fauna attacking gorse foliage and the amount of foliage "living space" did not support Lawton's (1978) theory » that plant complexity played a dominant part in determining the number of insects which inhabit gorse foliage, though in this respect gorse is very different from bracken. Similarly, secondary chemistry and other defensive properties of foliage did not seem to exert a dominant effect on the timing of foliage attack. There was some evidence that the low concentration of nitrogenous compounds in gorse foliage was probably the dominant influence, and may have evolved as a response to predator grazing (Moran
& Hamilton, 1980). This was not inconsistent with the optimal defense theory of Rhoades (1979).
Ulex europaeus (along with other Ulex species) has proven to be a most unusual plant. It bears many of the attributes of a stress-adapted species, including evergreenness, slow metabolism and growth rate, and reduction in leaf area (Mattson, 1980). All of these appear to be adapt- ations to survival, and exploitation of the highly infertile habitats in which it lives. This plant possesses a unique growth form which probably evolved as a response to vertebrate grazing pressure, but appears to lack many of the chemical defensive mechanisms against insect herbivores often associated with woody plants. Ulex europaeus possesses root nodules, and its symbionts are very active nitrogen-fixers. Perhaps the most unusual feature of gorse metabolism is that the concentration of nitrogenous compounds in the foliage is very low (Southwood, 1973; McNeill & Southwood,
1976) for 90% of the year. This is in sharp contrast to the closely related species broom, Cytvsus scoparius, where the nitrogen concentration in foliage is double that of gorse, and is almost constant through the year (J. Riggall, personal communication). The same appears to be true of other species in the tribe Genisteae. It is this unusual pattern of food quality which has led to the suggestion that low nitrogen concentration during summer may be an adaptation on the part of gorse to reduce overall grazing pressure by limiting the feeding period during which insects can successfully develop and reproduce (White, 1978; Moran & Hamilton, 1980).
Broom, which lives in a more nutrient-rich habitat has more nutritious and therefore more susceptible foliage, but it is protected from the effects of insects by a battery of toxins and digestibility-reducing compounds. This view is consistent with the highly conservative life-style of Ulex europaeus in other regards.
The phytophagous insect fauna of gorse in Britain is fairly complete ccmppr«>d with the European fauna. By and large it is a specialist fauna, and many of the literature records of generalists on gorse are either spurious or are incidental records. The number of species which inhabit gorse in Britain is rather small in comparison with similar woody shrubs, and only few of the species are common. The abundance of insects inhabiting flower^ seemed comparable with those attacking similar species like broom, but the abundance of foliage feeding species was very low in comparison
(e.g. only 8 species attacked gorse foliage in recordable numbers). Most species were univoltine, and in general, the fecundity of individual species was low (e.g. approximately 10 for D. strichnocera). In general, the fauna resembled the host-plant in its conservatism.
Much of the current theory in the field of insect/plant relationships has been developed from the examination of literature records or by extra- pilation from laboratory experiments. The obvious exceptions are the theories developed by Lawton (1976, 1978) who has worked from detailed knowledge of the biology of bracken and its insects. Lawton maintains that advances in this field require detailed studies such as his. This
study is one of the very few which provide such detail.
Experimentation has also been advocated as a means of looking more closely at existing theories, and it is here that this study has met its most serious limitations. Apart from the difficulties involved in
sampling insects on plants with the growth form of Ulex spp, and the problems of adequately sampling a fauna whose members are often rare, the conservative nature of both host-plant and fauna have made experimentation extremely difficult (Section 6 and Section 7). Any future attempts to change the stable relationship between gorse and its fauna, especially in the manner described in Section 6, will require treatment and monitoring over a period of years to ascertain any resulting differences in the fauna.
These and many other points have been adequately covered in the discussions accompanying each section, but some further conclusions can be drawn from the work presented here. This study represents one of the most detailed investigations yet carried out of a weed and its natural fauna as part of a biological control programme. While it has provided invaluable information regarding prospects for the control of gorse in other parts of the world, this study has also provided information on aspects of the theory of biological control.
From studies on the fauna of this particular stress-selected species, it seems likely that the type of fauna may be similar in other species from infertile habitats (McNeill & Prestidge, 1982). If this is the case, then assessment of potential control agents in their native environment 214. will require careful timing, and some knowledge of host plant biology.
This study also confirms the importance of timing when carrying out safety screening of candidates for the biological control of stress-adapted weeds. Test plants probably show as much variation in their foliage chemistry as has been shown for gorse, and so the acceptability of an alternative host to an insect probably varies considerably through the season. It is therefore extremely important that screening experiments should be carried out within the natural larval period of the insect involved, and experiments carried out with lab-reared larvae at other times of the year cannot be regarded as valid. Conversely, screening of a multivoltine control agent must be repeated in each larval period if reliable results are to be achieved.
Seasonal variation in food quality has now been demonstrated in numerous plants (e.g. Feeny, 1970; McNeill & Prestidge, 1982 etc), and release programmes must take this factor into account. In the case of gorse, it appears that releases of any foliage-feeding insects must be tjimod such that young stages feed in early June. Release at any other time will presumably result in decreased likelihood of establishment (Section
7). From the work of McNeill & Prestidge (1982) (but not perhaps from this work) application of fertilisers may also aid in establishment of biological control agents.
The biological control practices advocated here are already standard to those working in the field of biological weed control, but this study provides further evidence of their necessity.
This study has produced another important conclusion regarding prospects for the biological control of gorse, and possibly other similar stress-adapted weed species." The insects studied on gorse were not abundant, showed low fecundity, and poor dispersive ability. Most were 215. univoltine, and had relatively long life cycles, largely because of the quality of their food source. Though some were quite heavily parasitised, it seems likely that the foliage-feeding insects were as much controlled from below (by their food source) as from above by their parasites and predators (White, 1978). Since weed control is largely based on the ability of control agents to "outbreak", the prospects for control of
Ulex eu.Topa.eus by insects seem less than hopeful. 216.
ACKNOWLEDGEMENTS
I would firstly like to thank Dr. Stuart McNeill for his advice and guidance throughout this study. I have also benefitted from discussions with Alan Broodbank, Vic Brown, Mick Crawley, Charles Godfray, Jerry
T Graham, David Greathead, Donal 0 Donnell, Ron Prestidge, John Riggall,
Clive Stinson and many others. To all of these people I am very grateful.
For assistance with computing and statistics I thank Mick Crawley,
% Charles Godfray, Hamish MacCallum and particularly Clive Stinson.
Assistance in identifying the insects collected from gorse was provided by Dr. Mike Morris and Ed Rispin (ITE),. Charles Godfray, Paul
Hyman, George McGavin, Dr. N. Waloff and the Commonwealth Institute of
Entomology.
J would also like to thank Professor J.B. Harborne, Dr. Jill Harrison
(Reading University) and particularly Alan Broodbank for assistance in defpi-mining some of the chemical characteristics of gorse foliage.
I would particularly like to thank Carole Collins for efficiently typing this thesis in a very short time.
The Silwood Park community, including fellow residents of Grove End
House,, and an endless stream of visiting travellers provided a conducive atmosphere for the execution of this work, and I am grateful to them all.
This study was supported by an award from the New Zealand Department of Scientific and Industrial Research, to whom I am also very grateful. 217.
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APPENDIX VII
Phenology of Ulex europaeus
Date Developmental event 1979 1980 1981
Major flowering begins early March early March
Peak flowering late April mid April
First pods early May late April
Vegetative bud-burst - non-flowering stems late April late April mid April - flowering stems mid May mid May mid May
No flowers mid June late May
Old stem senescence begins mid June mid June
First pod dehisces late June mid June
Hardening of shoots begins late June late June
Senescence complete mid July early July
Terminal spines appear late July early August
Flower buds form mid August mid Augus t
Ulex minor flowering begins mid August APPENDIX II
Changes in the proportions of U. europaeus reproductive structures in different classes
Yateley Common
% of No. of No. of Date Day reproductive samples Immature Mature parts Buds Flowers pods pods 2 Apr. 80 80094 14 982 92.2 4.5 3.4 0 23 Apr. 80 80115 5 186 31.2 59.1 9.7 0 UN>3 1 June 79 79152 2 44 15.9 59.1 25.0 0 18 June 79 79169 5 84 0 0 28.5 71.4 28 June 79 79179 5 26 0 0 0 100 9 July 79 79190 3 17' 0 0 0 100 23 July 79 79204 5 12 0 0 0 100
Windsor Great Park
80077 15 1530 91.4 7.8 0.8 0
3 Apr. 81 81093 - - 92.6 7.4 0 0 80101 15 920 82.9 15.6 1.5 0 80122 4 513 51.1 25.6 23.2 0 79151 7 279 14.3 23.7 60.9 79163 10 209 1.0 21.1 54.0 23.9 25 June 79 79176 8 128 0 0 22.6 77.3 6 July 79 79187 8 139 0 0 13.7 86.3 24 July 79 79201 10 131 0 0 0 100 232.
APPENDIX III
Water content of Ulex europaeus (%)
WGP 1979 Mean
16 May 68.8 70.7 68.0 69.3 - 69.2
31 May 76. A 73 76.8 73.7 - 75.0 17 June 76.1 8A 65.0 77.6 75.9
77.9 - - - - 76.1 25 June 76 7A.1 70.5 71.9 72.9
7A.7 73.A 7A.6 - - 73.6 6 July 72.6 73.2 70.6 73.7 73.1 72.8 20 July 7 A. A 70 70.2 69.5 69.3
68.5. 69.7 66.8 - - 69.8
31 July 6A.7 66.9 69.2 67.9 - 67.2
10 Aug. 66.A 67.5 66.3 66. A - 66.7 20 Aug. 63.7 62.6 61.6 67.A 65.9
63.9 - - - - 6A.2
30 Aug. 61.2 59.3 59.9 - - 60.1
12 Oct. 58.8 - - - - 58.8
YC 1979
1 June 68.5 69.0 - 68.8
18 June 70.9 73.2 71.8 72 - 72.0
28 June 71.5 72.A 71.6 71.6 - 71.8 10 July 70 69.6 70.3 69.6 70. A 70.0 23 July 6A.6 66.6 67.2 62 66.1 65.3
5 Aug. 65.3 63.2 68.0 65 - 65. A 16 Aug. 60.3 6A.9 6A.1 69.1 53.A
70 - - - - 63.6
27 Aug. 61.7 63.6 63.6 65 - 63.5 17 Oct. 63.7 63.7 233.
Appendix VIII : Continued.
YC 1980 Mean
2 June 71.7 68.7 71.1 69 71 69.7 70.5 23 June 68.5 68.6 68 67.9 66.7 67 68.6 67.7 67.9 3 July 70.2 73.6 71 70.6 70.8 70.4 70.1 68.9 73 69.5 70.8 16 July 66.9 68.8 69.4 70.9 69.8
71 71.5 68.5 - - 69.6 1 Aug. 67.9 69.1 66.5 68.3 68.9
68.7 67.3 69.3 68.9 - 68.3 22 Aug. 62.9 61.9 61.2 63.6 65.7 61.8 ' 62.8 65.6 63.9 63.3 26 Sept. 54 54
WGP 1980
27 May 70 73.1 71.5 72.1 - 71.7 10 June 69.7 67.4 66.7 63 61.5
62.7 63.9 63.1 63.5 - 64.6 26 June 61.8 60.7 60.6 61 61.5 62.7 63.4 63.5 61.5 62.7 61.9 8 July 62.4 63 64.4 63.6 66.4
— 64 64.9 64.8 63.7 - 64.1 30 July 61.3 60.6 65.4 60.1 61.6 68.5 61.5 68.1 67.1 72
72.3 68.5 - - - 65.6 15 Aug. 60.2 69.4 69.2 61.3 61.6 63.1 65.5 61.7 64.2 64 234.
Appendix VIII : Continued.
YC 1981 Mean
21 May 68.8 68.5 68.5 69.1 - 68.7 2 June 69.9 70.7 68.9 65.2 65.7 69.1
16 June 67.6 61.1 60.5 61.3 - 61.1 6 July 67.2 67.2 64.7 67.2 64
65.1 62.7 - - - 65.4 25 July 69.5 67.7 66.2 67.6 67.7 67.7
20 Aug. 59.7 66.9 62 - - 62.9
Water content of U. minor
1979
1 June 62 60.5 61.3 18 June 68.3 65.7 66.7 66.9 28 June 66.7 66.1 66.4 10 July 66.2 64.1 64.1 67.6 66.1 65.6 23 July 64 60.5 62 62 62.1 5 Aug. 55.7 57.4 60.4 61.6 58.8 16 Aug. 61.1 57.5 60.3 54.6 58.4 27 Aug. 56 54.9 56.8 57 56.2 7 Aug. 52.2 52.2 16 Sept. 50 50.0 17 Oct. 49.8 49.8
1980 (old growth 42 .6, 45.2 )
2 June 61 66.7 62.5 63.4 23 June 51.9 45 60.9 60 57.9 55.1
4 July 68.1 69.1 67.3 70.4 69.2 - 70.8 67 70 68.6 68.9
16 July 63.9 63.5 62.2 67.5 67.7 -
65.6 - - - - 65
1 Aug. 58.2 63.3 65.1 62.1 - 62.2 22 Aug. 60 56.1 57.4 .55.7 57.4 60. 4 57.8 235.
Appendix VIII : Continued.
Foliage water content by parts
Terminal Next Next Basal (YC) 2 cm 2 cm 2 cm 2 cm
23 June 66.2 66.9 59.2 67 66.7 63.3 Mean 66.6 66.8 61.6
30 June 65.3 63.1 70.6 66.7 72.2 77.8 68.8 Mean. 68.8 70.5 69.7
16 July 72.5 73.1 68.1 65.8 71.6 71.1 67.1 66.7 Mean 72.1 72.1 67.6 66.2
1 Aug. 73.5 70.7 68.8 66.1 78.3 69.2 66.7 - Mean 75.9 69.9 67.8 66.1
22 Aug. 68.8 61.4 61.2 59 64.9 64.8 59.4 = Mean 66.9 63.1 60.3 59 236.
Appendix VIII : Continued.
(WGP) Terminal Next Next Basal 2 cm 2 cm 2 cm 2 cm
15 Aug. 74.3 70.4 68.3 67.1 76.0 71.9 69.3 Mean 75.2 71.2 68.8 67.1
30 July 74.8 70.6 67.6 68.1 _75 70.3 68.8 Mean 74.9 70.5 68.2 68.1
8 July 80.3 76.3 75 70.5 76.2 79.2 72.9 70.9 Mean 78.3 77.8 74.0 70.9
26 June 76.7 76 72.4 71 75 72.1 Mean 76.7 75.5 72.3 71 237.
APPENDIX VII
Nitrogen content of gorse foliage
Total nitrogen - Ulex europaeus
Old foliage Date X SD SE n or new
WGP 28 Feb. 79 19.9 2.3 1.3 3 0 21 Mar. 79 22.0 3.0 2.0 2 0 %
28 Mar. 79 19.2 - - 1 0 5 Apr. 79 18.7 3.3 1.9 3 0 11 Apr. 79 19.3 5.9 3.4 2 0 20 Apr. 79 19.1 4.7 2.7 2 0 2 May 79 23.2 2.9 1.7 3 0 16 May 79 17.9 5.3 3.1 3 0 46.6 5.0 2.9 3 N 31 May 79 20.9 5.8 3.4 2 0 40.3 .03 .01 3 N 12 June 79 19.7 2^0 1.2 3 0 37.5 3.0 1.3 5 N
25 June 79 18.8 - - 1 0 32.1 6.5 3.3 4 N 6 July 79 24.3 4.7 2.7 3 N
20 July 79 18.4 - - 1 N 31 July 79 18.0 2.4 0.8 8 N 20 Aug. 79 18.3 2.9 1.7 3 N 30 Aug. 79 20.5 3.6 1.6 5 N 11 Oct. 79 22.3 4.1 2.3 3 N
WGP 12 May 80 41.5 1.5 1.1 2 N 27 May 80 39.3 3.0 1.5 4 N 26 June 80 32.0 3.2 1.6 4 N 30 July 80 29.2 2.4 1.2 4 N 15 Aug. 80 27.8 2.4 1.2 4 N 238.
Appendix VIII : Continued.
Old fol Date X SD SE n or n
YC 10 Apr. 79 16.8 0.9 0.7 2 0 26 Apr. 79 13.1 1.8 1.0 3 0 8 May 79 18.2 4.1 2.4 3 0
40.7 - - 1 N 18 May 79 13.6 1.5 1.6 3 0 41.8 2.8 0.4 3 N 1 June 79 16 0.7 0.4 3 0. 42.7 6.3 4.5 2 N 18 June 79 20.0 1.0 0.6 2 0 35.1 2.1 1.0 3 N 28 June 79 30.4 3.6 2.1 2 N 9 July 79 23.6 3.6 1.1 10 N 5 Aug. 79 17.5 1.2 0.6 4 N 16 Aug. 79 15 2.9 1.7 3 N
YC 8 May 80 36.8 - - 1 N 21 May 80 39.9 1.3 0.9 3 N 2 June 80 39.0 3.6 1.5 6 N 23 June 80 29.7 2.6 0.9 8 N 3 July 80 28.8 2.3 0.8 7 N 15 July 80 26.1 5.1 1.7 9 N 22 Aug. 80 20.3 1.6 0.5 9 N 19 Sep. 80 20.9 0.4 0.2 3 N
YC 3 Apr. 81 18.3 2.3 1.1 5 0 15 Apr. 81 14.2 2.0 0.9 5 0 30 Apr. 81 16.2 1.0 0.4 5 0
- 25.6 - - 1 N 14 May 81 32.9 1.9 0.8 5 N 21 May 81 37.5 1.6 0.7 5 N 1 June 81 35.6 2.1 0.9 5 N 15 June 81 30.1 4.7 2.1 5 N 9 July 81 23.3 1.6 0.7 5 N 25 July 81 20.7 1.8 0.8 5 N 239.
Appendix IV : Continued.
Total nitrogen - Wlex minor
Old foliage Date X SD SE n or new
10 Apr. 79 17.1 3.3 2.3 2 0 18 Apr. 79 14.4 1 0 26 Apr. 79 18.7 0.4 0.2 3 0 19 May 79 17.1 1.1 0.6 3 0 39.2 1 N' 1 June 79 18.0 1.7 1.0 3 0 18 June 79 15.1 1.7 1.2 2 0 31.1 5.3 2.6 4 N 28 June 79 . 28.9 2.7 1.4 4 N 9 July 79 24.1 1.3 1.0 4 N 5 Aug. 79 17.9 9.2 4.1 5 N 16 Aug. 79 19.8 3.1 2.2 2 N 27 Aug. 79 18.5 1.7 1.2 2 N 3 Oct. 79 23.1 3.2 1.6 4 N
21 May 80 34.4 3.7 2.1 3 N 3 June 80 36.4 2.9 2.1 2 N 23 June 80 29.3 2.2 1.1 4 N 3 July 80 25.9 1.0 0.6 3 N 15 July 80 23.5 1.3 0.7 4 N 1 Aug. 80 21.6 1.0 0.5 3 N 22 Aug. 80 18.8 1.8 1.0 4 N
21 July 81 20.8 1.7 0.8 5 N 240.
Appendix IV : Continued.
Soluble nitrogen - Ulex europaeus
Old foliage Date X SD SE n or new
WGP 21 MarMar.. 79 2.2 0.6 0.5 2 0
28 Mar. 79 3.1 - - 1 0 5 Apr. 79 2.1 0.8 0.5 3 0 11 Apr. 79 2.2 0.1 0.1 2 0 20 Apr. 79 2.5 0.2 0.1 2 a 2 May 79 2.9 0.7 0.4 3 0 16 May 79 3.2 0.3 0.2 3 0 6.1 1.5 1.0 2 N 31 May 79 2.3 0.4 0.4 2 0 3.1 0.6 0.3 4 N 12 June 79 3.0 0.5 0.3 3 0 4.3 1.5 0.6 6 N
25 June 79 3.1 - - 1 0 2.2 0.5 0.2 5 N 6 July 79 2.7 0.2 0.1 4 N
20 July 79 1.8 - - 1 N 31 July 79 1.5 0.3 0.1 8 N 20 Aug. 79 2.0 0.3 0.2 3 N 30 Aug. 79 2.4 0.7 0.4 4 N 11 Oct. 79 1.9 0.2 0.1 3 N
WGP 12 MaMayy 80 5.8 1.8 1.3 2 N 27 May 80 4.9 0.6 0.3 4 N 26 June 80 3.2 0.6 0.3 4 N 8 July 80 3.4 0.6 0.3 4 N 30 July 80 3.1 0.5 0.3 4 N 15 Aug. 80 2.8 0.5 0.3 4 N 241.
Appendix IV : Continued.
Old foliage Date X SD SE n or new
YC 10 Apr. 79 1.8 0.1 0.1 2 0
18 Apr. 79 6.3 - - 1 N
26 Apr. 79 8.8 - - 1 N
1 June 79 2.0 - - 1 0 5.4 1.0 0.7 2 N 15 June 79 2.8 0.8 0.5 3 0 3.6 1.4 0.6 5 N' 28 June 79 2.4 0.8 0.4 3 0 2.4 1.0 0.7 2 N 9 July 79 2.3 0.1 0.03 3 0 1.8 0.5 0.2 9 N 5 Aug. 79 1.6 0.5 0.2 4 N 16 Aug. 79 1.2 0.1 0.1 3 N 27 Aug. 79 2.1 0.8 0.4 3 N 3 Oct. 79 1.9 0.2 0.1 3 N
YC 8 May 80 1.6 - - 1 0 21 May 80 4.7 0.4 0.3 2 N 3 June 80 5.4 1.7 0.8 5 N 23 June 80 2.8 0.5 0.2 7 N 3 July 80 2.5 0.6 0.2 9 N 15 July 80 2.1 0.4 0.1 9 N 22 Aug. 80 1.7 0.4 0.1 9 N
ULex galHi,
1 August 79 total N 21.4 20.4 23.1 17 September 79 total N 11.0 15.9 September 79 total N 21.7 242.
APPENDIX VII
Ulex europaeus foliage toughness
Toughness of spine at x cm from apex
No. of x = 1 cm tests 2 cm n 3 cm n 4 cm n 5 cm n 6 cm n
(YC)
14 May 81 77 13 225 21 May 81 53 10 1 June 81 44 21 78 10 15 June 81 91 11 238 15 374 9 667 3 825 3 July 81 170 14 368 19 1027 11 1169 8 18 Aug. 81 950 17 1036 18 1097 18 1152 18 1200
(WGP)
8 July 80 108 16 . 142 13 593 14 732 14 941 11 - 29 July 80 453 29 786 29 969 29 1200 28 1200 1200
16 Aug. 80 621 22 841 23 993 23 1150 — 1200 - —
(YC)
23 July 80 170 26 629 25 943 22 1150 — 1200 - -
1 Aug. 80 204 25 374 25 872 25 1150 - - -
18 Aug. 80 506 873 31 1137 29 1200 26 - -
Toughness of stem at x cm from apex
x = 1 cm n 2 cm n 3 cm n
(YC) 14 May 81 346 15 21 May 81 345 15 1 June 81 313 25 422 11 15 June 81 489 19 550 14 647 3 July 81 567 18 788 16 1110 18 Aug. 81 1133 18 1200 1200 APPENDIX VI
Mean length of new shoots
Mean new shoot length in 1979 and 1980 was estimated from the number of shoots in each of 4 size categories (0-1 em, 1-4, 4-8, 8-12). Length was estimated by the number of shoots times mean length of size category divided by total number of shoots. In 1981 the same procedure was used, but shoots were also measured individually. The relationship between lengths measured, and estimated from category numbers is shown.
1979
WGP u. europaeus YC u. europaeus YC u. minor
est. est. est. date date date length length length
10 Apr. 0.2 18 May 0.5 18 May 0.2 16 May 0.5 18 June 2.2 18 June 1. 0 12 June 2.2 9 July 5.5 9 July 3.3 6 July 5.3 31 July 7.0
1980
YC U. europaeus unfertilised YC U. europaeus fertilised
date est. length date est. length
3 June 0.81 3 June 1.40 17 June 1.89 17 June 2.41 1 July 2.65 1 July 3.07 15 July 3.51 15 July 5.90 31 July 6.30 31 July 7.10 19 Aug. 7.69 19 Aug. 8.59 244.
Appendix VIII : Continued.
1981
YC U. europaeus unfertilised (10 samples)
date estimated length measured length SD no. of shoots
14 May 0.56 0.50 0.08 100 21 May 0.86 0.78 0.40 213 2 June 1.98 1.59 0.61 241 15 June 2.29 2.0 0.45 809 . 7 July 4.40 4.16 1.10 366 25 July 4.82 4.90 1.00 387 21 Aug. 6.91 6.90 2.10 199
YC U. europaeus fertilised (10 samples)
14 May 0.98 0.78 0.50 126 21 May 0.89 1.05 0. 60 353 2 June 2.20 1.74 0.63 320 15 June 3.01 3.25 1.17 681 6 July 4.43 4.56 1.10 357 25 July 5.51 5.97 1.08 336 21 Aug. 7.05 8.8 4.80 187 245.
APPENDIX VII
Enzyme - inhibition reaction times
(see Section 3.4.9)
20 May 1981
Time to end point at enzyme concentration
Standard reaction 0.1 mg/ml 0.2 mg/ml 0.3 mg/ml 0.4 mg/ml
11.20 4.40 3.00 2.20 ' 10.00 5.20 4.00 3.00 10.00 5.20 4.20 3.00 10.40 6.00 4.20 3.20 12.00 6.40 4.00 3.00 13.20 7.20 4.40 3.40 . 14.00 6.40 4.20 3.00
Extract concn.
gorse 40 mg/ml 12.00 6.40 5.20 3.40 50 9.40 6.00 4.20 3.20 60 11.40 8.40 200 16.40 9.20 6.40 4.00 " 200 13.00 7.40 4.40 3.40 200 14.40 7.20 6.20 4.00 oak 200 15.00 10.20 7.00 6.00
11 June 1981
Standard reaction 0.1 0.2 0.3 0.4 12.40 6.20 4.20 3.40 12.20 6.20 4.40 3.20 13.00 6.40 5.00 3.40 11.40 6.20 4.20 3.40
Extract concn.
gorse 60 mg/ml 11.20 7.40 4.40 3.20 " 60 13.20 6.40 4.20 3.40 60 14.40 7.40 5.40 4.20 60 11.40 6.20 5.00 4.00 heather 60 12.20 7.20 6.20 oak 60 24.20 13.20 7.20 6.00 246.
Appendix VIII : Continued.
14 July 1981
Time to end point at enzyme concentration
Standard reaction 0.1 mg/ml 0.2 mg/ml 0.3 mg/ml 0.4 mg/ml
10.00 6.20 4.00 3.00 10.40 6.00 4.00 3.00 11.20 7.40 5.20 3.40
Extract concn. gorse 100 mg/ml 12.20 9.00 6.00 4.00 " 100 11.00 7.20 5.20 3.20 100 13.00 8.40 5.40 3.40 " 100 12.20 7.40 4.40 3.00
20 August 1981
Standard reaction 0.1 0.2 0.3 0.4 12.00 7.00 4.40 3.20 10.40 6.00 4.00 3.20 11.00 5.40 3.40 2.40 12.00 6.20 4.00 3.00
Extract concn.
gorse 60 mg/ml 11.20 6.40 5.00 3.20 11.00 6.40 4.40 3.40 11.40 7.00 5.20 3.20 247 .
APPENDIX VIII
Summarised insect data
The mean abundance per sample of each species beaten from gorse foliage is presented for each sampling occasion. Absence of a record for any sampling occasion represents zero abundance. 95% confidence limits are also presented. 15 samples were taken on each occasion. Day represents day of year, and its Julian equivalent is presented below.
Key to species
Species Species Name Name No. No.
Dromius linearis/ 27 E. nivalis melanocephalus 28 Sminthurus viridis Corticaria crenulata/ 29 Tomocerus spp. serrata 30 Forficula auricularia 6 Micrambe vini • 31 Dasineura sp. 8 Apion scutellare (Ad) 32 Anthocoris sp. 9 A. striatum (Ad) 33 Berytinus minor 10 A. ulicis (Ad) 34 Lygaeid sp. 12 Polydrusus confluens (Ad) 35 Asciodema obsoletum 13 Sitona regensteinensis (Ad) 38 Pachylops bicolor 14 S. tibialis (Ad) 39 Phytocoris varipes 15 Strophosomus lateralis 40 Natis rugosus (Ad) 42 Piezodorus lituratus S. melanogrammus (Ad) 16 43 Aphis ulicis 17 Athous haemmorhoidalis 44 Euceraphis punctipennis (Ad) 50 Philaenus sp. 18 Gdnopus aerugineus (Ad) 55 Coleophora albricosta 19 Dalopius marginatus (Ad) 56 Anarsia spartiella 20 Phloeophthorus rhodo- dactylus (Ad) 57 Ematurga atomaria 23 Philorinum sordidum 58 Gymnoscelis rufifasciata 25 Cylindronotus laevioct- 59 Peribatodes rhomboidaria ostriatus (Ad) 60 Pseudopterpna pruinata 26 Entomobryia multifasciata 248.
Appendix VIII : Continued.
Species Species Name Name No. No.
61 Gecmetrid 1 72 Odontothrips ulicis 62 " 2 73 Sericothrips staphylinus 63 " 3 74 Thrips flavus 64 Callophrys rubi 78 Dictyonota strichnocera 65 Agonopterix nervosa 81 Cydia spp. 66 A. ulicetella 82 ' Phariococcus aceris 67 Psocopteran sp. 83 Leptophyes punctatissimfo 69 Tenthredinid sp. 84 Ceramica pi si 70 Aeolothrips sp.
Sampling dates
(ERRATUM: IN 1981 SAMPLES, FOR DAY 199 READ 230)
1980 1981
Day Date Day Date
94 3 Apr. 115 25 Apr. 115 24 Apr. 133 13 May 128 7 May 154 3 June 133 12 May 167 16 June 142 21 May 187 6 July 148 27 May 230 18 Aug. 155 3 June 163 11 June 171 19 June 111 25 June 182 30 June 188 6 July 198 15 July 211 29 July 213 31 July 227 14 Aug. 233 20 Aug. 249.
Appendix VIII : Continued.
Sampling dates
1980 YC unfertilised Ulex europaeus 94, 115, 128, 142, 155, 171, 182, 198, 213, 233, 263
1980 YC fertilised Ulex europaeus 128, 155, 182, 213, 233
1980 YC Ulex minor 94, 115, 128, 142, 155, 171, 182, 198, 213, 233
1980 WGP Ulex europaeus 101, 122, 133, 148, 163, 177, 188, 211, 227
1981 YC unfertilised Ulex europaeus 115, 133, 154, 167, 187, 230 (= 199 in table)
1981 YC fertilised 115, 133, 154, 167, 187, 230 (= 199 in table) 1980 WGP Ulex europaeus SPECIES .JU.'.libK 13 X DAY ME Art CONF SPECIES f l U i'I b h. K 01 iJ i\ L '•IE AH CONE L IU rT 101' . 4 0 .51 148 .07 .14 122 . oO .55 177 .20 .23 1 J3 .13 .20 .07 .14 148 .33 .27 188 163 .07 .14 04 SPECIES ilUnoEK 0 A l H E A CONF LIMIT SPECIES tl U ti ci EK 14 1 • i a .13 .20 OAX M E A a CONF LIMIT i 63 1.13 .89 101 .07 .14 177 . 73 .65 122 .07 .14 1 U ri .73 .65 177 .07 . 1 4 2 11 1.80 .94 '211 .07 .14 2 27 .33 .34 SPECIES .iUMBKH 16 DA if ME AM LIMIT SPECIES •'IU.moEU 06 OhY MEAN CONF LIMIT 148 .07 .14 10 i 1 .60 1.22 122 .80 .64 r 1 J3 .87 .59 SPECIES h U i; i> E R 2 0/''' 1'tH 1 .47 1.09 ; • DAY •'IE Ati CONF LIMIT N3 loJ .37 .55 122 .33 .27 Ul 177 .47 .63 133 .07 .14 o 16b .80 .87 148 .07 .14 * .ill .53 . 46 1 b 3 .13 .20 221 2.8 0 2.24 188 .07 .14 u9 SPECIES NUMBER 2 3 SPECIES 'JUi-.bEK u A i MEAN CONF LIMIT DA If MEAW CONF LIMIT .13 .20 101 .13 .20 121021 .33 .34 122 l.bO 1.20 163 .07 .14 133 .53 .41 1 7 7 .67 .72 148 .33 .40 1(58 .20 .23 211 .07 .14 SPECIES riUfiOEW 2 7 22 7 .07 .14 OA/ MEAN COTIF LIMIT 101 19.33 4.y1 122 21.00 5.86 SPECIES MU.Itjt-.r 10 ,-IEAN CONF LIMIT 133 3.33 2.13 u a X 5.53 2.61 148 12.33 4.6U iOi 6.47 2.1b 163 7.53 2.80 122 4.07 1.62 17 7 7 . 6 0 3.27 til 4.67 2.12 Hi 8 2 5.00 14.36 i£3 3.87 I .b 4 211 9.67 2.22 l"7 7 2.47 1.11 22 7 3.13 3.58 i 8 B 4.47 1.09 211 4.20 1.25 6.67 2.37 SPECIES WO.-IjcK 30 22 7 uAx M:J AN CO (IF LIMIT 122 .73 1.43 133 .07 .1* SPKClEo '< > >. i 2 •IE/wm CUflK LIMIT 14 8 .13 .20 .07 .14 16 3 .07 .14 121323 .07 .14 177 . U .20 148 .13 .20 16 8 .27 .33 .13 .20 2U .27 .44 i 7 7 2 2 7 .07 . i 4 1980 WGP Ueuropaeus SPECIES .lU.'iiibK 33 t n r »r» SPECIES NljMuER 5 5 DAY MEAN CONF LIMIT l-i A i 11E A i CUNF LIMIT 211 .07 .14 101 .07 .14 211 .07 .14 SPECIES ii'UIloEK 35 D A ¥ MEAN CUUF LIMIT SPECIES NUMBER 56 101 .20 .43 DAY lEAii COiJF LIMIT 133 1.73 1.23 133 13 . 20 148 2.6 7 2.20 163 .93 .77 188 .67 .54 SPECIES tJ U M ii E K 5y 211 .07 .14 r-lEAN 148 .07 .14 ill .20 .31 SPEC IES '. I >.; b E K 38 188 .07 .14 day ME A rl CUN F LIMIT 163 .20 .43 1 77 2 .13 1.45 SPECIES riUMtiER 61 188 3 .00 2.08 DAY MEAN CONF LIMIT 211 3 . uO 2.2 2 227 . u 7 .14 227 1 .73 1.06 SPECIES U ij.'LsEH 63 SPECIES iiuMoEi-: 39 DAY MEAN CUNF LIMIT U i\ * ME Ail CONF LIMIT 2 11 .07 .14 177 .07 .14 227 .07 .14 SPECIES NUMBER 65 DAY MEAN CONF LIMIT SPECIES I.U.MjEK 40 122 .07 .14 i;AY MEAN CONF LIMIT 148 .53 .66 211 1 .00 1 .36 22 7 .4 7 .29 SPECIES NUMBER 66 r DaY MEAN CONF LIMIT SPECIEu io • i)Ki 42 163 .07 .14 OA Y MEAN CONF LIMIT ill .13 .20 101 .20 .23 227 .07 .14 122 .0 7 .14 163 .13 .29 177 1 .07 . 77 SPECIES f J < J nBEH 67 18b .13 .20 DAY MEAN CONF LIMIT 211 I.0 0 . 8 1 101 . 13 .20 22 7 .93 .83 1^2 10.93 5.19 133 21 .00 7.73 148 8.67 4.86 SPECIES i'l iJ .•' L, 1,1 4i 163 23.67 5.19 OA* MEAN CiJNF LIMIT 1 77 14.00 3.81 177 .13 .20 188 1 t3 . OO 5.85 188 .07 .14 211 3.7 3 2.15 21 I 2 .73 5.73 227 14.0 J 6.05 227 .07 .14 SPECIES hiJMiEH 70 SPEC IKo ii u :!trjJ! 44 U/J ' 1E A i-l CON F LIM 1T MEAN C O; i FL1 M 11 148 .27 .57 D13 A 3^ .33 .72 163 .60 .41 17 7 .53 .29 177 1 . oO 1.07 2. 2.1 .13 .29 188 .13 . 20 1980 WGP U. europaeus
SPECIES ii u i-i U E R 72 day MEAN CONF LIMIT lol 13.17 6.32 122 6.40 2.19 * 133 4.60 2.42 • 148 1.53 1.29 163 .27 .39 138 .20 .23
SPECIES lUMttEJ-: 73 DAY MEAN COflF LIMIT 10 1 16.93 12.23 N3 122 10.80 4.93 U"i 133 12.47 4.18 Ni 148 17 . 20 7.39 * 1 o3 7.00 4.04 177 18.00 13.75 188 20.73 8.25' 211 14.87 9.93 2 27 21.73 6.03
SPECIES 11 o ii b E R 78 DAY 'IE Ail CONF LIMIT 1 33 .67 .91 118 12.80 4.89 163 11.33 5.83 177 5.93 2.8 6 188 5.2 0 2.52 211 2.00 1.19 227 .80 .85
SPECIES r:u 81 JAY MEAN CONF LIMIT 122 .07 ,14 SPECIES woMKEi: 83 i.'A Y 'lEAIi CONF LIMIT 177 .13 ,20 188 .13 ,29 211 .0 7 .14 unfertilised 1980 Yateley Common
SPECIES fluMtiEfc 0 1 D A Y i-l EA N CO UK DAY M E A N CON F L55 .07 .14 128 .07 . 14 263 .07 .14 142 .13 .20 171 .27 .33 182 .07 . 14- SPECIES :UJ:VnEK 04 196 .93 .53 0 AY MEAN CONF 213 .33 .27 155 .07 .14 233 . 13 .20 171 .13 .20 263 .27 .25 182 .07 .14
SPECIES NUMbER 06 DAY .MEAN CONF U A Y MEAN CONF 94 1.07 I . 14 9A .40 .41 11? .80 .64 115 .53 .99 128 .40 .35 128 .60 .81 142 .40 .28 142 .27 . 25 155 - .60 .SI 182 .07 .14 233 .13 .20 190 .07 .14 263 .13 .29 213 .20 .3 1 233 .07 . 14 263 1.00 .84 D A Y nEAM CONF 94 .73 .49 SPECIES i i I) i i b E t< 08 115 1 .40 1.13 u AY r i E A i J CONF 120 1.27 .90 94 .07 . 1 4 142 1 .87 1.09 1 15 .07 .14 155 .93 .57 128 .07 .14 171 1.73 .80 142 .13 .20 162 1.47 .41 155 .07 .14 198 1 .40 .98 17 1 .07 .14 213 1 .07 .68 182 .13 .20 233 .07 . 14 263 .47 .29 SPECIES !J U :•! tj ti H 09 M E A ; I CUfJF LIMIT 128 .20 ,31 DaY MEAN CONF LIMIT 1D5 .07 ,14 94 .27 .44 17 1 .20 ,23 115 .67 .58 182 . 2 0 23 129 .20 .31 198 .20 23 233 .07 14
MEAN CONF LIMIT SPECIES riiJMiiEP 10 142 .13 .20 i' MEAN COUF tjI i-i IT 171 .20 .23 94 1 . 93 1 .32 198 .07 .14 115 2.67 .95 128 3.7 3 2.0 2 142 1 .93 1.20 155 1.67 .91 j A * MEAN CONF LIMIT 111 .73 .44 155 .13 .20 182 .67 .50 i 98 1 . 00 .66 213 1.90 .90 233 2.00 1.17 DAY i-IEAN CONF LIMIT 263 3 .33 . 8b 171 .07 .14 1980 YC U.europaeus unfertilised SPECIES iHji'::lLi. 23 U i\ 1 .mEA.J CONF 35 m • 13 .20 DAY MEAN CUNF LIMIT 128 .13 .29 142 7.53 3.51 SPECIES NUMbEK 25 155 3.87 1.84 DA i i 1E A i 1 C 0 N F 171 3.27 1.90 94 .07 . 14 182 2.00 .94 115 .27 .44 198 1 .00 ' .56 155 .07 .14 233 .07 .14 171 .20 .23 182 .20 .23 196 .20 .23 SPEC ItS laJMbEH 38 233 .07 .14 DAY MEAN CONF 263 .20 .31 155 .53 .81 171 l.OO .70 182 6.13 2.96 SPECIES NUMbER 26 198 7.13 2.11 DA Y ri E A N CO 213 "5 .4 7 2 .55 94 24 .33 13 .19 233 3.13 1.13 115 17 .20 4 .08 263 1.07 .57 12 0 7 .27 2 .49 142 7 .07 2 .87 i55 7 .20 2 . 12 SPECIES tiUi'\ti E R 40 171 19 .00 4 .35 DAY MEAN CUNF LIMIT. 182 12 .33 .30 94 .07 .14 196 23 .13 5 .64 182 .07 .14 213 38 .67 17 .27 213 .13 .20 233 24 .13 10 .30 233 .13 .20 2 (53 57 .00 25 .35 263 .13 .20
SPECIES NUMbER 29 SPECIES NUi-iOEK 42 D A 1 r-lEAM CONF LIMIT uAY MEAN CONF 142 .13 .20 171 .33 .40 182 .33 .34 198 .27 .25 SPECIES NUMbER 29 2 13 .13 .20 u A Y /; E a CONF LIMIT 94 .27 .39 SPECIES NUMtlER 43 DAY MEAN CUNF LIMIT SPECIES NUMjL'r; 30 213 1.53 2.86 ^ /v r ;• I E A I I CU;;F limit 233 2.40 4.33 142 . 07 ,14 263 1.73 2.90 155 .13 ,29 171 .07 .14 .27 .25" SPECIEb .MJMbER 44 18L 928 .87 ,59 'JAY MEAN CONF LIMIT 213 . 40 ,59 128 .07 . 14 233 .13 .20 155 .13 .20 2 62> .13 ,20 171 .13 .20 213 .13 .20 263 .07 .14 SPECIES Ndiitii.k 31 >v l ': E A. I COIlF LIMIT SPECIES i-U.'.BER 66 SPECIES NUMBER 18 DA i fiEAN CONF LIMIT DA* MEAN CONF 11? .20 .31 115 .47 .69 128 .33 .40 128 .33 .72 155 .13 .20 142 11.73 3.94 171 .47 .41 155 9.67 3.70 192 .80 .48 171 11. 13 3.94 196 .87 .75 182 8.2 7 2.65 2 1 3 .0 7 .14 19d 5.33 2.0 0 213 3.33 1 .99 233 .67 .50 SPECIES lib.-a Em 67 2 o 3 .33 .27 \.t X ;: E A COwF LIM1T 17 1 . 0 7 . 14 .07 .14 1 182 SPECIES i.' UMBER 1 90 . 1 3 .20 Da* MEAN CO IF LIMIT 213 .20 115 .07 . 14 263 1 .33 2.22 12 3 .0 I .14 sptCILS ;;U,UT,I 70 SPLCIES IiU.it; t. m e2 1 ' t. X t ErX.'i CiJtiK LIMIT r-l E A l'i COME LIMIT 17 1 .33 .27 17 1 .07 .14 182 .07 .14 2 o 3 .07 .14 1980 Yateley Common U • minor 14 SPECIES WU.-UiER 01 SPECIES iilirioEP HM it- D A i* i-.EAti C l) i J F .JAY i i E A i'i COiiF 94 .27 .39 94 2.40 1.27 171 .13 .29 115 2.80 2.21 182 .13 .29 128 1.87 .98 142 1.07 1.02 155 1.73 1.38 SPECIES riUMoEH 04 171 1.33 .69 'J A I i-.EA?/ conf 182 1.87 .89 155 .13 .29 198 1.73 .93 213 .40 .46 233 .40 .46 SPECIES .ju;lbht< 06 un Y wE AN CONF 94 .13 .29 SPECIES nbi-lbER 15 115 .27 .39 DAY MEAN CONF limit 155 .13 .29 9 4 1.33 1.08 115 1.87 1 . lb 128 .67 .54 SPECIES rjU.idtl? 08 142 .80 .82 A I ME Aw CUNF 155 1 .33 I.00 Ni 94 .27 .39 Ui 115 .27 .39 Os 125 .13 .29 SPECIES fiUrlLiER 16 155 .53 .99 DAY mE AN COflF LIMIT 171 .40 .62 1 28 . d0 .92 152 .27 .39 142 .13 .29 i 98 .13 .29 155 .13 .29 171 .27 .39 198 .13 .29 SPECIES ilUHticE 10 day ME aN CUNF 94 1.07 .93 SPECIES NUMBER 23 115 .53 .66 DAY h E A N CON F LIMIT 123 .30 .92 233 .13 .29 142 . 13 .29 155 .27 .39 171 .27 SPECIES NUMBER 25 182 .40 .62 CON F LIMIT 213 1.60 .96 115 .13 .29 233 1 .20 .82 SPECIES ii U i-lbEH 26 oPECIES ilu iuEi-> 12 JAY i E A i i C0:J E L IM1T u.\ i hCiAil C uf LIMIT 94 4 8.00 19.04 128 .27 .39 115 29.20 6.92 142 . 13 .29 128 13.73 6.31 17 1 .80 .92 142 13.60 5.75 182 .93 .57 155 16.53 4.61 i 9 9 .93 .71 171 22.93 3.89 213 .27 .5 7 192 30.00 10.07 196 42.67 9.0 2 213 58.67 17.3 0 .PECILo iiU..uKi: 13 233 52.00 16.16 i. / . i .E An COn F 94 1 .20 1.25 115 .53 .51 SPECIES r; U> ifiLR 28 L 28 . 27 .39 DA Y MEAN CUNr LIMIT 142 . 13 .29 115 .27 .57 17 1 . 13 .29 14 2 2.00 4.30 1980 Yateley Common U minor SPECIES 43 SPECIES M Lu-» L) E l\ 30 Dm Y ME AN CONF L' A * MEAN CUNF LIMIT 213 1.73 2.30 94 1.8 7 1. a 5 233 1.73 2.33 155 .27 .57 213 .13 .29 SPECIEo 56 JAY MEAN CONF SPECIES ll u,IbEr i 31 1 42 .13 .29 u A * MEAN CUNt LIMIT 94 .13 .29 115 .13 .29 SPECIES 58 JAY 1'iEA.J CUNF 115 .13 .29 SPECIES ; i uibE .- R 32 171 < .27 .39 DAY MEAN CUNF LIMIT 94 .13 .29 SPECIES 59 DAY MEAN CUHF SPECIES w u •'i o EH 34 171 .13 .29 DAY MEAN CONF bIMIT 182 .53 .51 198 .13 .29 SPECIES 60 SPECIES i. J :i b E t< 35 DA* MEAN CONF !;/, i MEAN CUNF LIMIT 115 .27 .39 142 3.93 3.51 " •if 12b .13 .29 155 3.73 2.22 142 .40 .62 171 1.20 1. 17 155 .13 .29 1 S 2 1.07 198 .40 .46 213 .07 .14 SPECIES 66 2J3 .13 .29 DA* MEAN CONF 155 .13 .29 171 .53 .51 1.07 SPECIES NUi-1MEH 38 182 .90 OA* MEAN CUNF LIMIT 198 .40 .46 155 I . 27 2.09 171 1.80 1.44 182 5 .bO 1.98 SPECIES 67 195 3.07 1.96 JAY MEAN CONF LIMIT 213 4.80 2.55 171 .13 .29 233 2.13 1.54 19 8 .27 .57 2 3 3 .27 .57 : SPECIES :i J,ib EH 39 DA* HE AN CUNF L1HIT SPECItS 69 ! 23'3 . 40 .46 DA* Mi; AN CONF LIMIT 2; i . : 3 .29 SPECIES i! Ui. L i E K 40 L, h i MEAN CONF L1M IT SPECIES 70 199 .27 U/,1 MEAN CUMF LIMIT 233 . 40 .46 155 .07 .14 11781 2 .1.133 .29 SPEC I t-S ; i Jiurii, . 42 U i\ * ;i E A r. CONF LIM 1 r 115 .13 .29 SPECIES 71 142 .13 .29 DAY ME Ail CQilF LIMIT 17 1 . t) 7 .80 233 .13 .29 182 .53 .51 19» . 1 -> .29 Ulex minor 1980 Yateley Common SPECIES NUMBER 7 2 DAY MEAfJ CONF LIMIT 94 .87 1.03 115 2.67 2.35 126 2.33 1.79 142 .73 1.20 155 1.33 1.06 171 .13 .29 198 ,27 .39 SPECIES NUMBER 73 DAY MEAN CONF LlrtlT 94 S.07 5.59 115 13.93 7.70 128 14.87 o.20 142 14.4U 5.32 155 22.20 8.90 171 2 0.60 7.15 182 9.93 4.uJ 198 13.80 5.41 213 24.87 15.11 233 22.80 7.82 SPECIES wuMbER 78 DA* MEAN CONF L1M11' 115 .53 1.15 128 .33 .72 142 16.53 8.44 155 14.80 5.25 171 11.67 5.54 182 5.87 1 .99 198 5.33 2.36 213 2.80 1.31 233 1.07 .93 SPEC IlS .lu. ibER 82 Un* MEAN CUNF LIMIT 155 .41 .62 1981 Yateley Common Ulex europaeus unfertilised SPECIES UU.ioER 13 SPECIE'S Nil Kb EH 01 D A Y M E A i i CONF LIMIT DAY " ] E A u C O !v F 133 .20 .23 133 .27 .33 .13 .20 154 .13 .20 199 167 .13 .20 iPECIES NUMuEK 04 LIMIT SPECIES iJUnbEK 14 UAY .•IE AN COrlF 115 .07 .14 DAY MEAN CON F 133 .13 .20 115 .60, .46 154 .47 .59 133 1.40 .66 167 .40 .51 154 .87 .66 167 -.4 7 . 29 187 .53 .41 199 .20 SPECIES ii Ut'ti E K 06 .23 i) A Y MEAN C 0 tl F L1M IT 1 1 5 .53 .41 133 .80 2.35 SPECIES flUi'ibER 16 154 .53 .78 DAY M E A i CUNF UNIT 167 .40 .83 133 .33 .58 137 .47 1 .00 154 . 13 .20 199 .40 .75 167 .33 ,27 199 .07 .14 SPECIES NUMBER 08 DAY me An CONF LIMIT SPECIES tlUMriEK 19 154 .40 .46 Da Y MEAi'j ClJMF 167 .33 .40 115 .07 . 14 187 .27 .33 133 .13 .20 199 .07 .14 SPECIES ."Ili.ioER 23 ME Aii SPEC IES NUScJEK 09 DA* CONF LiHi MEAN CONF LIMIT 133 .20 .23 133 .40 .35 154 .07 167 1.00 .63 SPECIES NUMBER 25 187 .93 .53 DAY MEAN CUN F 115 .33 .34 133 .73 .53 St't-CIES uU.inER 10 154 .33 .27 L/t; i MEAN CGflF LIMIT. 167 .40 .41 US 3 . 1.24 187 .20 .23 13i 1.67 1.18 199 .07 . 14 154 2.53 1.47 167 4-. 2 0 1 .40 187 2.13 .91 SPECIES NUMoER 26 199 5.3 3 D A Y MEAN CONF B IM I T 2.21 115 10 .27 4.31 133 19 .13 5.55 SPECIES .ib.'oEf. 12 154 21 .53 B .02 ..En. CunF LIMIT 167 13 .33 4.44 1 15 .07 .14 167 4-3 .67 13.18 154 .07 .14 199 25 .67 167 . 13 .20 18 / . 13 . 2u 1981 YG U . europaeus unfertilised IPECIES MJMBEK 30 SPECIES iUJi-mtK 57 .' i E A : I CONE LIMIT DAY MEAN COhF LIMIT 1 L5 .07 ,14 199 .07 .34 -'V 154 .07 ,14 187 .13 ,20 199 .13 ,29 SPECIES Ab;.bEP. 58 u AY M E A N CUNF LIMIT .23 SPECIES NU.ibER 35 154 .20 jAY MEAN CUNF LIMIT 133 2.13 1.05 SPECIES NUMbER 6o 154 10.93 3.51 D A Y .•IE AN CONF LIMIT 167 5.73 1.94 115 .07 . 14 187 3.00 1.21 133 . 13. .20 154 .07 .14 167 .13 .20 SPECIES NU.-ioErt 3 S J A Y MEAN CUNF LIMIT 154 .73 ,88 65 167 .40 .59 SPECIES NUMBER LAY MEAN COhF LIMIT 187 10.13 3.93 115 1.47 .63 199 3.73 1.58 133 2.93 1.3 7 154 1.60 -4 o SPECIES DUMBER 39 b A * i ;EAN CONF LIMIT 66 199 .07 ,14 SPECIES NUMBER DA* ME A.N CONF LIMIT 154 .33 .40 167 .60 .55 fC IE S li u M u E H 4C 187 1.40 .72 ua Y ' i E A N CONF LIMIT 167 .13 .29 199 .20 .23 6 7 SPECIES NUMBER DAY MEAN CONF LIMIT 187 .73 .83 .'EC IES rib.iBER 42 199 3.40 5.83 MAY MEAW CONF LIMIT 167 .87 1.31 187 .07 .14 72 199 .20 .23 SPECIES NUMoER CAY MEAN CONF LIMIT 115 9.80 3.3U J 133 16.53 11.57 >t r.ClES fi'uMbc-K 43 154 15.87 17.43 u,U ME A;. CONF 15"4 . 07 .14 167 .20 .31 SPECIES NUMBER 73 l 87 3 . 80 4.32 D A Y MEAN CUNF LIMIT 19? 2.20 1.95 115 11.53 4.36 133 16.00 4.36 154 17.93 3 . bfi PECIES U ruiLIv 56 16/ 2 6.73 7 .04 J A Y HE Aw CUNF LIMIT lfiV 65.93 21 .Off 115 .07 ,14 199 100.^3 26.59 1 54 .07 ,14 167 . 13 • ,20 187 . 1 3 20 1981 YC U. europaeus unfertilised SPECIES nU.-ibEH 7 8 I) A 'I ME AIM CUNF LIMIT 103 4.53 2.70 154 22.67 7.67 167 15.93 5.10 187 7.67 3.99 L 99 2. 13 .94 SPECIES iiU.ldEK okl iiEAN CONF LIMIT U? .80 .99 133 .53 .41 SPECIES MU.-mEK 8 2 DAY MEAN CONF LIMIT 133 .13 .20 154 .13 .20 SPECIES MJKUEH 34 ME AM CONF LIMIT 115 .13 .20 •jAX 199 .07 .14 1980 Yateley Common Ulex europaeus fertilised SPECIES uU LM Li E R 01 SPECIES NUi'IUER 16 UAI ilEAii CUNF LIMIT DAY MEAN CUNF 213 .13 .29 155 .47 1.00 233 .07 .14 182 .07 . 14 SPECIES NU MBLR 06 SPECIES NUMBER 23 j A Y ME AH CONF LIMIT DAY MEAN CUNF 12 6 . o7 .54 128 .27 .25 1 B 2 .07 .14 2 i 3 .33 .34 233 1.00 .76 SPECIES NUISDER 25 DAY MEAN CONF 182 , .07 .14 SPECIES M U 08 213 .07 . 14 DAY MEAN CONF LIMIT 12b .07 .14 132 .07 .14 SPECIES NUMBER 26 DAY MEAN CUNF 129 15.00 4.92 SPECIES N ii .-.oER 09 155 13.33 2.91 D a * MEAN CONF LIMIT 182 21.00 5.27 128 .07 .14 213 28.00 6.45 i 8 2 .13 .20 233 31. o7 8.89 233 .07 .14 SPECIES NUMBER 30 SPECIES .JU i-l D t. R 10 DAY MEAN CONF U.\ Y MEAN CONF LIMIT 155 .13 .20 12 d 5.00 2.26 233 .40 .35 155 65 182 1 .87 1 .00 213 2.13 .84 SPECIES NUMBER 35 233 3.53 1.15 UAY MEAN CONF LIMIT 155 5.80 1.46 182 3.00 1.17 SPECIES Nu.'.rjLK 213 .33 .27 12 DAY MEAN CCU«F LIMIT 192 2.87 1.22 213 .47 .36 SPECIES f J U il B E R 38 23 3 .13 .20 DAY MEAN CUNF 155 .33 .50 182 8.20 3 .68 SPECIES NU;MOER 13 213 5.13 1 .78 uni MEAN CONE LIMIT 23 3 4.60 1 .05 126 .40 ,28 155 .27 ,33 233 .07 ,14 SPECIES NoMbER 40 DAI M E A N CONF 213 .13 .20 SPECIES iiU.uiEh 14 f 233 .13 .20 n A i *i E A; J CONF LIMIT 128 1.33 .91 155 .80 .bo SPECIES uU.-.bER 42 182 .93 .44 UAY ME A it CONF LIMIT 213 .27 .33 155 .27 ,57 233 .07 .14 182 .13 ,29 SPECIES MUMDEi< 15 i; K Y MEAi-l CUNF L IMIT 128 .40 .35 1980 Yateley Common Ulex europaeus fertilised SPECIES niifvbEK 43 uAY f 1EAN CONE LIMIT i b 2 .07 .14 213 1.07 1.27 233 1.53 2.87 SPECIES NUMBER 44 DAY rlEAN CONF LIMIT 155 .07 .14 182 .40 .So : SPECIES iU I'ibEK 56 DAY MEAN CONF LIMIT 155 .20 .23 SPECIES NUMBER 73 JAY MEAN CONF LIMIT 182 .13 .20 16.60 .36 1215b5 29.33 .73 2 7.40 .31 SPECIES NUM-.uER 61 211832 25.87 33 J A I MEAN CONF LIMIT 34.30 11.09 233 .07 .14 233 78 SPECIES NUMBER SPECIES NbMbER 62 DAY MEAN CONF LIMIT J MEAN COWF LIMIT .47 .07 .14 .55 213 151285 10.47 5.43 182 5.53 213 3.47 2.82 SPEC IEb NU.'bER 65 1.60 1.11 DAY MEAN CONF LIMIT 233 .72 128 .60 .46 155 1 .67 .65 182 .27 .33 SPECIES NUrtflER 81 DAY MEAN CONF LIMIT 128 .13 .29 SPEClbS NUMbEK 66 DAY MEAN CONF LIMIT 155 .20 .31 SPECIES NUMBER 6 2 DAY MEAN CONF LIMIT 155 .07 .14 SPECIES wU,:uEK 67 bAY MEAN CONF LIMIT 120 .40 .46 155 2.0 7 2 .03 1fi 2 1.00 .98 2 13 . 6u .55 233 1.67 1 .77 S P E C IE S i J U i: b r. K 70 b A Y MEAN CUN F L1M IT 155 .13 .20 132 .13 .20 SPECIES NUMBER 72 bo* , E A N CUNF LIMIT 128 6 . 1*3 1 .65 155 .87 .55 1 «2 .07 .14 213 .07 .14 1981 Yateley Common Ulex europaeus unfertilised SPECIES NUMBER 13 SPECIES NiJrincUl 01 DA* MEAN CONF LIMIT J AY . i E AN CUNE 115 .20 .31 .07 .14 133 .13 .20 iiv .07 .14 154 .13 .20 16 7 .20 .31 SPECIES NbiibEiv 04 0/v Y , lEAii CONF SPECIES N u i-l b E R 14 lis .20 .43 DA* MEAl'i CUNF LIMIT 133 .27 .33 115 . 87 12 15 4 1 .40 .86 133 .60 .,4o 16 7 I .0 7 .90 154 .47 .46 199 .07 .14 167 .93 .7 4 187 .33 .34 199 .07 .14 SPECIES iJiJMriLK 06 JAY -lEAi-i CONF 115 5 .33 2.48 SPECIES i-i UMbER 16 133 .13 1 .db DA* 1"! E A11 CONF LIMIT 3 .00 1.76 154 .07 .14 167 1 .80 .76 187 .13 .20 187 1 .47 .69 199 6 .20 3.03 SPECIES iJ UMbER 17 DAY MEAN CUNF LIMIT SPECIES tJUnuLK 08 154 .20 .31 uAY , lEAN CONF 167 .07 .14 lib .07 .14 16 7 .60 .55 18 / .40 .51 SPECIES NUribER 19 DAY MEAN CONF LIMIT 133 .13 .20 SPECIES rJJiit'.EH 09 : 154 .0 7 .14 J A I E AN CONF 115 .13 .20 154 .97 .14 SPECIES NUMHEF. 167 .40 .41 2 3 DA * MEAN CONF LIMIT i 3 7 .8 7 .55 115 .13 .20 199 . 13 .20 133 .13 .20 154 .33 .34 SPECIES I-MJ.iiMJ-: 10 u A Y IE AN CUNF SPECIES NUMtlEi; 25 115 2.53 .98 DAY HE AM CONF LIMI r 133 1.73 .80 115 .53 .41 154 2 .0 u 1.03 133 .07 .14 167 1.53 .81 154 .47 .51 i 87 1.2 0 .73 167 .07 .14 199 7.40 2.36 199 .07 . 14 SPECIES 'i.t.ts 12 SPECIES ri u i-i t» 1.1 i 2 6 .. E A CONF JA* MEAN CON F L1 M IT 13 3 .33 .27 115 22.60 7.15 154 .20 .23 133 19.87 4.81 187 . 27 .25 154 12.07 3.75 197 . 53 .41 167 21.20 5.75 199 .07 .14 1 b 7 40.27 7.9 1 199 2 2.07 7.60 1981 Yateley Common Ulex europaeus fertilised SPECIES NUMBER 30 DA* MEAN CUM F SPECIES NUMbEK 58 115 .07 .14 u A Y MEAN CUNF LIMIT 133 .07 .14 154 .40 .35 167 .13 . 2 0 187 .07 .14 199 .47 .29 SPECIES NUMBER 60 JA* i-iEAN CONF LIMIT 133 .13 ,20 SPECIES NUMBER 35 b A Y MEAN CONF LIMIT 133 4.13 1.53 SPECIES NUMBER 61 154 9 . 20 3.0 9 U A Y iEAN CONF LIMIT 167 3.73 1.34 167 ,07 ,14 197 2.80 1.19 199 .07 .14 SPECIES NUMBER 65 DAY MEAN CONF LIMIT 115 .80 .52 SPECIES NU.IBER 38 2.60 .59 i J 4 Y MEAN CONF LIMIT 133 187 10. 73 154 1.80 .82 199 4 . oil 2.1.68 08 167 .13 .20 SPECIES NUMBER 40 SPECIES NUMBER 66 DAY iEAN CONF LIMIT JAY MEAN CONF LIMIT 18 7 . 20 ,23 167 .13 .20 199 .07 ,14 187 .60 .46 SPECIES NUi-ibER 42 SPECIES NUMBER 67 Ur\ Y MEAN' CONF LIMIT DAY MEAN CONF 167 .07 ,14 133 .67 .65 187 .00 ,67 154 .87 1.19 199 .73 ,53 167 .60 .51 187 .60 .75 199 2.20 1.30 SPECIES NUMBER 43 DAY MEAN CONF I 54 .13 .20 SPECIES NUMbER 72 167 .67 .65 UAY MEAM CONF LIMIT 187 6 . 60 4.64 115 2 0.13 6.56 199 4 .53 2.49 133 26.13 10.70 lbi 65.93 45.70 : SPECIES -UMoEE f Jol' 1E A i * CuNF i>I i 11T SPECIES NUMBER 73 ME Mi CON .53 ,36 L hX c 133 .20 , J 1 1 i '•> 19.3 j ? 154 . 2 0 23 133 16.33 4 I 99 167 .0 7 ,14 154 21.40 H .09 1(57 167 23.7 3 5 .69 187 99.20 21 .02 species ; u;, i»t. 57 199 55.40 8 .46 l) !\ I MEAN CUNF LIMIT 133 . 13 ,20 199 .07 ,14 1981 Yateley Qommon Ulex europaeus fertilised PECIES NUMbEH 78 L»A * MEAN CONF LIMIT 133 5.73 3.02 154 20.13 12.75 167 8.8 0 5.28 187 7.67 3.65 199 2.40 1.20 K> PfCIEa NUMBER 81 ON u A Y MEAN CUNF LIMIT ON 115 .13 .20 133 .33 .34 PECIES NUi-iHGR 82 U A * •IE AN CONF LIMIT 187 .07 ,14 PECIES NUMBER 84 MEAN CONF LIMIT DM199 .13 .20 267. APPENDIX IX Variables used in regression analysis Variables 1-3 represent species breeding on gorse foliage; variables 4-6 represent all phytophagous species; variables 7-14 are independent variables. Simpson- Row log S log (N+l) log S log (N+l) Yule index 1 .6020 1.0970 1.0990 1.1460' 1.2900 2 .6020 1.4800 3.1250 1.1460 1.5720 3 .8450 1.4790 2.7030 1.2790 1.5440 4 .9030 1.4640 3.0300 1.3010 1.5240 5 .9030 1.5260 3.3330 1.2550 1.5690 6 .6990 1.5260 2.6320 1.1760 1.5890 7 .7780 1.3560 2.9410 1.0790 1.4270 8 .6990 1.4070 1.7240 1.1140 1.4500 9 .7780 1.7380 1.1360 1.1460 1.7800 10 0.0000 1.0330 1.0000 1.0410 1.3070 11 .6020 1.1820 1.4930 1.0410 1.3140 12 .6020 1.5150 2.3810 1.1760 1.6C90 13 .7780 1.2940 2 .3260> 1.1460 1.4230 14 .9030 1.4350 2.1280 1.2790 1.5420 15 .8450 1.4730 1.9610 1.1760 1.5680 16 .9030 1.3600 2.2730v 1.1760 1.4890 17 .8450 1.3910 1.2820 1.1460 1.5530 18 .6990 1.3600 1.9610 1.2040 1.5300 19 .9030 1.7230 3.0300 1.3220 1.7790 20 .8450 1.6960 2.5640 1.2790 1.7750 21 .7780 1.9630 1.8870 1.2040 1.9910 22 . 7780 2.0360 1.1630 1.2040 2.0660 log arc sin log Simpson- log Row shoot water shoot Yule index nitrogen toughness content length content 1 2.6320 1.6990 .7610 0.0000 1.5660 2 4.7620 1.7240 .7610 .2040 1.6010 3 3.7040 1.6430 .7820 .2550 1.5910 4 4.0000 1.9590 .7460 .4620 1.473Q 5 4.0000 2.398C .7870 .5680 1.4590 6 3.4480 2.5440 .7700 .6630 1.4170 7 4.0000 2.9400 .7520 .8330 1.3650 8 2.1280 3.0610 .6850 .9030 1.3070 9 1.3700 3.0790 .5700 .9140 1.3200 10 2.7780 1.3010 .8040 .0790 1.5910 11 2.5640 1.3010 .7990 .1760 1.6180 268. Appendix IX : Continued. log arc sin log log Simpson- Row shoot water shoot nitrogen Yule index toughness content length content 12 3.5710 1.6990 .7480 .3800 1.5940 13 4.0000 1.9540 .7020 .5050 1 5470 14 3.4480 2.4770 .6670 .6990 1.5050 15 2.9410 2.5560 .6960 .7990 i. ,910 16 4.0000 3.0410 .7160 .9030 f 4650 17 2.5000 3.0410 .6940 .9140 1.4440 18 4.1670 1.8450 .7570 .1760 1.5990 19 4.0000 1.6430 .7630 .4150' 1.6020 20 3.5710 1.9590 .6570 .4770 1.6040 21 2.1280 2.5660 .7130 .7160 1.3160 22 1.3330 3.0490- .6800 .8980 1.2550 log log log , log spider Row alkaloid isoflavone carbohydrate biomass content content content index 1 1.3420 .6720 .9490 1.1790 2 1.3010 .3980 .9540 1.2830 3 1.2040 .1460 .8570 1.3960 4 1.0610 -.0460 .9240 1.3120 5 .8450 -.0970 .9440 1.2010 6 .5440 -.1550 .9190 1.1990 7 .3010 0.0000 .8920 .9680 8 -.0970 .0790 .9030 1.2970 9 -.0460 .1140 .8980 1.3120 10 1.3980 .7160 .9590 1.4760 11 1.3010 .5560 .9540 1.4360 12 1.2790 .3010 .9290 1.6120 13 1.1140 .0410 .8920 1.5690 14 .9780 -.0970 .9340 1.4200 15 .7780 -.1550 .9340 1.5480 16 .3010 0.0000 .8920 1.4460 17 -.0460 .0410 .8980 1.5750 18 1.3010 .6530 .9490 1.2070 19 1.2550 .2040 .9640 1.1880 20 1.0000 .0790 .9680 1.1430 21 .7780 0.0000 .9340 1.2380 22 -.0460 0.0000 .9030 1.3640