lowland woodland structure and pattern and the distribution of arboreal, phytophagous arthropods

Biodiversity and Conservation 4.728-744 (1995 )

Lowland woodland structure and pattern and the distribution of arboreal, phytophagous arthropods PETER DENNIS* Institute of Terrestrial Ecology, Edinburgh Research Station, Bush Estate. Penicuik, Midlothian EH26 OQB UK

GRAHAM B. USHER Institute for Ecology and Resource Management, Darwin Building, King’s Buildings, The University of Edinburgh EH9 .?JT UK

ALLAN D. WATT Institute of Terrestrial Ecology, Edinburgh Research Station, Bush Estate. Penicuik, Midlothian EH26 OQB UK

Received 12 September 1994: accepted 15 November 1994

We investigated factors that limited the distribution of phytophagous species within a woodland system in Midlothian, Scotland. A pattern analysis was conducted of phytophagous species on a total of 45 Fugus sylvatica within 15 woodlands. Species richness counted on collected leaves was tested against within- and between-wood variables. Variables used in a regression with arthropod data from Fagus were used to estimate the phytophage richness on Bet&a pendula and Quercus robur in the same woods. Covariance in the number of phytophages in sampled woods was found for Fugus over three years and for Fagus, Betula and Quercus in 1992. Association analysis was used to classify the woods into species rich or poor based on presence or absence matrices. The main factors that limit phytophages on Fagus (gaps along the woodland edge, depth and species richness of the field layer. density of leaf litter and the extent of contiguous woodland cover, when including hedgerows and lines of trees) affect phytophages of similar life history strategy on other tree species within the same woods. Eighty-six per cent of species were lost because certain life history stages were vulnerable to factors that prevail in woods of poor structure. The nature conservation value of woodlands could be assessed using the correlated vulnerability of particular phytophages across tree species under specific woodland conditions.

Keywords: arboreal phytophages; arthropods; life history: distribution; woodlands: habitat structure; pattern: fragmentation

Introduction

Guidelines based on sound scientific knowledge are required to improve management practices for wildlife conservation in existing and new, lowland woodlands, promoted by

*To whom correspondence should be addressed at: Macaulay Land Use Research Institute, Craigiebuckler. Aberdeen AB9 2QJ IJK.

0960-3115 0 19Y.5 Chapman & Hall

Arboreal arthropods and wood structure and puttern 729

incentives such as the Farm Woodland Premium Scheme (Rodwell and Patterson, 1994). The full conservation benefits of woodland planted as a result of current incentives will not be known for several decades and hence advice on management programmes, in order to improve a woodland’s conservation value, can come only from the literature reinforced by new studies of established woodlands.

Leaf feeding or phytophagous guilds of arthropods include chewers, miners, sap feeders and gall formers. The numerous species of phytophagous arthropods on trees make a major contribution to the diversity of organisms in woodland habitats (Strong et al., 19&Q), although there are a variable number of phytophage species associated with different tree species (Birks, 1980; Kennedy and Southwood, 1984). These phytophagous arthropods make an important cont~bution to the food chain. Thus, their presence can be used as an indicator of the overall conservation value of a woodland (Kirby, 1992).

Careful consideration was made of the phytophage species and habitat components of the woodland system we wished to study, to allow meanin~ul inte~retation and useful application of the results, after problems which have been encountered in previous studies (Simberloff, 1988). Different phytophagous arthropods are found on the different tree species in a given wood. Therefore, we simplified the study by restricting it to the fauna of a single non-native, tree species, beech, Fagus sylvafica L., but acknowledged that a few of the arthropod species of beech are polyphagous. The essential resource for these species comprised the three-dimensional extent of the leaf canopies of the host tree species, both in woodlands and the tree lines and hedgerows that lay between the woods. Therefore, we devised parameters that measured the context of the leaf canopy at several scales throughout a woodland system (Table 1).

This study was conducted in two parts. In the first part, we investigated the habitat factors that limited the dist~bution of phytophagous arthropods in woodlands and compared these factors with those that are known to limit the distribution of other wildlife species. Thus, features of woodlands could be identified that should be encouraged when new woodlands are established for the promotion of nature conservation. In the second part of the study, leaves of mature Fugus, oak (Quercus robur L.), and birch (Be&la pendula Roth.) were collected from the litter layer in winter to measure the phytophagous species richness in representative types of lowland woodland in Midlothian, Scotland. We used these data to explore whether the factors that accounted for the distribution of phytophagous arthropods on Fagus could be used to estimate the size of these arthropod guilds on other tree species.

The implications of these results are discussed in terms of understanding the way that woodland structure and pattern limit arboreal phytophagous species. The approach used is also offered as a possible method of assessment of the overall nature conservation value of woodlands. This is something not clearly achieved in previous studies that have fitted regression lines to species-area data on particular wildlife groups (Haila, 1986).

Materials and methods Study area

All 15 woods sampled in this investigation were in Midlothian, Scotland, lying south of Edinburgh and east of the Pentland Hills on both sides of the glen of the River Esk (Appendix 1). Altitude ranged from 115 m to 270m above sea level and the sites overlie basalt lava at the foot of the Pentland Hills, millstone grit with an intrusion of

730 Dennis et al.

Table 1. Insect, tree and woodland variables measured in the Midlothian woodland system

Description Units source Variable code

Variables recorded on each tree Numbers alive on Fugus leaves: Arboreal phytophage

species-1990 Arboreal phytophage

species-1991 Tree height Diameter at breast height Dry weight leaves Dry weight Ieaves Average leaf area damaged

Relative stage of budburst

n

n m m g 100 leaves-’ g 200 leaves-’ % (V’arcsine)

% (V&sine)

Variables to quantify tree situation Distance to ten nearest trees m Variance in distance to 10 trees m Distance to ten nearest Fagus m Variance in distance to 10 Fagus m Distance to nearest woodland

edge m Density of leaf litter in winter m -’ National Grid Reference Easting National Grid Reference Northing

Variabies to quantify woodiand structure Number of tree species tl Number of understorey species n Number of field layer species n Height of low vegetation cm Edge structure on northeast of

wood Index Edge structure on southwest of

wood Index Draughtiness Average n

Variables to quantify woodland situation Area of woodland block ha Log area of woodland block Log ha Woodland edge in adjacent land

unit km Connections by hedges or tree

lines Index Woodland area connected to

target Fugus ha Distance to the nearest woodland m Distance in to prevailing wind to:

-wood containing Fagus m -shelterbelt m

100 leaves per tree

200 leaves per tree Hypsometer Tape measure Dual range balance Dual range balance Visual estimate (100 leaves, 1991) Visual estimate

Ground survey DlOTREE Calculated from previous VlUTREE Calculated from previous DlOFAGUS Calculated from previous VlOFAGUS

Calculated from previous Five 0.25 m* quads Map Map

DTOEDGE MNLITIER EASTING NORTHING

Vegetation survey Vegetation survey Vegetation survey Ground survey

Hypsometer and tape

Hypsometer and tape Average porosity

Map and aerial photo Calculated from previous

Map and aerial photo

Map and aerial photo

Map and aerial photo Map and aerial photo

Map and aerial photo Map and aerial photo

ENDPHG90

ENDPHG91 HEIGHT DBH LEAFDWT90 LEAFDWT91

LEAFDMGE91 BUDBURST

NTREESPP UNDSTRYSPP FLDLYRSPP HTLOWVEG

NEPOROSITY

SwPoROSITY DRAUGHT

AREA LOGAREA

PERIMETER

HDGTREEROW

AREACONNECT DISTNRWOOD

DISTSWWOOD DISTSWSHBELT

Arboreal arthropods and wood structure and pattern 731

carboniferous limestone around the River Esk at Roslin Glen and Penicuik and sandstone in the rest of the area (Geological Survey, 1957). The woodlands were managed for a variety of purposes that included game, timber production and shelter and one was designated a nature reserve.

Leaf collection from Fagus canopies

Three Fagus were sampled in each wood in 1991(12 woods in 1990). Phytophagous species which mined, galled (endophage) and sucked sap on leaves, were sampled by leaf collection from the canopy in late summer. The phytophages were counted on 200 leaves in 1991 (100 leaves in 1990) collected from throughout the canopy of each tree by clipping small branches (25-30 leaves) haphazardly with long handled pruners wielded from the ground and from mid-canopy after ascending a pre-placed wire ladder. This method allowed access to all parts of the canopy of each tree. Individual leaves were carefully removed with secateurs and placed in a small polyethylene bag before storage in a cold room at cu. 4°C. We recorded evidence of the number of species on each sample of leaves and whether individuals had successfully emerged as adults or were still alive as larvae. Shed cuticle and honeydew were used to determine the species of sap-suckers. The leaf length and area of each leaf was measured with a Delta T image analyser in 1990. In 1991, length only was measured for each leaf but estimates of leaf area damaged by mines, galls, ectophage feeding damage, mycoflora and abrasion were made in both years. The dry weight of all leaves in each sample was measured with a Mettler AE163 dual-range balance.

Tree structure and situation

Standard measurements were made of tree height, diameter at breast height (dbh) and date of budburst for each Fagus. Parameters that described tree situation are listed in Table 1. The vegetation was surveyed by recording all species except Bryophytes in an area out to a radius of 50 m from each Fagus. Eight lines were laid out at 45” intervals and radii marked at 22.4,31.6,38.7,44.7 and 50 m to produce forty sectors of equal area in which the vegetation was surveyed.

Woodland structure and situation

Woodland structure was divided into categories described in Table 1. The distances to ten Fagus or any other tree (dbh > 15 cm) gave a measure of the spatial relationship of the sampled tree with other trees in the wood. The mean and variance were calculated for these parameters for the purposes of the multiple regression. Parameters used to describe woodland situation (Table 1) were measured directly from Ordnance Survey 1:lO 000 scale maps, supplemented by 1: 24 000 aerial photographs. The term, ‘area of wood’, was defined for blocks divided in relation to the insect groups studied. Roads, rivers and narrow gaps in tree canopies such as clearings around power lines were not considered barriers to movement by adults of the phytophagous species studied and were ignored in measuring the size of woods.

Leaf collection from field layer below Fagus, Quercus and Betula Leaf collection was carried out over a three week period, between mid-November and early December 1992. Of the woods listed in Appendix 1,12 were used in this study and comprised four structural types: semi-natural woodland, particularly along the margins of

Dennis et al.

river courses; policy or planted woods established between 1650 and 1840: woods integrated with shelterbelt networks; and, insular woods established in wet flushes, field corners or as derelict shelterbelt.

Three woods were chosen from each classification and at each site mature Fugus, Quercus and Beth were selected at random. In two sites, one species was missing and samples were taken from the nearest woodland of the same category. The nearest 25 leaves in the leaf litter at the base of each tree were collected at points placed a distance two thirds of the radius of the tree canopy out to the north-east, south-east, south-west and north-west, resulting in a total of 100 leaves. The leaves were frozen at - 15°C for seven days to kill any living organisms, then stored in polyethylene bags at 4°C until inspection. Each leaf was examined at 20 X magnification to identify endophage species from mines, galls and other endophage artifacts, for example cast cuticle and feeding holes (Darlington, 1975; Emmet, 1976; Emmet ef al., 1985; Bevan, 1987). Each species was recorded as present or absent on each leaf and the frequency of occurrence was recorded out of each sample of 100 leaves.

Data analysis

Species counts derived from leaf collection from the canopies of Fugus in 1990 and 1991 were tested separately against the variables listed in Table 1. Stepwise variable selection was used to reduce the number of variables that accounted for the variation in the species richness of phytophages. This was carried out in three phases. Variables that represented the general woodland categories and woodland situation and structure were entered first, then tree factors and finally, covariates that interacted within the woodland. A multiple regression was then calculated on the basis of the final variable list for 1990 and 1991 data separately.

The regression models were used to estimate values for the species richness of similar phytophages on Fugus, Beth and Quercus in those woods in which leaves were collected in winter. The regression equations were modified with a scaler which corrected for the differences in species number observed between these tree species. Species richness predicted for each wood from the 1990 and 1991 models were compared with the observed values using a paired t-test. Covariation, both between the species richness of Fagus for three consecutive years and for the three tree species over one year, were tested with the Spearman rank correlation.

The frequency data of phytophagous species were calculated for each woodland element and reduced to a binary table that represented species presence or absence. The variance ratio test for species association was carried out for the five discrete data sets. An association analysis was carried out on those datasets for which a significant species association was detected. The groups of woods derived from the various association analyses were compared for consistency and the species components of three main endophage families compared between tree species. Finally, information on the distribution and life history of endophagous species specific to these trees in Scotland were extracted from the literature and potential numbers of species calculated for good and poor woodlands for comparison with the groups derived from the association analysis.

Arboreal a~~r~p~ds and wood str~c~re and pattern

a.

Insular 1

Connected

insular Policy

q Fagus r-l m B&Jlla

f3 ouercus

Figure 1. Species richness of phytophagous insects in subjective woodland categories on a. Fagus, leaves collected from leaf canopies in 1990 and 1991 (ANOVA between categories, F2,,* = 27.98;p < 0.001) and b. Fagus, Bet&a and Qtserczti, leaves collected from the leaf litter in winter 1992 (ANOVA between categories, tree species combined, F3,g = 76.22; p < 0.001).

Results

A total of 30 species of phytophagous arthropod were recorded on leaves from Fagus, Quercus and Bet&a (Appendix 2). The species richness of the phytophages was consistentiy greater on trees sampled from policy and semi-natural woodlands than other categories (Fig. 1).

Of the woodland and tree scale variables entered into the stepwise variable selection (values shown in Table 2), five in total provided the best fit to the phytophage data from Fugus for the two years, The draughtiness of the woodland and the covariate, density of leaf litter by height of the low vegetation under each tree, accounted for 54% of the variation in the distribution of the phytophagous species in 1990 (Table 3a). The extent of hedgerows and lines of trees out from the woodland block, height of the low vegetation and the covariate, plant species richness in the field layer by density of leaf litter accounted for 64% of the distribution of endophage species in 1991 (Table 3b). Values of arthropod species richness calculated from the two regression models for the three tree species showed varying predictive power. The model from the 1991 Fagus data gave the best estimate of species richness on other tree species amongst the woodland elements sampled

134 Dennis et al.

Table 2. Sample sizes, means, ranges and standard deviation of insect, tree and woodland variables

Variables n Minimum Maximum Mean SD

Variables recorded on each tree ENDPHG90 ENDPHG91 HEIGHT DBH LEAFDWTOO LEAFDWT91 LEAFDAMGE91 BUDBURST

Variables to quantify tree situation DlOTREE VlOTREE DlOFAGUS VlOFAGUS DTOEDGE MNLI’ITER EASTING NORTHING

36 1.0 9.0 5.167 2.158 45 2.0 14.0 7.378 2.910 45 11 32 19.613 5.970 45 0.4 1.2 0.824 0.186 36 3.45 10.75 5.717 1.482 45 6.75 17.60 10.923 2.299 4s 3.85 18.08 11.919 2.641 45 0 Xl.9 50.613 26.843

45 4.57 lY.82 11.820 3.959 45 0.55 49.86 13.801 11.014 45 5.14 87.67 21.814 16.608 45 0.81 461.03 54.500 78.520 45 6 150 31.959 37.338 45 0.2 388.8 112.129 106.319 45 1691 2544 2148.156 247.038 45 5625 6487 6049.53 265.154

Variables to quantify woodland structure NTREESPP 45 UNDSTRYSPP 45 FLDLYRSPP 45 TOTVEGSPP 45 HTLOWVEG 45 DRAUGHT 15

Variables to quantify woodland situation LOGAREA 15 PERIMETER 15 HDGTREEROW 15 AREACONNECT 15 DISTNRWOOD 15 DISTSWWOOD 15 DISTSWSHBELT 15

1 12 6.867 2.642 0 6 2.156 1.718

11 42 25.378 7.423 15 55 37.911 10.317 0 29.4 9.113 6.949 1.8 7.0 3.52 1.730

0.176 1.778 1.046 0.528 2.38 7.60 4.429 1.403 0 8 3.600 2.553 0.5 77 39.833 30.075

50 1225 218.333 325.149 100 4375 2061.667 1220.977 100 1900 563.333 518.208

(Table 4). There was also significant covariation between species richness on Fugus in woodland elements for three consecutive years (regardless of sampling method; Table 5a) and species richness between the tree species (including Fugus sampled during Autumn 1991; Table Sb).

There was significant and positive species association for all five of the datasets (Table 6) and association analysis of the woodland elements grouped 95% of the woods in the same categories (Figs 2 and 3). A loss of 86% of species in several phytophage families was


Table 3. Results of the stepwise variable selection and multiple regression of phytophage species of Fagus in a. 1990 and b. 1991 against variables that characterized woodland structure and situation in Midlothian.

Variable Coefficient F-ratio df p R2

a. INTERCEPT 7.384 DRAUGHT -0.695 MNLITIER* HTLOWVEG o.ooo1 21.64 2,33 < 0.001 0.54

b. INTERCEPT. 3.650 HDGTREEROW 0.611 HTLOWVEG 0.095 FLDLYRSPP* MNLITIER O.oool 27.52 3,41 < 0.001 0.64

*Variables with significant interaction that were combined for the analyses.

calculated on the assumption that these species have life history strategies which are vulnerable to extrinsic factors that prevail in woods of poor structure. A total of eight endophagous species were recorded in the woods that represented poor sites compared with 15 in the woods grouped as good sites by the association analysis, a difference of 53% (Table 7). However, records in the literature suggested that the potential number of specieswas 37for the same geographical region (Darlington, 1975; Emmet, 1976; Emmet et aZ., 1985).

Discussion

The distribution of phytophages on Fagus was related to the draughtiness, species richness and height of the field layer, density of leaf litter, and connectivity by hedgerows and lines of trees (Table 3). The pattern of distribution of the phytophagous species on Fagus was consistent over a three year period. There was also a significant tendency for insect species richness on different tree species to vary proportionally according to the woodland quality (Table 5). This could suggest that the principal mechanisms that accounted for the restriction of insect species on Fagus (Table 3) are likely to apply to the native tree species Quercus and Betufa which occur in the same woodlands. Certainly many species of micromoth and gall midge on different tree hosts share similar life history strategies and therefore would be vulnerable to the same physical processes (Table 7a). The potential range of micromoth and gall midge species on native tree species in wooded landscapes in Scotland could be much diminished if many of the woods are small (cu. 1 ha), draughty and exposed. The theoretical percentage of species excluded from exposed and draughty woods may be 86% of micromoths and gall forming flies on Fagus, Bet&a and Quercus in Scottish woods (Table 7a).

The calculated difference in species richness between the woodland classes derived from association analysis was 53% and the maximum species richness observed was also lower than the theoretical figure (Table 7b). Evidence of endophagous species was harder to interpret on ground collected leaves in winter than those collected from canopies in summer. Rapid browning and small leaf size of Bet&a in the litter layer limited the number of species that could be identified to six. Collection of leaves from the canopy of this species would improve the accuracy of the estimates. Leaves damaged by phytophagous insects

736 Dennis et al.

Table 4. Estimated species richness of phytophages on Quercus robur, Betula pendula and Fagus sylvatica from the 1990 and 1991 regression models derived from autumn counts of phytophages on Fagus syivatica and between- and within-woodland variables. The predicted species richness was compared with observed counts derived from a winter leaf collection from the litter under three tree species in each wood. Significance tested with a paired r-test.

Species Observed Estimated-l 990 model Estimated-1991 model

a. Quercus robur Number of woods Mean species richness

(for three trees) SD

t

Degrees of freedom Significance

b. Betula spp. Number of woods Mean species richness


t


c. Fagus sylvatica Number of woods Mean species richness


t


10

7.73 1.404

10

4.07 0.334

10

5.30 0.675

10

5.07 7.06 0.373 1.301

-~ 4.707 - 1.136 9 9

p < 0.01 NS

10

2.34 3.26 0.080 0.277

- 6.650 - 3.671 9 9

p < 0.001 p < 0.01

10

3.90 5.43 0.221 0.768

- 3.619 0.322 9 9

p < 0.01 NS

10

10

10

SD: standard deviation; NS: not significant.

are thought to abscise earlier than undamaged leaves (Hespenheide, 1991) and the winter collection of surface leaves from the litter layer may have underestimated both the number of endophage species and their frequency of occurrence on leaves. If the leaf litter is deep and the first 25 leaves were collected, those with phytophagous insect damage may, due to being abscissed earlier, be at the bottom (damp forest floor) or blown away (if dry). The arthropod species recorded on native species in a wood may be represented by smaller populations than expected because of the historical decline and fragmentation of woodland cover, typical of lowland Britain. It was, therefore, of interest to compare the distribution of arthropod species on native QuercuS and Bet& with the species on introduced Fugus. Our results suggest the distribution pattern of the arthropod species on these two tree species types reflects the current quality and pattern of woodland cover as opposed to an artifact of previous deforestation (Warren and Key, 1991). This phenomenon could otherwise confound the interpretation of an observed pattern of


Table 5. Covariation in phytophage species between farm woodlands for a. Fagus between years (n = 8) and b. Fagus, Betula and Quercus species, including Fagus leaf data derived from canopy and litter (n = 10). The matrices show the Spearman rank correlation coefficient below the diagonal significance above. Null hypothesis states that the ranked values of species richness from each data source are uncorrelated between woods

a. Fagus 1990 Fagus 1991 Fagus 1992

Fagus 1990 1.00 p < 0.01 p < 0.05 Fagus 1991 0.99 1.00 p < 0.05 Fagus 1992 0.81 0.80 1.00

b. Fagus 1991 Fagus 1992 Quercus 1992 Bet&a 1992

Fagus 1991 1.00 p < 0.01 p < 0.01 p < 0.01 Fagus 1992 0.82 1.00 p < 0.01 p < 0.01 Quercus 1992 0.85 0.93 1.00 p < 0.01 Bet&a 1992 0.85 0.98 0.94 1.00

arthropods on native species in a given woodland system. Therefore, it was useful to collect data on arthropods of Fagus because it was introduced into Midlothian ca. 300 years ago and exists today in policy or planted woods, networks of shelterbelts, small, insular woods, tree lines and hedgerows (Brown, 1953).

Some endophagous members (gall formers and miners) of the phytophagous species over-winter in leaf litter (Darlington, 1975; Emmet, 1976; Emmet et al., 1985) and factors that facilitate a loss of leaf litter by wind could decrease the endophage populations within the wood. Connor (1984) found that when trees were isolated, and only colonized from the leaf litter, local population extinction readily occurred. Certainly, adults of the micromoths are poor fliers and usually fly at about 1 m above the ground although they occasionally fly more freely and may maintain populations on Fagus in poorer quality woods (Woiwod and Stewart, 1990). This lack of power to their flight may restrict them to sheltered patches of woodland and limit dispersal between woods and reduce species’ viability (Dempster, 1991). We should also consider the corollary of the leaf litter argument. Leaf loss from one woodland may contribute to the leaf litter of other woods although most will go somewhere unsuitable. We have to assume that endophagous larvae can survive this passive dispersal and that adult endophages may contribute to the population of a remote woodland site, if there is vegetation to trap leaves, although they may not survive in an open habitat. Pasek (1988) showed that insects accumulate in areas of wind speed reduction such as around woodland and hedgerows. It might be assumed therefore, that some proportion of leaves with later adult endophage emergence or emergent adult endophages by flight may reach other woodlands and, in particular, hedgerows. Other phytophagous species may be excluded from small, exposed and draughty woodlands because these woods fail to provide suitable conditions for the species to feed, locate a mate or oviposit. At present, we have no direct evidence for these mechanisms but they allow us to generate the testable hypothesis that phytophagous species are excluded from woodland habitats by the combination of a vulnerable life history strategy (period of endophagy, etc.), a deficiency in the structure and context of the wood (draughty edge and

738 Dennis et al.

a. Fagus 1990 Twelve woods I

Sfigme//a tityrella (p sum = 22.7) - .

I (P max = 2.92) Pentlandfield Pentland Grove Castlelaw Brunstane Silverburn Bush Estate Penicuik

Crosshouse III (P max = 4.00) Braidwood Eastside Farm Jww W Joppa (El)

b. Fagus 1991

I (9 max = 1.67) Pentlandfield Pentland Grove Castlelaw B~nstane Silverburn Bush Estate Penicuik Hurley Cove Amazondean Cornton Burn

II (Y max = 2.00) Crosshouse Joppa (El)

Ill (2 max = 3.00) Braidwood Eastside Farm Joppa (W

Eogure 2. Association analysis of woodland sites defined by a. Fagus 1990 and b. Fugus 1991 datasets. Croups are defined by the presence (+) or absence (-) of phytophage species that account for the strongest association (x” sum). No further division of woodlands made when p max becomes < 6.0. See Table 6 for variance ratio tests for significant species association.

exposed location) and an extrinsic environmental impact (wind). We also suggest that the same phenomenon may exist for many other arthropod species adapted to different host tree species. This means that the pattern expressed for phytophagous arthropod species of known life history amongst trees of one species throughout a woodland system, may be used to predict the extent of the same guild on other tree species in the same woodlands (Table 4).

The value of the equilibrium theory of island biogeography (MacArthur and Wilson.


a. Fagus 1992 Twelve woods I

+ Stigme//a tityreila (2 sum = 12.24) -

I (P max = 0.14) Penicuik Hurley Cove Cornton Bum Roslin (north) Roslin (south)

Crosshouse Braidwood Jww (W Pentland Grove Castlelaw Silverburn Bush Estate

b. Be&/a 1992 Twelve woods I

+ Ca/opMia popuieforum (p sum = 12.0) -

1 I (9 max = 0.0) II (x4 max = 0.0) Bush Estate Crosshouse Penicuik Braidwood Hurley Cove Jwa (W Comton Bum Roslin (north) Roslin (south)

Pentland Grove Castlelaw Silverbum

c. Quefcus 1992 ,Twelve woods

+ Stigmella fufic&IiB (9 sum = 23.2) -

+ Stigmella roborella (2 sum = 12.0) -

I (9 max = 3.0) Bush Estate Penicuik Hurley Cove

II (2 max = 0.0) Pentland Grove

Ill (9 max = 1.9) Crosshouse Braidwood Jwpa (W

Cornton Burn Roslin (north) Roslin (south)

Castlelaw Silverburn

Figure 3. Association analysis of woodland sites defined by a. Fagus, b. Bet&a and c. Quercus datasets, 1992. Symbols described in Fig. 2 legend.

1967) is immense but the application of the species-area relationship has been of limited value in understanding how species interact with systems of terrestrial habitats (Haila, 1986). Many studies abused the species-area regression and few achieved more than to fit a regression model devoid of ecological meaning (Connor and McCoy, 1979). It is not

740 Dennis et al.

Appendix 1. Details of the farm woodlands included in the study of phytophage species richness. Woods sampled indicated for ‘Fagus 1990. 2Fagus 1991 and “Fagus, Betula and Quercus 1992 datasets

Name Code Grid reference Subjective category

Crosshouse”’ AI NT 237 635 Insular-derelict shelterbelt Braidwood’2” BI NT 197 588 Insular-regenerated around wet flush Eastside Farm” CI NT198598 Insular-planted stand Joppa’” DI NT 194 578 Insular-derelict shelterbelt Joppa”” EI NT 189 58s Insular-derelict shelterbelt and regenerated stand PentlandfieIdl’ AC NT 251646 Connected-integrated with shelterbelt network Pentland Grove”’ BC NT 252 648 Connected-integrated with shelterbelt network Castlelaw” CC NT 234 638 Connected-integrated with shelterbelt network Brunstane” DC NT 201 586 Connected-integrated by tree lines to policy wood Silverburn”’ EC NT 208 599 Connected-integrated by tree lines to poiicy wood Bush Estate”’ SA NT 254 632 Policy woodland with regeneration by native species Penicuik’” SB NT 219 587 Policy woodland with regeneration by native species Hurley Cove” SC NT 216 585 Policy woodland with regeneration by native species Amazondean’ SD NT 169 563 Policy woodland-mixed non-native species stand Cornton Burn’” SE NT 207 588 Policy woodland-predominantly ~agus/Q~Frc~~ Roslin (north)’ RN NT 274 629 Semi-natural woodland-nature reserve Roslin (south)’ RS NT 274 625 Semi-natural woodland-nature reserve

surmising therefore, that previous studies of different wildlife groups, in which woodlands were treated as islands, proved either contradictory or inconclusive (Simberloff, 1988). One problem is deahng with the scale of interaction of the organism with the habitat (Haila, 1990). The ‘island’ could be the individual host plant to a stenophagous insect, a mosaic that comprised several plants to a polyphagous insect; or a monocultured plantation to a mobile stenophagous species (Claridge and Evans, 1990). In some studies it may be appropriate to treat a wood as the island unit (e.g. grey squirrels, Fitzgibbon, 1993) but for organisms such as phytophagous insects there may be little relevance because the ‘island’ could be represented by an individual host plant (Dempster, 1991). Woodlands are complex habitats that include composites of surrounding simple biotopes. The fauna sampled in a woodland may, therefore, be ubiquitous. Many field layer plant and arthropod species are common to habitats within and between woodlands (Usher et al.. 1992, 1993). For large, mobile fauna, the size of woodland habitat would not matter if enough was available, dispersed within reach of the fauna, and no barriers to movement existed. Birds are capable of selecting particular resources from a large number of insular woodlands because few species are confined within the margins of a wood for their whole lifetime (van Dorp and Opdam. 1987). The number of species will be constrained by the resources available within a woodland system (Hill et al., 1991). However, we recognize that there are true woodland species in larger, less disturbed woodland systems (Askins et al., 1987). IJndisturbed, ancient or semi-natural woodland must still be retained both for the species and age diversity of trees and dead wood which provide for the saproxylic species least likely to occur in new woods and as a source of colonists for the new woodlands (Warren and Key, 1991).

Island biogeography is not appropriate to identify how plant and animal populations interact with lowland woodlands because many woodlands are not clearly definable as


Appendix 2. Phytophage species identified from leaves collected from the host trees Fagus sylvatica (F), Be&la pendula (B) and Quercus robur (Q) in 17 woodland sites

Scientific name Authority Host tree Order and Family

Ectoedemia albifasciella Heinemann E. occultella Linnaeus Stigmella hemargyrella Kollar S. lapponica Wocke S. roborella Johansson S. rufkapitella Haworth S. tityrella Stainton Caloptilia alchimiella Scopoli C. betulicola Hering C. populetorum Zeller Phyllonorycter maestingella Muller P. messaniella Zeller P. quercifoliella Zeller P. corylifoliella f. betulae Hubner Parornix fagivora Frey Hartigiola annulipes Hartig Rhynchaenus fagi Linnaeus

Fagocyba cruenta Phyllaphis fagi Neuroterus albipes N. numismalis N. tricolor Cynips divisa C. quercus-folli Andricus curvator A. ostreus Eriophyes lionotus E. macrorhynchus ferrugineus E. nervisquus E. stenopis typicus

Her&h-Schaefer Linnaeus Schenck Geofroy in Forcroy Hartig Hartig Linnaeus Hartig Hartig Nalepa Nalepa Nalepa Pagenstecher

Q B F B Q Q F Q B B F Q&F Q B F F F

F F Q Q Q Q Q Q Q B F F F

Lepidoptera, Nepticulidae Lepidoptera, Nepticulidae Lepidoptera, Nepticulidae Lepidoptera, Nepticulidae Lepidoptera, Nepticulidae Lepidoptera, Nepticulidae Lepidoptera, Nepticulidae Lepidoptera, Gracillariidae Lepidoptera, Gracillariidae Lepidoptera, Gracillariidae Lepidoptera, Gracillariidae Lepidoptera, Gracillariidae Lepidoptera, Gracillariidae Lepidoptera, Gracillariidae Lepidoptera, Gracillariidae Diptera, Cecidomyiidae Coleoptera, Curculionoidea Hemiptera, Cicadellidae Hemiptera, Callaphididae Hymenoptera, Cynipidae Hymenoptera, Cynipidae Hymenoptera, Cynipidae Hymenoptera, Cynipidae Hymenoptera, Cynipidae Hymenoptera, Cynipidae Hymenoptera, Cynipidae Acarina, Eriophyidae Acarina, Eriophyidae Acarina, Eriophyidae Acarina, Eriophyidae

distinct, insular units of habitat. We cannot simplify the woodland cover of typical landscapes into islands because of the context. For example, the division of woodlands by rivers, roads and railways may represent a complete or partial barrier to organisms active in the field layer and justify a definition of the habitat into two ‘islands’. If we consider organisms active in the canopy layer, a single ‘island’ definition would be appropriate, particularly if the canopy interlocked above barriers to epigeal organisms. The connection of the wood to other habitats that emulate woodland (such as hedgerows) raises a challenge to current definitions of ‘island’. Species of Acarina seemed to form a distinct shift between woodland soil and arable soil along a transect (Sgardelis and Usher, 1994) but to conclude that they were isolated would be misguided because interconnected hedgerows have similar soil conditions to the woodland and therefore support many of the mite species over a much larger contiguous area than measured for the wood alone, There

Dennis et al.

Table 6. Variance ratio test of woodland species presence/absence data. Null hypothesis states that there is no association between species. V 3> 1 indicates possible association, V < 1 negative association. If species not associated there is a 90% chance that W will lie in the range: X’,,,,,N < = W ‘c = X2,mw null hypothesis accepted. Association analysis carried where null hypothesis rejected

Leaf data V w P 0 “S,N X2,, W.N Null hypothesis Species association

Fagus 1990 Fagus 1991 Fagus 1992 Betula 1992 Quercus 1992

3.23 3.03 3.25 2.16 3.43

38.8 45.5 39.0 25.9 41.1

21.0 25.0 21.0 21.0 21.0

5.2 7.3 5.2 5.2 5.2

Rejected Rejected Rejected Rejected Rejected

Positive Positive Positive Positive Positive

Table 7. a. Species of leaf mining Microlepidoptera and gall forming Diptera expected on tree species sampled in the Midlothian study area that could be excluded from poor quality woodlands (derived from Emmet 1976, Emmet et al. 1985 and Darlington 1975). smephg: in summer, feed as larvae in leaf mines or galls: o/w: overwinter in mines or cocoons in litter. b. Actual species observed in woods from two main groupings derived from association analyses (GI and GII)

Leaf mining Lepidoptera Gall midges Total endophages Nepticulidae Gracillariidae Canopy Litter Canopy

Cecidomyiidac Litter Canopy - Litter Canopy Litter --------

smlephg o/w smlephg o/w sm/ephg o/w sm/ephg olw

Birch (Bet& spp.) 6 4 8 h 0 0 14 IO Oak (Quercus spp.) 5 5 IO 9 2 7 17 Ill Beech (Fagus s~/vaticu) 2 2 2 1 2 2 6 h Total 13 11 20 17 4 4 37 32

b Tree species Leaf mining Lepidoptera Gall midges Total endophages

Nepticulidae Gracillariidae Cecidomyiidae (Cynipids) GI GII GI GII GI GII GI GII GI GII

Birch (Bet&a spp.) I 0 3 7 0 0 4 2 0 II Oak (Quercus spp.) 3 1 3 3 0 0 6 4 1 5 Beech (Fqus .s~~lvatica) 1 1 2 I I 0 5 2 0 0 Total h 2 8 h I 0 15 8

were fewer problems with the method we present than with previous applications of island biogeography because we use species richness and propose in addition a functional relationship of each species with the habitat. The emphasis on a complement of species on one host plant (Fugus) made the interpretation of the results clearer. The covariation of the distribution pattern of phytophage species on two further tree species (Quercus and Bet&z) added credence to the methodology. The assessment of the phytophagous arthropods on one tree species could provide a useful and economic estimate of the richness of species on other tree species of the same wood. It should also be possible to estimate which species would be absent from other tree species by an assessment of vulnerable periods in the species’ life histories.


More diverse plant structure and species in the woodland field layer may provide draught free conditions that entrap leaves and ensure viable populations of phytophagous arthropods and winter shelter for other arboreal groups. The wider habitat diversity would also promote further arthropod diversity in the woodland vegetation and offer resources for a more general woodland fauna. Practical manuals on farm woodland planting promote the incorporation of mixed scrub and tall field layer vegetation to produce draught free, well structured, new woodlands and we agree with Insley’s (1988) view that new lowland woodlands could provide valuable wildlife habitat. Some other studies of woodland flora and fauna emphasize the value of large woodlands (Usher et al., 1992,1993). We suggest that small woods (ca. l-5 ha), likely to be established under new incentive schemes, could support more of the potential insect populations than would be predicted by a species/area relationship, if the woods are spaced to maximize mutual shelter and are located into established hedgerow or shelterbelt networks or they are planted in areas such as hollows, that trap leaves.

Acknowledgements

P.D. was funded by the Forestry Research Coordination Committee, Special Topic in Farm Forestry, 1990-1993. We are indebted to Murray Black, Harriet Palmer (Scottish Agricultural College), Sir John Clarke, Robert McDougal (Penicuik Estate) and Mrs Cesford (Amazondean) for allowing access to the woodlands. Roslin Glen woodland nature reserve (Scottish Wildlife Trust) was open to public access. We express thanks to Dr M.R. Young for his comments which helped us to improve the manuscript considerably.

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