BiologicalJournal ofthe Linnean Society (1995), 55: 109-127. With 8 figures
Food-plantfamilies of British insects and mites:
the influence of life form and plant family
LENA K. WARD, A. HACKSHAW* AND R. T. CLARKE
Institute of TerrestrialEcology, Furzebrook Research Station, Furzebrook Rd, Wareham,
Dorset BH20 7AS; * f i e WolfsonInstitute, St Bartholomew’sMedical College,
Charterhouse Square, London EClM 6BQ
Received 14 April 1994; acceptedfor publication 23 September 1994
The dissimilarities between 107 British plant families with respect to the insect and mite
species which feed on them were analysed using a principal co-ordinates analysis. The
relationships between the plant families were strongly influenced by the plant life forms.
Major groups were woody plants (trees and shrubs), aquatic plants and herbs. A wet to dry
gradient was distinguished, as were evergreen plants, and early successional plant families
with weeds and annuals. Taxonomically, plant families of the same order were closer together
if they were predominantly of the same life form. Fagales and several orders of monocotyledons
formed particularly clear groups. The three ‘nearest neighbours’ of each plant family based
on the dissimilarities measures were listed. These provide some interesting, but conjectural,
data on evolutionary aspects of plant families. This was illustrated briefly by the Cornaceae
and Euphorbiaceae. The underlying progressive evolution of plants from woody species and
wetter areas to herbs and annual plants of dry and cold places may be reflected by insect
and mite food plant family associations.
ADDITIONAL KEY WORDS:+volution
-taxonomy.
CONTENTS
Introduction . . . . . . . . . . . . .
Methods. . . . . . . . . . . . . .
D a t a . . . . . . . . . . . . . .
Statistical methods
. . . . . . . . . .
Results
. . . . . . . . . . . . . . .
Principal co-ordinates analysis . . . . . . . .
Life form and related features . . . . . . . .
Taxonomy
. . . . . . . . . . . .
. . . . . . . . . . . . .
Discussion
Acknowledgements . . . . . . . . . . .
References
. . . . . . . . . . . . .
Appendices . . . . . . . . . . . . .
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INTRODUCTION
The habitats of the food-plants of insects are influential in food-plant
preferences and host-switching in insects. Insect species are more likely to
come into close contact with particular suites of plants which grow in the
0024-4066/95/060109+ 19 $12.00/0
109
0 1995 The Linnean Society of London
110
L. K. WARD E T A L
same habitats (Chew & Courtney, 1991) or have ecologically similar niches
such as life form (Raunkiaer, 1934). The taxonomy of the plants is a very
important factor to insects and in turn relates to evolution (Mitter, Farrell &
Futuyma, 1991), biochemistry (Ehrlich & Raven, 1964) and other characteristics
(Bernays, 1991). All these features are interwoven strands in the preferences
of insects for different plants. In ecology, patterns of association at the family
level of taxonomic classification are sometimes thought to reflect some
fundamental and historical characteristics (Ricklefs, 1987), and this perspective
may help us to understand the complexities of insect food-plant associations
by reducing the detailed complications of variability in insect food-plants at
the species level.
Analysis of the extensive data in the Phytophagous Insects Data Bank
(PIDB) provided an opportunity to investigate the influence of some of the
features which are important in the preferences of insects for the different
food-plant families. (Total numbers and polyphagy were considered in Ward
& Spalding (1993).) Multivariate analyses have been used to show how the
plant families group together in relation to the insect species which feed on
them. Similar analyses were done for British macrolepidoptera (Holloway &
Herbert, 1979) and for leaf-chewing guilds on common woody plant species
in New York State (Futuyma & Gould, 1979), but this is the first time that
comprehensive data on all families of insects and plants have been used in
the study of food-plant preferences. In this paper the results of a principal
co-ordinates analysis (PCA) of the British plant families and insect species
display the major groupings of life forms of the food-plants. It also illustrates
part of the background of taxonomic preference, which is shown here by
plant families which are considered to belong to the same plant order, and
are therefore more closely related genetically and taxonomically.
METHODS
Data
The validity and interpretation of the original source records of insect
food-plants were considered by Ward (1988), and some descriptive statistics
were given in Ward & Spalding (1993). The basic data set used for the
multivariate analyses is the same as that in Ward & Spalding (1993), and
uses records for 6935 species (primary and secondary morphs of aphids on
different winter and summer food-plants are included as ‘species’) of insects
and mites and about 2000 plants.
The angiosperm plant families follow the arrangement of Cronquist (1981).
A few differences have been allowed in order to follow the customary usage
in Britain. The most important is the retention of the Corylaceae as distinct
from the Betulaceae. Conifers follow Flora Europaea (Tutin et al., 1964-80).
Nonnative plant families occurring in Britain are only included where these
have common species, for example Buddlejaceae. The fern families keep the
old arrangement of ferns in the second edition of Clapham, Tutin & Warburg
(1962). Coverage of insects feeding on non-vascular plants is incomplete (for
example Mycetophilidae feeding on fungi are not in the PIDB). Most of the
data are for species within primarily higher-plant feeding genera or families,
INSECT FOOD-PLANTS, LIFE FORM AND TAXONOMY
111
for example Anthomyiidae. Nevertheless the available data on lower plants
are still thought to be of interest and so are included as group categories of
M u d , Lichenes, Fungi and Algae. The plant families in the analysis are
listed in Appendix 2.
The life forms of plants as classified by Raunkiaer (1934) have seven
major sub-divisions. These are therophytes (overwintering as seeds, i.e.
annuals), hydrophytes (water plants), helophytes (marsh plants), geophytes
(overwintering buds below soil level e.g. bulbs), hemicryptophytes (buds at
soil level), chamaephytes (woody or herbaceous plants with buds above the
soil but below 25 cm), and phanerophytes (woody plants with buds more
than 25 cm above soil level). The latter are particularly important because
insects are most abundant on woody plants (Lawton & Schroder, 1977;
Strong, Lawton & Southwood, 1984). Phanerophytes in this paper were
therefore further sub-divided into trees (Mega and mesophanerophytes with
overwintering buds above 8 m) and shrubs (micro and nanophanerophytes
with buds between 25 cm and 8 m). The numbers of each of the eight life
forms as described above were totalled for the plant species in each plant
family in Britain using Clapham, Tutin & Warburg (1962). This is reasonably
reliable except for the ‘microspecies’ of Rosaceae and Compositae.
The insect families are those of Kloet & Hincks (1964-78) with a
few updating alterations, notably in psyllids (Aphalaridae-Triozidae), aphids
(Mindaridae), coccids (Kermisidae) and Lepidoptera (Choreutidae). Mite
families are those of Evans, Sheals & Macfarlane (1961) & Krantz (1970).
Statistical methods
The complete database includes some 240 plant families of which 120 are
British and are native, or if introduced occur commonly. The main aim of
the analysis was to assess the dissimilarity between the British plant families
with respect to the insect species which feed on them. To simplify the data
and to highlight relationships, only the 107 plant families which had two or
more insect species using them as food plants were included. Insect species
which fed only on one plant family were excluded, because they do not
indicate the extent of dissimilarity between two plant families.
Relationships between plant families were determined by a principal coordinates analysis (PCA) (Krzanowski, 1987). This is a metric multidimensional
scaling technique which ordinates the observations in r dimensions (r is
usually 2 or 3) so that the distances between any two observations in the
ordination space best represent the estimated dissimilarity between the two
observations.
The dissimilarity, dq between each pair ij of plant families, was quantified
using the Czekanowski coefficient (Krzanowski, 1987), as follows:
Plant Family i
Number of insect species
Plant Family j
Number of insect species
Host
Absent
b+c
dissimilarity = d,,=2a+b+c
Host
a
Absent
b
C
e
L. K. WARD ET AL
112
This measure is appropriate as it does not involve the e insect species
which do not feed on either plant family i or j, and therefore give no
indication of similarity or dissimilarity.
RESULTS
The measures of dissimilarity describe those plant families which are the
most closely related to a particular plant family according to the associated
insects. Appendix 1 gives the three ‘nearest neighbours’ of each plant family.
The association with life form and taxonomy is often apparent. For example,
Scrophulariaceae had Labiatae as the nearest neighbour and Plantaginaceae
as the third nearest. Both of these might be expected on taxonomic grounds,
and Jolivet, Petitpiere & Daccordi (1986) and Stroyan (1964) also noted
closely related pairs of insect species on Scrophulariaceae and Plantaginaceae.
However the second associate was Cruciferae, probably due to similar habitats
with hemicryptophytes and therophytes, as this family is biochemically and
taxonomically very different.
There may also be a swamping effect due to polyphagous species in larger
families. Thus Resedaceae and Cruciferae are generally agreed to be closely
associated taxonomically, but only the Resedaceae have Cruciferae as the
nearest neighbour. The Cruciferae are more closely associated with families
with weeds (Chenopodiaceae, Solanaceae and Papilionaceae).
The nearest neighbours data may also be examined from a plant
evolutionary view. Two examples are cited. The Cornaceae in the Cornales
may have evolved near the Araliales (Becker, 1973). However, Cronquist (1981)
believed that they were derived from the Rosales, near the Hydrangeaceae and
Grossulariaceae. The nearest neighbours to Cornaceae are Rhamnaceae,
Aceraceae and Grossulariaceae. Even the raw data with the more polyphagous
insect species removed shows no relationship to the Araliales (Table 1). The
TABLE1. Total numbers of linkages in records in the PIDB for important food-plant families
for insect/mite species recorded feeding on Euphorbiaceae and Cornaceae (All=total insects/mites
including all polyphagous species feeding on the 20 plant families with the highest numbers:
<6 fams=insects/mites, with less than six food plant families, feeding on all plant families
with two or more linkages)
No species
Numbers of recorded linkages
Insect species on Cornaceae
45 (all)
160 Rosaceae, 59 Cornaceae, 50 Papilionaceae, 45 Oleaceae, 44 Salicaceae, 37
Fagaceae, 36 Compositae, 32 Ericaceae, 26 Aceraceae, 23 Betulaceae, 2 1 Solanaceae,
20 Caprifoliaceae, 19 Corylaceae, 16 Araliaceae, 15 Rhamnaceae, 15 Grossulariaceae,
13 Ulmaceae, 11 Cruciferae, 11 Chenopodiaceae, 10 Hippocastanaceae
21 ( < 6 fams)
24 Cornaceae, 20 Rosaceae, 4 Grossulariaceae, 4 Fagaceae, 4 Apocynaceae, 3
Oleaceae, 2 Vitaceae, 2 Salicaceae, 2 Ericaceae, 2 Caprifoliaceae, 2 Betulaceae
11 on Cornaceae only (24% of total species)
Insect species on Euphorbiaceae
5 1 (all)
105 Euphorbiaceae, 137 Compositae, 57 Cruciferae, 57 Papilionaceae, 36 Rosaceae,
35 Labiatae, 27 Scrophulariaceae, 27 Ranunculaceae, 23 Polygonaceae, 22 Solanaceae,
18 Chenopodiaceae, 17 Malvaceae, 17 Umbelliierae, 17 Liliaceae, 15 Caryophyllaceae,
14 Primulaceae, 14 Onagraceae, 14 Gramineae, 12 Plantaginaceae, 12 Convolvulaceae
32 ( 1 6 fams)
72 Euphorbiaceae, 6 Scrophulariaceae, 4 Linaceae, 3 Compositae, 2 Urticaceae, 2
Ranunculaceae, 2 Hypericaceae
23 on Euphorbiaceae only (43% of total species)
INSECT FOOD-PLANTS, LIFE FORM AND TAXONOMY
113
Grossulariaceae appear more important although they have relatively few
plant species in Britain. A second example is the Euphorbiaceae, a family
which is relatively isolated taxonomically with respect to the phytophagous
insects and mites, as 43% are entirely specific. The family is thought to be
near the Celastrales, or possibly the Sapindales, by Cronquist (1981). The
Geraniales and Malvales have also been suggested (Becker, 1973). The nearest
neighbours are Papaveraceae, Linaceae and Malvaceae (Appendix I) while
the Scrophulariaceae and Linaceae are important in the raw data on the
insects feeding on <six plant families (Table 1). There is probably some
taxonomic significance in the association of the Euphorbiales to the Linales,
especially as the latter have few plant species in Britain. The Malvales appear
as associates, but there is no evidence for the Geraniales, Celastrales or
Sapindales.
Principal co-ordinates analysis
The PCA was performed using the dissimilarity coefficients {dq} and the
statistical package GENSTAT (Genstat 5 committee, 1987). The first two axes
are the most important and are shown in Figure 1, where all the names of
the plant families are given as abbreviations (The full names are in Appendix
2.) These two axes account for 6% of the variation, which is not surprising
given that there are 106 possible axes.
The relationships between the plant families, as represented in the
ordinations, are considered from two viewpoints, the plant life forms (Fig. 2)
and the major taxonomic groups of plant families (Figs 3-6). The biochemistry
of secondary plant compounds is another important angle, and will be
considered in another paper. For the life forms, the first two axes clearly
separate the plant families with woody plants (trees and many shrubs) in the
upper right quadrant, while the aquatic and marsh plants are intermixed in
the lower right quadrant. Non aquatic and marsh herbs are in the left hand
quadrants, while hemicryptophytes are predominantly in the left upper
quadrant. Taxonomically, the first two axes clearly separate the
monocotyledons (composed primarily of Alismatidae and Commelinidae) from
the dicotyledons. Approximately two thirds (lZjl7) of the monocotyledons
(and all the Alismatidae) are concentrated in the right lower quadrant of
Figure 1.
More detailed aspects of the relationships between plant families are
considered under life form (and related features) and taxonomy.
Life form and related features
Figure 2 shows the most frequent life form for the plant families in the
analysis (refer to Figure 1 for the plant family names). Fungi, algae, mosses
and lichens are included. The major gradients are related to the woody
plants, aquatic and marsh plants and to other herbs of various life forms.
Those herbs with a tendency to drier ground are in the upper left quadrant.
These three major groups will now be described together with other subsidiary
clusters of habitat or plant characteristics which affect the insects and can
be recognized in the figure.
L. K. WARD E T A L
114
0.5
0.4
0.3
0.2
uos
Pira
cu
Him
0.1
.-
v)
2
0.0
-0.1
Hip
c.n
-0.2
-0.3
wa
-0.4
wr WI
~srm
J
-0.4
I
I
I
I
I
I
I
I
I
-0.3
-0.2
-0.1
0.0
0.1
0.2
0.3
0.4
0.5
Axis 1
Figure 1. The first two axes of the principal co-ordinate analysis (PCA) of the similarity
between British plant families determined by the insect species which feed on them. The
names of the plant families are abbreviated and the full names appear in Appendix 2.
Woody plants (phanerophytes and chamaephytes)
Eight out of nine plant families in which trees are the major life form are
located in the upper right quadrant with most of the trees well over to the
right. Families with shrubs are primarily towards the centre of the upper
right quadrant but there are scattered outliers, mainly explained by the good
representation of other life forms in the family. The Rosaceae are placed
highest on axis 2, and this family has many hemicryptophytes. The
Buddlejaceae are close to the hemicryptophytes in the quadrant representing
the drier situations (see below). The Solanaceae are an outlier in the upper
left quadrant.
One of the distinguishing reasons for the clustering of trees and shrubs is
that plants with woody stems are attacked by several insect families specializing
almost entirely in wood and bark feeding. This applies particularly to a
number of families of Coleoptera, especially Cerambycidae and Scolyhdae.
Many of these insects are not very specific to plant family although they do often
INSECT FOOD-PLANTS, LIFE FORM AND TAXONOMY
0.5
0
0.4
O
115
..
@.
0
0.3
*
0
0.2
0
0.1
0
N
Q
v)
3
0.0
0
0
a
-0.1
-0.2
I
-0.4
I
X
-0.3
-0.2
-0.1
0.0
0.1
0.2
0.3
0.4
0.5
Axis 1
Figure 2. The predominant life forms of the plant families in the PCA of Fig. 1.
: trees
(phanerophytes 1) ; 0: shrubs (phanerophytes 2) ; *: dwarf shrubs etc. (chamaephytes) ; A :
rosette plants etc. (hemicryptophytes) ; x : bulbous plants etc. (geophytes); 0 : annuals
(therophytes); 0 : marsh plants (helophytes); @ : aquatic plants (hydrophytes) ; + : ‘lower
plants’ (algae, fungi, lichens, mosses).
discriminate between gymnosperm and angiosperm families. The preference for
woody stems will also be one cause of the gradient relating to stature of the
woody plants with trees more to the upper right of Figure 2 and shrubs to
the centre. More insects feed exclusively on the larger volumes of wood
presented by trees than on the slender branches of smaller shrubs.
It must not be supposed, however, that the wood-feeding insects are the
only cause of the woody plant gradient; there are other families which
specialize in feeding on the leaves and shoots of trees and shrubs, for
example calliphorid aphids, sawflies and various families of microlepidoptera.
Plant families with evergreen species of trees, shrubs and dwarf shrubs
(chamaephytes) form a loose grouping towards the centre of the figure.
These include Aquifoliaceae, Araliaceae, Buxaceae, Cistaceae, Cupressaceae,
Ericaceae, Pinaceae, Plumbaginaceae, Tamaricaceae, Taxaceae, Vitaceae and
some Caprifoliaceae. Scale insects (Coccoidea) are important in this clustering,
for example 17 coccids are recorded for the evergreen Ericaceae (274
phytophagous insects in total), while the deciduous Betulaceae, which often
occur in the same heathland habitats, have 15 (600 total). Generally, more
coccid species are associated with evergreens or with woody stems, although
Cornell & Kahn (1989) found that ‘evergreenness’ did not account for residual
variation in their analysis of arboreal guild structure. This was possibly
because their guilds were rather broadly defined. Association with evergreen
plants would be expected from insects which have relatively immobile
females; some last instar larvae and adults of coccids are virtually legless
116
L. K.WARD E T A L
(Kosztarab & Kozar, 1988). These insects are therefore vulnerable to losses
with the falling of deciduous leaves, unless their generation times are fully
seasonally adapted. Indeed, two example genera in the PIDB data have more
species recorded on evergreens than deciduous-Euonymus europaeus has two
species and E. japonicus has three, while Viburnum lantana and V; opulus have
no records, compared to two on V; tinus. Scale insects are also more frequent
on Gramineae and Cyperaceae, where many species are also wintergreen.
This could also be a reason for the more frequent representation of scale
insects on Gramineae and Cyperaceae, many of which are also wintergreen.
Aquatic and marsh plants (hydrophytes and halophytes)
Twelve families in the distinctive aquatic lower right quadrant of Figure 2
are hydrophytes (aquatic plants which may be submerged, floating or
emergent). Only three families are mainly helophytes (marsh plants).
Monocotyledons are obviously an important part of this aquatic gradient, but
there are several dicotyledonous families with the same habit. Additionally,
the reliability of the analysis for these plants is less because many of the
families are small and have few insect feeders. Indeed several (omitted)
aquatic families had no records of insect feeders (Ward & Spalding, 1993).
It has also been shown that herbivory in general is less on water plants
(Warren, 1993).
The insects that feed on aquatic plants are fairly distinctive, and include
species in various families of Diptera, Lepidoptera Chrysomelidae and
Curculionidae. Some genera, for example Bagous (Curculionidae) show
particularly good radiations of species in the aquatic habitat.
Towards the centre and left of this quadrant the plant families are of
various life forms but include families which have a proportion of marsh or
aquatic species or live in damp habitats. Cyperaceae for example have 65
hemicryptophytes and 45 marsh plants, while most Juncaceae and many
Equisetaceae live in wet or damp places even though the majority are
hemicryptophytes or geophytes respectively. Gramineae are more centrally
placed and have a higher proportion of annuals and plants of dry habitats.
The algae, fungi, mosses and lichens also appear in the central left part
of the figure which is considered to represent the damper habitats. Although
the horsetails (Equisetaceae) are positioned here, the important fern family,
Polypodiaceae, is placed nearer the herbs, where drier habitats are represented.
There does not appear to be a cohesive group of families with a coastal
element. Plumbaginaceae are not positioned too far from Zosteraceae, but
Chenopodiaceae are at a distance.
Herbs (hemimyptophytes, geophytes and therophytes)
The left side of Figure 2 is almost entirely composed of plant families of
herbs. The upper quadrant is mainly of hemicryptophytes (rosette herbs and
others), while therophytes (annuals) tend to be more frequent on the fringes
of the figure. There is a gradient towards the woody plants on the right of
this side of the ordination space. Plants with bulbs and corms etc. (geophytes)
are placed mainly in lower half of the figure near the herbs and aquatic
families. The Araceae are an extreme outlier between the aquatic and herb
gradients.
INSECT FOOD-PLANTS, LIFE FORM AND TAXONOMY
117
The placing of these herb families could be due to several factors. These
include the various life forms, a wet to dry gradient, early successional and
weed habitats and the biochemistry.
Many of the families towards the outer fringe of the upper left quadrant
contain annuals, weeds and early successional plants of drier places. These
include Caryophyllaceae, Chenopodiaceae, Compositae, Cruciferae, Labiatae,
Papaveraceae, Papilionaceae, Plantaginaceae, Polygonaceae, Scrophulariaceae
and Solanaceae. This clustering is probably determined mainly by the
polyphagous macro-moths and Hemiptera.
The families with annuals to the bottom of the figure tend to occur in
wetter places. Families with geophytes also tend to occur in the damper
areas. Many geophytes have a poor fauna (Ward & Spalding, 1993) and
Diptera are an important group of associated insects.
The gradient towards woody plants in the upper part of the diagram is
shown by various families with mixed life forms, for example Papilionaceae.
Families with mainly chamaephytes occur in the herb part of the clustering
figure, but towards the centre there is a transition to woody shrubs. The native
Celastraceae and the introduced Tamaricaceae, Vitaceae and Buddlejaceae are
the shrubs closest to the herbs. The Papilionaceae are the most distant of
the herbaceous families in which hemicryptophytes are preponderant, but
this family has a good representation of shrubs in the Genisteae. Conversely,
the Rosaceae are placed well into the tree and shrub gradient but do have
many species which are hemicryptophytes.
Secondary plant biochemistry may be particularly involved in determining
the position of some of the outer families. These are the families which are
known to have various toxic substances for example Cucurbitaceae, Solanaceae
and Papaveraceae.
Taxonomy
Taxonomic clusters of plants are represented simply in the PCA by circling
together plant families in each sub-class that are in the same orders of
Angiosperms (Figs 4-8). The orders are those classified by Cronquist (1981),
used as an excellent recent summary of the taxonomy of Angiosperms.
However, a number of these families are very uncertainly placed in the
plant orders and have been variously classified at different times in the past
by various authorities (Becker, 1973). The ‘lower plants’ and ferns and
conifers appear in Figure 3. Important insect families associated with the
various taxonomic groups of plants will be examined in detail in a later paper.
The ‘lower plants’ here include ferns and horsetails as well as algae, fungi,
mosses and lichens (Fig. 3). These groups are fairly closely clustered by
insects near the main plant families of the damper habitats and the
monocotyledons. The Polypodiaceae are more separated, reflecting mainly
the records of polyphagous species feeding on Pteridium aquilinum. Taxaceae,
Cupressaceae and Pinaceae are reasonably close together and positioned
towards the lower section of the trees and among the shrubs where there is
also a grade towards the monocotyledons and wetter habitats.
In the Hamamelidae the Fagales demonstrate a particularly close affinity
by having the closest cluster in the analysis (Fig. 4). Myr’icaceae are among
L. K. WARD E T A L
118
a5
0.4 0.3
-
0.2
-
'Lower plants'
and conifers 0
..
. * ..
.
. ..
:w .
.; ..
0
.
.
.
**
c\I
* .
v)
2 0.0
0.
.. .
**
. *
*.
0.1
*
**
. .
-0.1
-a2
.
I-
0 .
i
-a4
-a3 -a4
-0.3 -a2
-ai
0.0
ai
0.2. .
0
0.3
a4
c
Axis 1
Figure 3. 'Lower plants' (algae, fungi,lichens, mosses), ferns and conifers in the PCA of Fig. 1.
a5
.
L
a4 -
Magnoliidae 0
Hamamelidae 0
0
.
:
.
-a3
-
-a4
-a4
I
I
I
-0.3
-a2
-ai
I
0.0
I
0.1
0
.
.
.
0.2
0.3
I
1
a4
0.
Axis 1
Figure 4. Magnoliidae and Hamamelidae in the PCA of Fig. 1.
the shrubs and towards the damper gradient. Platanaceae being introduced
in Britain have a very poor fauna and may not be reliably positioned. The
Urticales however demonstrate a phenomenon that is apparent in many of
INSECT FOOD-PLANTS, LIFE FORM AND TAXONOMY
119
a5
a4
0.3
a2
0.1
rJ
0.0
v)
2 -0.1
0
-0.2
0
-a3
-a4
a4
a3
-a2
-a1
0.0
ai
0.2
0.3
a4
a
Axis 1
Figure 5 . Rosidae in the PCA of Fig. 1.
the clusters in the analysis. This is that families in orders which have quite
different life forms, such as trees and herbs, are much more separated. In
the Urticales this is between the trees of the Ulmaceae, and the herbs of
the Cannabiaceae and Urticaceae.
In the Magnoliidae the aquatic habit and its fauna places the Nymphales
among many of the monocotyledons (Fig. 4). The Ranales span the shrubs
of the Berberidaceae (poor fauna in Britain) and the herbs of the
Ranunculaceae. The mainly annual plants of the Fumariaceae and
Papaveraceae with their toxic secondary chemicals appear on the bottom left
of the figure.
The Rosidae are particularly notable for the number of orders which are
stretched between the various life forms (Fig. 5 ) , the Rosales themselves
having the greatest spread. Few of these families are on the extreme left of
the diagram, where the early successional plants, annuals and plants of high
toxicity and possibly later evolution occur.
The Asteridae lie mainly to the left in the analysis (Fig. 6) with only the
Scrophulariales having the Oleaceae stretching across to the trees. There are
several families in the aquatic sector, and a good example of an order
with families along the wet/dry gradient is the Solanales (Menyanthaceae,
Polemoniaceae, Convolvulaceae and Solanaceae).
The families of the Dilleniidae are mainly in the middle parts of Figure
7. In the Malvales there is a marked difference between the Malvaceae with
many herbs and the trees of the Tiliaceae. The Violales are a loose-knit
group of families with few annuals and with rather specific insects. Most of
the Caryophyllidae are towards the left of Figure 7, although the
Plumbaginaceae have a few shrubby species.
L. K. WARD ET AL
I20
a5
.
L
Dilleniidae
0
Caryophyllidae 0
0.4 -
0
0.3 -
e
J
0.2
-
0.1
-
In
2
0.0 -
-0.1 -
-a2
-a3
-a4
. *
..
:
.
.
-
4
...
-a4
-0.3
-a2 -ai
0.0
0.1
0.2
a3
c
a4
Axis 1
Figure 6. Dilleniidae and Caryophyllidae in the PCA of Fig. 1.
1
.
0.5Io.4
Asteridae @
...
a3
0.2
4c
.
0.1
In
2 0.0
-a1
-0.2
-0.3
-a4
Axis 1
Figure 7. Asteridae in the PCA of Fig. 1.
Most of the monocotyledons are positioned in the aquatic area (Fig. 8)
and there are several fairly closely related families in the Alismatales,
Sparganiales and Cyperales. The terrestrial families of the Liliales (Liliaceae,
INSECT FOOD-PLANTS. LIFE FORM AND TAXONOMY
121
0.5
Monocotyledons 0
w
:
0.4
0.3
..
w
f
w
w
w
0.2
* w
0.1
B
0.0
w
-0.1
w
w
w
.
v)
-\
ww
-0.2
-0.3
-a4
Axis 1
Figure 8. Monocotyledons in the PCA of Fig. 1.
Amaryllidaceae and Dioscoreaceae) and the Orchidales are mainly in the
lower quadrants of the figure, sharing both the habitat and some taxonomic
features. Apart from the Cyperales, the fauna of most of the families of
monocotyledons is low in numbers, so that the reliability of analysis is less.
DISCUSSION
The major subdivisions of life forms of plants (Raunkiaer, 1934) have been
recognized as important factors in grouping plant families. Insect and mite
species feeding on more than one plant host were used in the PCA of foodplant records, and so this analysis emphasizes the characteristics of these
species, as compared to the majority of species which are restricted to only
one plant family. However, the use of plant families as the unit has reduced
the effect of life forms because many plant families have species with different
life forms, rather than just the predominant type used in the analysis.
The taxonomy, including morphological and chemical similarities between
plants, has also influenced the clustering. Plant families in the same order
are often fairly close in the analysis provided that they fall within the same
life form type. The description of these interrelationships is complicated,
because the life form itself is a taxonomic feature of the plants. Many of
the earlier evolved families are considered to have been woody, and there
has also been progressive evolutionary adaptation to arid regions and to
polar and high altitudinal conditions (Takhtajan, 1991). In these regions there
are many more annual plants and herbs. There have also been corresponding
changes in secondary plant chemistry (Cronquist, 1981). In some ways
therefore the results produced by the PCA can be thought of as showing
122
L. K. WARD ET AL
the pattern of evolutionary adaptation in the plants and in their associated
phytophages.
Life form is a rather mixed classification, as it includes elements of both
habitat and structure. This is especially true of aquatic and marsh plants,
where the habitat is the determining factor. The terrestrial plant classification
is more clearly based on structure. However the importance of life form is
greater than that of the taxonomy when families in an Order are of both
woody and herbaceous types. These Orders are stretched out along the
gradient of trees to annual herbs and geophytic plants. For example even
though trees and their ground floras in woods are in the same habitat they
are less likely to share phytophagous faunas than are species of the canopy
or of the field layer. Oak trees and bluebells occur together in UK woodlands,
but have nothing in common in life form, taxonomy or insect fauna.
The relative emphasis on taxonomy or ecology as determinants of patterns
in food plants of insects varies according to the particular plant or insect
families or groups being studied, the taxonomic levels (species through to
orders) and the analytical methods. Taxonomy was more important in a
numerical analysis of Lepidoptera feeding on different species of woody plant
(Holloway & Herbert, 1979) and in gall midge host plant evolution (Roskam,
1985). Habitat and phylogenetic associations were noted in leaf-chewing
guilds on several woody plants (Futuyma & Gould, 1979), while Anderson
(1993) considering weevils, and the present study found that ecological factors,
such as structure and habitat, outweighed taxonomy.
Insects have major adaptations-ecological, morphological physiological and
behavioural-to particular types of habitats (Bernays & Chapman, 1994), and
these are reflected in the results from the PCA. Adaptations are obvious in
aquatic faunas, but arboreal and ground faunas also have basic differences,
for example in locomotion on the plants and in the adapted predators
encountered. Heteroptera for example, are thought to have been originally
ground dwelling predators (Schaeffer, 1981) and to show increasing arboreal
and phytophagous adaptations. Differences in layer communities were observed
in various studies noted by Lawton (1983), though he was considering species
richness rather than inter-relationships. Habitat structure is a determinant of
predator diversity in spiders (Hurd & Fagan, 1992). Even for grassland
communities, there are differences between the insect communities associated
with tall herbs and rosette plants. The fauna of Cirsium acaule, for example,
is affected more by the microclimate than is Centuureu scabiosu, which is
affected by grazing and grassland management (Volkl et ul., 1993). Geophytic
plants differ from other field layer species in that insects feeding on these
plants must be particularly efficient at finding the often ephemeral overground
vegetation and/or be adapted to feeding on underground bulbs and corms.
This strategy, which occurs in several groups of monocotyledons (probably
with chemical defences also), results in relatively few phytophagous insects
(Ward & Spalding, 1993). Annual plants produce problems to insects in their
ephemeral appearance in different places and sometimes in their small size.
Adapted insect species must be mobile and in some groups polyphagy is
more common. Larger insects, like Macrolepidoptera may exhaust the
resources of small plants and feed on different species nearby. A few specific
species to annual plants (and incidentally sometimes to seeds), have evolved
INSECT FOOD-PLANTS, LIFE FORM AND TAXONOMY
123
strategies of staggered diapause of eggs or pupae to survive poor years for
annuals, e.g. wheat blossom midge Sitodiplosis mosellana (Gehin).
It was hoped that insect food-plant family data from all insect orders
would provide an additional taxonomic character of use in angiosperm
taxonomy, although this has always been somewhat controversial (Hedberg,
1979). For fungi, Dalgren (1979) thought that host family taxonomy caused
greater conjecture about angiosperm relationships. The value of food-plant
data in plant systematics is considered to be unproven so far for the insects,
and indeed some recent studies at the species level have tended towards
discounting detailed parallel cladogenesis between insects and plants (Miller,
1987; Anderson, 1993); there were some phylogenetic affinities but more
similarities related to plant habitat. These suggested that convergent evolution
in host properties and habitats made associated faunas poor indicators of
phylogenetic relationships. However, there are very few extensive data sets
for testing. Although the PIDB is limited because it is composed of British
insects and mites, it does include continental European data for many of
these species. However, such data is still not fully representative of the
northern temperate area. Nevertheless Appendix 1 on nearest neighbours
does provide some interesting conjectures about inter-relationships of plant
families. Refined statistical analyses and data could be used in the future. It
is the oligophagous species that are clearly important (Thorne, 1979; Futuyma
& Gould, 1979) and not the very polyphagous species. Analysis could be
repeated after deleting some categories of polyphagous species. Other groups
could also be omitted depending on objectives. Thus wood and bark feeders
could be omitted as they are a strong influence in the segregation of woody
plants and herbs.
This paper has considered relationships of the plant families as seen by
the insects feeding on more than one plant family. However little detail has
been presented about the insect families with many specific species and the
complex subject of evolutionary history. It is intended to describe this side
of insect and mite food-plant interrelationships in subsequent work.
ACKNOWLEDGEMENTS
The extensive work of compilation of the PIDB would have been impossible
without the help and expertise of numerous colleagues and experts, and we
particularly thank H. Brundle, C. Brown and D. F. Spalding.
The Nature Conservancy Council supported the project from 1977- 1980.
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INSECT FOOD-PLANTS, LIFE FORM AND TAXONOMY
125
APPENDIX 1
The three nearest neighbours of each plant family or group in an average linkage clusters
analysis of 120 families (The abbreviations used are the same as in Appendix 2)
Nearest neighbours
~
Family
First
Second
_
~~
Aceraceae
Algae
Alismataceae
Amaryllidaceae
Apocynaceae
Aquifoliaceae
Araceae
Araliaceae
Balsaminaceae
Berberidaceae
Betulaceae
Boraginaceae
Buddlejaceae
Butomaceae
Buxaceae
Callitrichaceae
Campanulaceae
Cannabiaceae
Caprifoliaceae
Caryophyllaceae
Celastraceae
Ceratophyllaceae
Chenopodiaceae
Cistaceae
Compositae
Convolvulaceae
Comaceae
Corylaceae
Crassulaceae
Cruciferae
Cucurbitaceae
Cupressaceae
Cyperaceae
Dipsacaceae
Elaeagnaceae
Empetraceae
Equisetaceae
Ericaceae
Euphorbiaceae
Fagaceae
Fumariaceae
Fungi
Gentianaceae
Geraniaceae
Gramineae
Grossulariaceae
Haloragaceae
Hippocastanaceae
Hippuridaceae
Hydrocharitaceae
Hypericaceae
Iridaceae
Juncaceae
Juncaginaceae
Labiatae
Tili
Lich
Lemn
Irid
Fuma
Aral
Fuma
Aqui
Port
Tama
Sali
Papa
Poly
Call
Aqui
Cera
Vale
Urti
Olea
Polg
Vita
Call
Sola
Dips
Papi
Chen
Rham
Betu
Papa
Chen
Verb
Pina
Junc
Bora
Tama
Eric
Alis
Myri
Papa
Betu
Port
Pina
Fuma
Cras
CYPe
Vita
Hipu
Acer
Halo
Lemn
Gera
Lili
CYPe
Cera
Comp
34.8
64.9
33.3
20.5
40.0
34.8
28.6
34.8
54.5
27.3
58.9
34.6
21.8
33.3
20.5
40.0
25.6
37.6
26.5
37.2
22.2
40.0
41.4
14.7
38.0
27.6
30.0
51.6
30.0
39.8
31.6
34.3
49.7
28.2
25.0
10.8
11.8
29.1
29.3
56.6
44.4
8.2
40.0
27.1
39.3
23.9
57.1
29.2
57.1
46.2
21.5
33.7
49.7
28.6
37.5
Ulma
Musc
Hydr
Lili
Verb
Buxa
Apoc
Capr
Fuma
Rham
Faga
Dips
Capr
Halo
Taxa
Buto
Papa
Chen
Aral
Comp
Verb
Jung
cruc
Plum
Labi
Sola
Acer
Faga
Gera
Sola
Fuma
Taxa
Gram
Cras
Berb
Saxi
Cist
Sali
Lina
Cory
Bals
Lich
oxal
Papa
Junc
Acer
Pota
Tili
Pota
Pota
Conv
Sola
Gram
Call
Scro
33.6
15.4
26.1
18.7
31.6
20.5
28.6
25.0
40.0
19.5
56.6
28.2
17.5
28.6
16.0
33.3
25.0
22.9
25.0
33.7
21.4
28.6
39.8
13.6
37.5
23.1
20.1
48.6
27.1
36.6
26.7
13.3
39.3
21.2
18.7
6.1
6.1
28.3
25.0
48.6
40.0
5.3
30.8
22.2
29.8
20.8
33.3
24.1
11.8
43.5
20.9
25.7
29.8
25.0
33.2
Third
Faga
Hydr
Buto
Tama
Arac
Plat
Lemn
Gros
Oxal
Elae
Cory
Malv
Cann
Lemn
Rham
Hydr
Saxi
Sola
Rosa
Plan
Cras
Hydr
Cary
Gera
Polg
Bora
Gros
Ulma
Saxi
Papi
Lina
Berb
TYPh
Ranu
Aral
Rham
Irid
Rosa
Malv
Sali
Apoc
Musc
Apoc
RanU
Comp
Olea
Call
Ulma
Bora
Call
Dips
Gera
TYPh
Saxi
Plan
_
~
33.0
9.1
23.5
14.3
28.6
18.2
28.6
19.8
30.8
18.7
51.6
24.4
16.9
28.6
15.8
33.3
24.4
20.7
20.3
33.6
21.3
18.2
32.5
13.1
37.3
21.7
19.3
40.1
24.5
30.8
26.1
8.5
23.6
20.6
16.9
5.4
5.7
25.0
19.7
48.3
40.0
5.0
23.5
22.0
21.9
19.9
28.6
19.8
4.8
33.3
16.7
21.9
10.2
7.4
32.8
L. K. WARD E T A L
126
APPENDIX 1 - ~ ~ n t .
Nearest Neighbours
-~
~~
Family
Second
First
_____
-~
Lemnaceae
Lichenes
Liliaceae
Linaceae
Loranthaceae
Lythraceae
Malvaceae
Menyanthaceae
Musci
Myricaceae
Nymphaeaceae
Oleaceae
Onagraceae
Orchidaceae
Orobanchaceae
Oxalidaceae
Papaveraceae
Papilionaceae
Pinaceae
Plantaginaceae
Platanaceae
Plumbaginaceae
Polemoniaceae
Polygalaceae
Polygonaceae
Polypodiaceae
Portulaceae
Potamogetonaceae
Primulaceae
Ranunculaceae
Resedaceae
Rhamnaceae
Rosaceae
Rubiaceae
Salicaceae
Saxifragaceae
Scrophulariaceae
Solanaceae
Sparganiaceae
Tamaricaceae
Taxaceae
Thymelaeaceae
Tiliaceae
Typhaceae
Ulmaceae
Umbelliferae
Urticaceae
Valerianaceae
Verbenaceae
Violaceaeae
Vitaceae
Zosteraceae
Hydr
Alga
Sola
Papa
Aqui
Onag
Sola
Call
Lich
Eric
Spa
Faga
LYth
Papa
Thym
Port
Verb
Comp
Cupr
Polg
Aqui
Thym
Verb
Pola
Comp
Buddl
Bals
Hydr
Polg
Umbe
Cruc
Corn
Sali
Onag
Betu
oxal
Labi
Chen
TYPh
oxal
Buxa
Orob
Ulma
Spar
Cory
Ranu
Cann
Camp
Papa
Camp
Gros
Pota
46.2
64.9
34.3
32.0
17.6
24.7
31.7
25.0
40.0
29.1
23.1
28.9
24.7
27.3
66.7
33.3
38.1
38.0
34.3
37.2
18.2
18.2
33.3
1.7
37.3
21.8
54.5
43.5
27.9
30.2
24.8
30.0
47.7
20.7
58.9
27.6
33.2
41.4
48.8
28.6
16.0
66.7
35.5
48.8
40.1
30.2
37.6
25.6
38.1
21.7
23.9
12.5
Alis
Musc
Irid
Verb
Elae
Bals
Bora
Buto
Alga
Sali
TYPh
Ulma
Vita
Apoc
Plum
BalS
Bora
cruc
Faga
Cary
Tama
Plan
Lma
Eric
Plan
Gent
Fuma
Halo
CarY
Labi
Papa
Berb
Faga
Polg
Fags
Cras
Cruc
cruc
NYmP
Berb
Aqui
Plum
Acer
CYPe
Faga
Comp
Labi
Papa
Fuma
Rese
Onag
Plan
33.3
40.0
33.7
30.0
16.7
20.7
24.4
25.0
15.4
14.0
20.7
27.8
23.7
20.0
12.1
30.8
34.6
30.8
21.7
33.6
15.4
16.0
25.0
1.1
37.2
20.7
44.4
33.3
23.6
25. I
24.2
19.5
44.7
19.4
48.3
24.5
28.4
36.6
23.1
27.3
15.0
18.2
34.8
23.6
38.7
28.8
24.9
24.2
33.3
21.3
23.7
1.6
Third
Call
Fung
cruc
cucu
Aral
Prim
Verb
Halo
Junc
Elae
Call
Capr
Camp
Lina
Vale
Gent
Lina
Polg
Taxa
Labi
Lora
Cist
Papa
Labi
cary
Oxal
oxal
Alis
Ranu
cruc
Viol
Buxa
Betu
cary
Rosa
Camp
Plan
Lili
CYPe
Elae
Pina
Umbe
Faga
NYmP
Tili
Sola
Chen
Verb
Pole
Papa
Cela
Papi
___
28.6
5.3
30.1
26.1
16.3
15.1
23.5
22.2
7.8
13.2
20.0
26.5
23.2
19.0
8.7
30.8
32.0
29.3
14.9
32.8
15.4
13.6
23.5
1.1
37.2
20.0
33.3
21.4
23.2
24.9
21.3
15.8
44.5
19.2
47.7
24.4
25.4
34.3
22.6
25.0
14.9
4.3
32.0
20.7
35.5
28.6
22.4
21.4
33.3
20.0
22.2
0.9
INSECT FOOD-PLANTS, LIFE FORM AND TAXONOMY
APPENDIX 2
Plant families and other groups in the analysis and their abbreviated names as
used in Figure 1.
Acer
&a
Alis
Amar
Apoc
Aqui
Arac
Aral
Bals
Berb
Betu
Bora
Budd
Buto
Bwa
Call
Camp
Cann
Capr
cary
Cela
Cera
Chen
Cist
Comp
Conv
Corn
Cory
Cras
CNC
cucu
Cupr
m e
Dips
Elae
Empe
Equi
Eric
Euph
Faga
Fuma
Fung
Gent
Gera
Gram
Gros
Halo
Hip0
Hipu
Hydr
Hype
Irid
Junc
J w
Aceraceae
Algae
Alismataceae
Amaryllidaceae
Apocynaceae
Aquifoliaceae
Araceae
Araliaceae
Balsaminaceae
Berberidaceae
Betulaceae
Boraginaceae
Buddlejaceae
Butomaceae
Bwaceae
Callitrichaceae
Campanulaceae
Cannabiaceae
Caprifoliaceae
Caryophyllaceae
Celastraceae
Ceratophyllaceae
Chenopodiaceae
Cistaceae
Compositae
Convolvulaceae
Cornaceae
Corylaceae
Crassulaceae
Cruciferae
Cucurbitaceae
Cupressaceae
Cyperaceae
Dipsacaceae
Elaeagnaceae
Empetraceae
Equisetaceae
Ericaceae
Euphorbiaceae
Fagaceae
Fumariaceae
Fungi
Gentianaceae
Geraniaceae
Gramineae
Grossulariaceae
Haloragaceae
Hippocastanaceae
Hippuridaceae
Hydrocharitaceae
Hypericaceae
Iridaceae
Juncaceae
Juncaginaceae
Labi
Lemn
Lich
Lili
Lina
Lora
Lyth
Malv
Meny
Musc
Myri
NYmP
Olea
Onag
Orch
Orob
oxal
Papa
Papi
Pina
Plan
Plat
Plum
Pole
Pola
Polg
Poly
Port
Pota
Prim
Ranu
Rese
Rham
Rosa
Rubi
Sali
Saxi
Scro
Sola
Spar
Tama
Taxa
ThYm
Tili
TYPh
Ulma
Umbe
Urti
Vale
Verb
Viol
Vita
Zost
Labiatae
Lemnaceae
Lichenes
Liliaceae
Linaceae
Loranthaceae
Lythraceae
Malvaceae
Menyanthaceae
Musci
Myricaceae
Nymphaeaceae
Oleaceae
Onagraceae
Orchidaceae
Orobanchaceae
Oxalidaceae
Papaveraceae
Papilionaceae
Pinaceae
Plantaginaceae
Platanaceae
Plumbaginaceae
Polemoniaceae
Polygalaceae
Polygonaceae
Polypodiaceae
Portulaceae
Potamogetonaceae
Primulaceae
Ranunculaceae
Resedaceae
Rhamnaceae
Rosaceae
Rubiaceae
Salicaceae
Saxifragaceae
Scrophulariaceae
Solanaceae
Sparganiaceae
Tamaricaceae
Taxaceae
Thymelaeaceae
Tiliaceae
Typhaceae
Ulmaceae
Umbelliferae
Urticaceae
Valerianaceae
Verbenaceae
Violaceae
Vitaceae
Zosteraceae
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