Vegetational and faunal changes in an area of heavily grazed woodland following relief of grazing

Biological Conservation 47 (1989) 13-32

Vegetational and Faunal Changes in an Area of Heavily Grazed Woodland Following Relief of Grazing

R. J. Putman, P. J. Edwards, J. C. E. Mann, R. C. How & S. D. Hill Department of Biology, Building 44, The University, Southampton SO9 5NH, UK (Received 13 November 1987; revised version received 21 April 1988; accepted 25 April 1988)

A BS TRA C T Two 5"6 ha inclosures were established in 1963 within an area of heavily grazed deciduous woodland in the New Forest, Hampshire. In one, a constant grazing pressure was maintained (at c. 1 fallow deer ha- 1); the other was kept free of all large herbivores. The vegetation of both was surveyed 6 years, 14 years and 22 years after inclosure. Changes over time in species composition and age structure of trees in the two areas are discussed, as are changes in composition, diversity and biomass of the ground flora and shrub layer. Clear differences were apparent between the two and also, within the ungrazed site, over time. While in the grazed plot no regeneration was apparent, rapid regeneration of birch, beech, oak, Scots pine, Douglas fir and holly had occurred in the ungrazed plot by 1969; by 1985, with closure of the canopy, establishment had virtually ceased. Clear differences were also recorded in species composition of both trees and ground flora, with species resistant to grazing more abundant in the grazed plot and with many graze-sensitive or palatable species absent in that plot becoming re-established in the ungrazed area. Analysis of the three-dimensional profile of the vegetation also showed clear differences in vertical distribution in the two plots. Surveys were undertaken in 1983-84 and in 1985 of the small mammal communities and ground invertebrates in the two areas. Marked differences in species composition again reflect structure and species composition of the vegetation under the grazed and ungrazed regimes. 13 Biol. Conserv. 0006-3207/89/$03"50 © 1989 Elsevier Science Publishers Ltd, England. Printed in Great Britain

14

R. J. Putman, P. J. Edwards, J. C. E. Mann, R. C. How, S. D. Hill The factors affecting the succession which followed relief of grazing are discussed. Even after 22 years, the vegetation o f the ungrazed area remains strikingly species-poor, and reasons for this--and implications for conservation--are considered.

INTRODUCTION Large herbivores and smaller herbivorous rodents may form a major part of the animal communities associated with woodland, and their grazing may have a significant effect on the vegetation dynamics. Thus it may be established that continuous grazing results in a change in species composition of both trees and herbaceous ground vegetation--with suppression or elimination of sensitive species and competitive release of graze-tolerant or graze-resistant species: (e.g. Harper, 1977; Bakker et al., 1983, 1984; Crawley, 1983; Pigott, 1985; Putman, 1986; de Bie et al., 1987; Edwards & Gillman, 1987). Grazing also influences the physical structure of the vegetation, causing selection for prostrate rather than erect growth form amongst the ground flora and often removing or reducing the shrub layer up to a distinct browse line of 1.5-2 m. Grazing or browsing damage may either stimulate or suppress productivity (Grant & Hunter, 1966; Krefting et aL, 1966; Coupland, 1979; McNaughton, 1979; Bobek et al., 1979), while differential patterns of feeding and elimination may cause gross changes to nutrient cycling (e.g. Spedding, 1971; Crawley, 1983). The degree to which such effects are observed depends on the density and species of grazers (Harper, 1977; Putman, 1986; de Bie et al., 1987), but grazing may result in major changes in the structure and dynamics of the vegetational community. Improved understanding of these various potential effects of grazing or browsing upon vegetation has led increasingly to attempts to exploit this process in conservation management. Densities of naturally-occurring large herbivores may be manipulated, or in other cases, populations of other species deliberately introduced (e.g. Thalen, 1984) in order to achieve some specific management objective. What is not yet fully understood, however, is to what extent vegetational changes produced by heavy grazing are reversible. This paper reports an investigation of the vegetational changes associated with the relief of grazing and browsing when large herbivores were excluded from an area of woodland previously subjected to heavy grazing over a long period. The New Forest in Southern England is an area of some 37 500 ha of mixed vegetation set aside as a royal hunting preserve in the 1lth century and for much of that time subjected to heavy grazing pressure from large

Changes after grazing in woodland

15

herbivores. Although the relative balance of numbers between deer (currently, fallow Dama dama, roe Capreolus capreolus, red Cervus elaphus, and sika Cervus nippon) and domestic stock (cattle and ponies pastured on the Forest under ancient rights of Common) has changed over the years, the Forest has probably sustained heavy pressure from these herbivore populations for most of 900 years. The effects of grazing pressure upon the Forest woodlands have been described in Peterken & Tubbs (1965), Tubbs (1986) and Putman (1986), but may be summarised as follows. (1)

Reduction in diversity and species composition of ground flora, with loss of graze-sensitive or particularly palatable species such as Mercurialis perennis and Galeobdolon lutea. The herb layer is typically very sparse, and unpalatable species such as Oxalis acetosella and Euphorbia amygdaloides predominate. (Nomenclatures for vascular plants follows Moore (1982).) (2) Virtual eradication of many species of the shrub layer, such as hazel Corylus avellana, blackthorn Prunus spinosa, hawthorn Crataegus monogyna, maple Acer campestris, and willows Salix caprea and S. cinerea, as well as brambles Rubus fruticosus agg. and briars Rosa arvensis and R. canina. At the same time holly Ilex aquifolium is both more abundant and more widespread than might be expected in woodlands of this type. (3) The elimination of many of the shrubby species and heavy grazing of the woodland floor have resulted in a physical change in structure with a virtually complete loss of the structural layer between 5 cm and 200cm. A clear browse line is established in most Forest woodlands at 200cm. (4) Finally, continued heavy grazing has resulted in almost complete lack of regeneration of trees within the Forest woodlands, which has only occurred during periods when animal numbers have fallen to low levels. Thus in the main they have a curiously impoverished age structure, with trees establishing successfully only during the periods 1650-1750, 1860-1910 and 1930-1945 (Peterken & Tubbs, 1965). The area thus provides an ideal study site to examine the effects of relief of grazing in an area markedly affected by a long history of heavy animal usage. MATERIALS A N D METHODS

Study site In 1963, ll.2 ha of mixed woodland were fenced off within Denny Lodge Inclosure (ref. SU 335055) to create two separate but adjoining plots of

16

R. J. Putman, P. J. Edwards, J. C. E. Mann, R. C. How, S. D. Hill

approximately equal area, known locally as the Denny Pens (Fig. 1). Until that time these areas of woodland had been grazed by large herbivores, chiefly deer and horses. In one plot grazing pressure was maintained by retaining within the area a population of fallow deer at a density of 1 per ha. The other plot had all larger herbivores removed and has since remained ungrazed.

330 053

Scale1:2850

~,

331 053

Grid reference SU 20/30

050

330

Ungrazedplot

Grazed plot

050 331

Fig. 1. Location of the Denny Pens experiment in the New Forest in Hampshire. Insert shows 50m × 50m sample grid imposed; small circles show, as an example, the location of 1 m 2 samples in 1977.

At the time of enclosure the area consisted of mature woodland dominated by oak Quercus robur and beech Fagus sylvatica. A few isolated specimens of mature Scots pine Pinus sylvestris were also present, and the occasional Douglas fir Pseudotsuga rnenziesii and larch Larix decidua. The ground flora was sparse, with a large proportion of the area bare or covered with litter; bracken Pteridium aquilinum occurred patchily throughout the area, forming dense stands when present.

Changes after grazing in woodland

17

Surveys The plots were surveyed six years after inclosure in 1969 to establish a baseline (Rowe, unpublished) and then surveyed in July 1977 (14 years; Mann, 1978) and July/August 1985 (22 years; How, 1986). In each case vegetational differences were recorded between the 'grazed' and 'ungrazed' plots, and changes over time within each plot assessed. Since changes in species composition, productivity and physical structure of the vegetation associated with relief from grazing might be expected to have 'knock-on' effects on other elements of the ecological community supported by that vegetation, surveys of small mammal populations and ground invertebrates were undertaken in both grazed and ungrazed plots in 1983 and 1984 (20 and 21 years after inclosure respectively; Hill, 1985; How, 1986). At each sample date, a 50m grid was established within each plot by recognised survey techniques (Fig. 1). All vegetation measurements were replicated within each grid square, providing 20 replicates in each plot. Where measurements taken did not extend to the full 2500 m 2 square but represented a sample only, the positions of the samples were located randomly within the grid square. Sample locations were not constant from survey to survey. The following parameters were recorded in at least one survey (with times after inclosure in parenthesis): Trees Species composition and numbers Basal diameter

(6, 14, 22 years) (14, 22 years)

Shrubs and herb layer Species composition Biomass Species diversity Structural diversity

(6, 14, 22 years) (6, 14, 22 years) (14, 22 years) (14, 22 years)

Animals Species and numbers of small mammals Species of ground invertebrates

(20, 21 years) (22 years)

Trees

No survey was undertaken in 1963, when the plots were first established, but the areas were subsequently mapped in 1969. At the time of inclosure in 1963 grazing had effectively prevented all regeneration and only mature trees were present in either plot. In the 1977 and 1985 surveys, however, regeneration in the ungrazed plot was so extensive as to render a total record impossible. Accordingly tree numbers and species composition were recorded in circular

18

R.J. Putman, P. J. Edwards, J. C. E. Mann, R. C. How, S. D. Hill

quadrats of l0 m radius established in each 50 m x 50 m grid square. Thus in each plot a total area of 20 x 314 m 2 ( o r 6280 m 2) w a s sampled, 11% of the entire plot area. In the 1977 and 1985 surveys basal diameters of all trees encountered in each 10 m radius circle were also recorded.

Shrub and herb layer Quadrats (1 m 2) were randomly located in each 50 x 50 m grid square in each survey, giving on each occasion a total of 20 quadrats within each plot. All species rooted within each quadrat were scored on a presence/absence basis and percentage cover of each estimated (the latter in 1977 and 1985 only). Data could then be pooled to provide estimates of frequency of occurrence (no. ofquadrats in which a species was recorded out of a total possible 20." all surveys) and mean percentage cover (1977, 1985 only). Shannon and Weaver's measure of diversity, H, (Shannon & Weaver, 1949) was calculated in 1977 and 1985 to offer an index of species diversity in the two plots. Above-ground biomass of herbaceous vegetation was estimated for each quadrat in 1977 and 1985 by clipping all plant material at ground level and fresh-weighing the harvested sample. In addition an assessment of the physical structure of the vegetation in terms of vertical distribution was made, creating in effect a vertical profile of the vegetation between ground level and 1.8 m. Different methods were used in the two surveys. In 1977, the three-dimensional distribution of vegetation in each quadrat sample was assessed using a 3-d pinframe. In two dimensions, a 1 m × 1 m frame, perforated at 10cm intervals in a regular grid, was superimposed upon the quadrat (giving a truly objective estimate of percentage cover, since the plant species touching 100 separate sample points within the quadrat were recorded). To assess the vertical pattern of vegetational distribution this technique was extended to three dimensions. The same pinframe was supported 1.8 m above the quadrat. Pins inserted into the frame were marked off at 10cm heights; accordingly the total number of times (of 100 pins) that a pin on the frame was touching living vegetation could be separately recorded at each 10cm height from ground level to 1.8 m (and if required, separately recorded for each plant species encountered). Results can be condensed to offer a figure for the mean number of vegetation 'hits' recorded at each height in an average quadrat (or per 100 pins). This method is, however, extremely labour intensive. Accordingly in 1985 a simpler technique was employed. A standard ranging pole was inserted into the vegetation 100 times in each plot at randomly determined positions. In each case records were again taken as to whether or not the pole was touched by vegetation at each 10 cm interval above ground level. Records were accumulated over 100 poles to provide again a frequency distribution for the number of vegetational hits recorded at each height.

Changes after grazing in woodland

19

Animal sampling: small mammals A regular routine of small m a m m a l trapping was carried out in each plot by S. D. Hill from February 1983 until June 1984. Traps were positioned in pairs at 15 m intervals in a 7 x 7 grid; (thus a total of 100 traps were spread over a grid of 0.81 ha). The plots were sampled at intervals of approx. 12 weeks through 1983 and at 4-week intervals in 1984. On each visit traps were prebaited for a pretrapping period of 3 days. Traps were then set and checked for a catching period of a further 3 days. Animal sampling: ground invertebrates A survey of ground invertebrates was carried out in August and September 1985, using pitfall traps (e.g. Gist & Crossley, 1973; Luff, 1975). Twenty traps were positioned in each plot. Each trap consisted of a plastic container of 10cm diameter and 14cm deep, set into the ground so that its lip was flush with the soil surface. Traps were filled to 4 cm depth with water to which a few drops of detergent had been added as a wetting agent. All traps were emptied at the end of a week and trapping continued over a 3-week period.

RESULTS

Species composition and population structure of the trees The plots were established in mature woodland dominated by oak and beech, and with some Douglas fir, Scots pine and larch. The first measurements o f d b h of trees in sample quadrats were taken in 1977 (Fig. 2). At that time the experiment had been running for 14 years; most trees of < 10 cm would thus have become established within that period. If we ignore these and consider only the larger trees, then the survey provides us with a reasonable picture of the woodland structure at the time that the plots were erected. The largest trees ( > 30 cm dbh) were mainly of oak, beech and Scots pine, which occurred in similar numbers in both plots, and Douglar fir which was more abundant in the ungrazed plot. Of the smaller trees from 10-30 cm dbh, beech was by the far the most abundant and accounts for 56% of individuals in this size class. The data suggest that even before 1963 a gradual change had been taking place in the species composition of the woodland, with increasing dominance by beech. The basal area of trees over 10cm dbh was 17"6m2ha -1 in the grazed pen and 17-7m2ha -1 in the ungrazed. It is clear from these data that at the start of the experiment the structure and composition of the vegetation in the two plots must have been very similar. There was probably very little tree regeneration occurring when the

R. J. Putman, P. J. Edwards, J. C. E. Mann, R. C. How, S. D. Hill

20

GRAZED PLOT Betula spp

Fagus sylvatica

3°L

20

10 0

1oI Ilex aquifolium 0

UNGRAZED PLOT

i i .L

Larix decidua

0

~

Plnt:¢

cv

~it

ri~

v

"6 I~] Pseudotsuga menzesii E •~

(~u~rcu~

r~htlr

v

Salix atrocinerea

lO

0 I0 20 3~0 40 .50 6'0 70 8'0 9~0 dbh (10 cm classes)

0 10 20 30 40 50 60 70 80 90 dbh (10crn classes)

Fig. 2. Sizefrequency distribution of trees (in 10cm dbh classes)in the grazed and ungrazed plots in Denny Lodge in 1977. The data were recorded in 20 circular quadrats of 10 m radius (total area = 0.628 0 ha) but are presented here on a 'per hectare' basis.

plots were formed. In 1969, six years after establishment, there was vigorous regeneration of trees in the ungrazed plot. There was a large number o f birch Betula pendula and B. pubescens saplings with a mean height o f 93 cm, and saplings of oak, beech, Douglas fir and Scots pine were also common. By 1977 the gaps between large trees in the ungrazed plot were dominated by birch saplings up to 5 m tall, and there were also abundant saplings of beech, oak, Scots pine, Douglas fir and holly. Other species present in smaller numbers included hawthorn, sycamore Acer pseudoplatanus, larch, spruce Picea abies and blackthorn (Fig. 2). The density of trees < 1 0 c m d b h was 6440 ha-1. In contrast there was no evidence from either survey that any trees had become established in the grazed plot since the start of the experiment and the density o f trees < 10cm dbh was 20 ha-1 in 1977.

Changes after grazing in woodland

21

By 1985 there was little change in the grazed plot but the ungrazed plot was an impenetrable thicket o f birch, sallow Salix cinerea and Douglas fir. Figure 3 shows the size distribution o f trees < 10 cm dbh in this plot. The density of saplings was by now 7115 h a - 1 but there were very few o f the smallest ( < 1 cm dbh) and it was clear that with the closure of the canopy establishment had virtually ceased. Although dbh is not a reliable indicator of tree age, especially when comparing species, the data do suggest that sallow was one of the first species to be affected by the developing canopy. Establishment of pine and birch continued until more recently, but most of the smallest (and presumably youngest) saplings are of oak and Douglas fir. In addition to the obvious differences in structure between the two plots, there are also m a r k e d differences in species composition of the trees present. Certain species were recorded only in the plot where grazing has now been Betula spp (3405)

Fogus sylvatica (172)

.°1

3O

%

P$

%

v

40" Quercus robur (356)

%

Salix atrocinerea (694)

3°11L 20-

10-

0

0

1

2

3

4

5

6

7

dbh (lcm classes)

Fig. 3.

8

9

10

1

2

3

4

5

6

7

8

9

10

dbh (lcm classes)

Size frequency distribution of small trees (< 10cm dbh, in 1cm dbh classes) in the ungrazed plot in Denny Lodge in 1985, expressed on a percentage basis.

22

R . J . Putman, P. J. Edwards, J. C. E. Mann, R. C. How, S. D. Hill

prevented: holly, hawthorn, sallow, goat willow Salix caprea, and blackthorn were recorded in this plot in both 1977and 1985, with additional species recorded for the first time in the 1985 survey as maple, alder buckthorn Frangula alnus, and rowan Sorbus aucuparia. Even those species common to both enclosures are markedly higher in abundance within the ungrazed area (Figs 2 and 3).

Changes within the herb and shrub layers Although no detailed survey of the vegetation in the two plots was carried out when they were first established in 1963, we can gain some impression of what the shrub and herb layers must have been like at this time by reference to the surrounding woodlands. These are heavily browsed by the Forest's larger herbivores and typically have a very thin understorey of holly and some hawthorn; there is usually a clear browse line at 2 m above the ground. The herb layer is usually sparse and composed chiefly of unpalatable species such as Hyacinthoides non-scripta, Oxalis acetosella and bracken. On open rides there is a close-cropped turf dominated by Agrostis capillaris, and with several other species including A. canina, Deschampsia cespitosa, Molinia

caerulea, Carex demissa, C. panicea, Juncus articulatus, J. effusus, Ranunculus repens, and Potentilla erecta. By the first detailed survey of 1969 there were clear differences between the two plots in the quantity and species composition of the herb and shrub layer. In the ungrazed plot the browse line had become indistinct and there was a dense shrub layer of bramble, with gorse Ulex europaeus, sallow and heather Calluna vulgaris especially where the canopy was open. Holly and ivy Hedera helix were also much more abundant than in the grazed plot. As in 1969, marked differences were recorded in both 1977 and 1985 in the composition of the ground flora of grazed and ungrazed plots; these differences mirror closely the changes observed within the ungrazed plot over time (Table 1). Thus species recorded only in the grazed area include

Molinia caerulea, Juncus conglomeratus, Luzula campestris, Digitalis purpurea, while Hypericum perforatum, Epilobium montanum, Rosa sp. and Calluna vulgaris occurred only in the ungrazed plot. Of those species common to both plots, Lonicera periclymenum and Rubus fruticosus agg. were significantly more abundant in the ungrazed plot in both 1977 and 1985 (P < 0-001), while Agrostis capillaris and Deschampsia cespitosa were more abundant in the grazed plot. Measures of diversity in both 1977 and 1985 showed species diversity to be higher in the ungrazed plot. Overall, it is clear that, by 1985, some 22 years after inclosure, the shrub layer of the ungrazed plot was becoming rather thin and dominated by bramble. Gorse and heather, which had previously been abundant, had by

Changes

after grazing

23

in w o o d l a n d

TABLE 1 Species Composition of the Ground Flora in the Grazed (G) and Ungrazed Plots (U): Frequency of Occurrence of Species i n 20 Quadrats in 1969, 1977 a n d 1985 Species

1969

1977

G

U

G

1985

U

G

U

--

--

Agrostis

canina

2

2

--

1

Agrostis

capillaris

2

2

10

1

--

1

---

Anthoxanthum Calluna

odoratum

vulgaris

Descharnpsia Digitalis

--

--

--

cespitosa

purpurea

Epilobiurn

montanum

Euphorbia

amygdaloides

--

6

2

--

6

10

3

1

--

3

--

2

--

2

1

.

Festuca

rubra

2

1

--

saxatile

2

1

--

Hedera

helix

Hypericum Juncus

conglomeratus

Lonicera Luzula

caerulea

Pteridium Rosa

7 3

--

2

6

2

8

1

3

--

10

10

4

--

1

1

--

--

13

15

13

13

--

13

16

--

--

europaeus

2

4

Viola riviniana

4

2

--

3

6

7

--9

--

19

2

1

--

1

--

2

--

--

---

8

-3

9 --

7

7

--

3 --

7

arvensis/canina scorodonia

5

1 1

5

14

Teucrium

-1

--

--

9

--

agg.

--

--

1 --

.

9

aquilinum

Rubus ]ruticosus Ulex

--

1

10

campestris

acetosella

3

--

periclymenum

Molinia Oxalis

--

perforaturn

--

6 1

.

4 --

-.

Galium

8

20 --

3

1

now largely disappeared, or were growing very poorly under the dense canopy of saplings. The herb layer was extremely sparse and composed chiefly of ivy (very scarce in the grazed plot) and the moss Thuidium tamariscinum; furthermore, by this time the biomass of the herb layer was lower than in the grazed plot. Only on the former rides was the cover of trees incomplete, and here rank and etiolated grassland species could still be found beneath sprawling masses of bramble. In contrast to the thicket of the ungrazed plot, the grazed plot remained very open and by 1985 the shrub layer had almost disappeared except where there was bracken. Indeed holly, gorse and hawthorn, which had been present in the 1969 survey, had largely disappeared. The most abundant herbs beneath the canopy were Deschampsia cespitosa, Viola riviniana and Oxalis acetosella (Table 1). In a survey in October 1986 a total of 66 flowering plant and fern species

24

R. J. Putman, P. J. Edwards, J. C. E. Mann, R. C. How, S. D. Hill

were found in the grazed plot. Of these 26 were in the woodland and 40 were grassland, marsh and ruderal species such as Carexpanicea, Juncus bufonius, Ranunculus repens and Trifolium repens, which were confined to the rides. In the ungrazed plot a total of 52 species were found, of which 27 were confined to the rides. It was clear that many of the smaller and more light-demanding species (e.g. Juncus bufonius, Anagallis tenella) had been lost. Twelve species were found in the ungrazed plot only, including woodland herbs such as Brachypodium sylvaticum, Poa nemoralis, Conopodium majus and Dryopteris carthusiana, and early successional trees such as rowan, goat willow and alder buckthorn. All of these species are c o m m o n in the surrounding woodland. However one 'new' species, Lathyrus montanus, was found whose presence in the plot is harder to explain.

Profile of the vegetation In both 1977 and 1985 the structural profile of the vegetation in the first 2 m above ground level was assessed by recording the number of vegetational 'hits' at different heights on a series of sample poles inserted vertically into the vegetation. Figures 4a and 4b show histograms of the proportion of vegetational interceptions (= vegetational bulk) recorded at different heights in each of the two areas in 1977 and 1985. In neither year did total vegetational bulk in the 2 m profile differ significantly between grazed and ungrazed plots; and in both areas the majority of the vegetation is concentrated in the first 50-60cm above the ground, with the volume of (b)

(a)

Height (cms)

Hei! Iht(cms)

1977

180 - -

180 - -

1985

i

160

160 -

140

140

120

120

100 - "

100

8O i ~ .

8 0 m.

•- I

Ii

60 --

6O 4

0

40

~

Ungrazed J Grazed .

n

20

2 0 - -

lb

2'o

3'o

4'o

of vegetational bulk

so

0

lb

20

3"0

4'0

•

5'o

~ of vegetational bulk

Fig. 4. Structural profile of the herb and shrub layer vegetation up to 1.8m above the ground, showing distribution of vegetation bulk in grazed and ungrazed plots in (a) 1977, and (b) 1985.

Changes after grazing in woodland

25

plant matter declining rapidly above this level. Clear differences between the plots are, however, apparent. From 20-170 cm there is a significantly greater volume ofvegetation in the ungrazed plot at all heights; indeed in all surveys, virtually no vegetation at all was recorded in the grazed plot between 80-170 cm (the height of the visible browse line). Because plants in the grazed plot tended towards a prostrate or dwarf growth form and there was poorer light penetration in the ungrazed area, the volume of vegetation at ground level and in the first 10 cm is consistently higher in the former than in the latter. Little difference between the profiles established in 1977 and 1985 is apparent in the grazed plot. However, in the ungrazed plot, the vegetational structure clearly changed during that 8-year period: significantly less vegetation was recorded between 60-100 cm in 1986, with more vegetation apparent at ground level (0cm).

The small mammal community The number of small mammals of different species trapped on a standard trapping grid in 1983-84 are shown in Table 2 (from Hill, 1985). Differences between the grazed and ungrazed areas are immediately apparent. Three species of small mammals (Apodemus sylvaticus, Clethrionomys glareolus, Sorex araneus) were regularly recorded throughout the trapping period in the ungrazed plot, with a further two species recorded only occasionally (Apodemus flavicollis and Sorex minutus). In the grazed area A. sylvaticus TABLE 2 Numbers of Small Mammals of Different Species Trapped in a 0.8 ha Standard Grid in 300 Trap-Nights during 1983-1984 (Data from Hill, 1985)

Species

Treatment

1983

1984 Week no.

Week no.

Apodemus sylvaticus Apodemus flavieollis Clethrionomys glareolus Sorex araneus Sorex minutus

Ungrazed Grazed Ungrazed Grazed Ungrazed Grazed Ungrazed Grazed Ungrazed Grazed

6

24

36

46

2

6

10

14

18

22

31 6 0 0 24 0 3 0 0 0

21 6 1 0 37 0 3 0 0 0

33 10 0 0 18 0 1 0 1 0

15 1 0 0 35 0 6 0 1 0

12 5 0 0 31 0 0 0 0 0

9 2 0 0 16 0 0 0 0 0

9 0 0 0 17 0 2 0 0 0

9 0 0 0 8 0 0 0 0 0

8 0 0 0 15 0 0 0 0 0

7 0 0 0 20 0 0 0 0 0

26

R.J. Putman, P. J. Edwards, J. C. E. Mann, R. C. How, S. D. Hill

alone was recorded and consistently at lower densities than in the ungrazed site. Invertebrates

Numbers of different species of invertebrates trapped in 400 pitfall days in the two plots during August and September 1985 are recorded in Table 3. Differences between the two plots in species composition and relative TABLE 3

Numbers of Ground Invertebrates Trapped in 420 Pitfall Nights (August/September 1985)

INSECTA Order

Order

Order

Order Order

Coleoptera Histeridae Carabidae Silphidae Staphylinidae Scarabeidae Larvae Hymenoptera Formicidae Ichneumonidae Diptera Calliphoridae Dolichopodidae Dryomyzidae Muscidae Phoridae Tipulidae Syrphidae Larvae Dermaptera Collembola

ARACHNIDA Order Araneae Order Phalangida (Opiliones) MALACOSTRACA Order Isopoda OTHERS TOTAL

Grazed

Ungrazed

17 431 3 108 14 24

35 508 6 24 24 40

181 39

65 32

6 13 285 40 196 3

13 78 421 53 445 10

1

2

3 4 216

7 360

107 38

37 71

8

12

13

11

1750

2254

Changes after grazing in woodland

27

abundance were highly significant (G-test; P < 0.001). Amongst the beetles the most clear-cut differences emerged as greater abundance of rove beetles (Staphylinidae) in the grazed plot, with a greater number of ground beetles (Carabidae) in the ungrazed area. At the species level, two species--Ocypus olens (Staphylinidae) and Nebria brevicollis (Carabidae)--were present only in the grazed plot (but were present in appreciable numbers); another carabid, Philonthus cognatus, was also notably more abundant in the grazed area. Indeed amongst the Coleoptera only one species, Abax parallelepipedus, was markedly more frequent in collections in the ungrazed site. Differences between the plots were also apparent in other faunal groups. Ants, in particular the wood ant Formica tufa, were more abundant in the grazed area, as were all spiders recorded. No species occurred only in the ungrazed area, but flies of all groups were more abundant there than in the grazed pen, as were harvestmen (phalangids).

DISCUSSION The woodlands of the New Forest, including those in which the experimental plots were established in 1963, have for centuries supported high populations of deer and other large herbivores. The plots were thus set up within an area of woodland which reflects in its structure and species composition this long history of grazing. Since 1963 the plot in which deer have been kept appears in practice to have sustained more intensive browsing than the vegetation outside, and this is reflected in the shrub and herb layers. The deer have prevented any tree regeneration, and have eliminated almost all holly, hawthorn and other understorey, even where these persist in the general forest woodlands beyond the plots. Gorse, where it persists within the plot, is severely 'hedged'. The species composition of the herb layer reflects both the selectivity of grazing which favours unpalatable species, and also the maintenance of open conditions, favouring a wide range of light-demanding grassland species in the rides. In contrast, the ungrazed site has been released from the pressures of large herbivores for the first time in centuries. The role of deer in preventing woodland regeneration is dramatically revealed by the thicket of saplings which rapidly became established. A succession has occurred in the ungrazed plot which can be summarised as follows (Fig. 2 shows the dbhclasses of different species in 1977, as a kind of'time-slice'). By 1969, six years after enclosure, a dense scrub of gorse, heather, sallow and brambles had developed within the ungrazed plot with abundant saplings of birch, oak, beech and other tree species. After some 14 years, in 1977, the open areas had become a birch thicket and light-demanding species such as gorse and

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heather were in decline. After 22 years (1985) tree seedling establishment had ceased (Fig. 2) and there was evidence of self-thinning of birch and sallow. Oak and beech were growing more slowly beneath the thicket. Many of the plant species which became abundant in the early stages following exclosure were probably always present, either as seed or as small plants suppressed by browsing (e.g. heather, gorse, Brachypodium sylvaticum). The seeds of several other species were probably introduced from the immediate neighbourhood. It is striking that those 'new' species which have become established all have seeds which are bird-dispersed (e.g. ivy, alder buckthorn, blackthorn) or have good wind-dispersal (Salix spp, Betula). All plants now established within the ungrazed plot---except possibly the single specimen of Lathyrus montanus--probably originated in the site itself or its immediate vicinity. While there are clear differences in relative species abundances between grazed and ungrazed plots, differences in actual species composition are rather few, and one of the striking conclusions of this study is just how little the area released from grazing has changed in terms of species composition in the succeeding 25 years. Clear differences in three-dimensional structure were, however, apparent in both 1977 and 1985 surveys between the grazed and ungrazed plots. Although the total bulk of vegetation recorded within the full 2 m profile was similar in each case, the distribution of that vegetation was clearly different in the two plots (Fig. 4). In the grazed plot much of the apparent bulk of vegetation between 10 cm and 70 cm is due to bracken, which is very patchily distributed, so that some areas have very high vegetation volume in this zone, while others lack ground flora completely. By contrast, vegetational structure of the ungrazed plot is more homogeneous, with regeneration occurring everywhere except in the deepest shade. Because so much of the structure of the middle-storey of the grazed plot is contributed by bracken--a deciduous species-differences in vegetational structure between the two plots were minimised at the time of our surveys in summer. Differences become even more apparent in winter when the bracken dies back and little or no vegetation is then found in the grazed plot in the 10-70cm zone. Such differences in vegetational structure and maturity might be expected to influence the animal community. Vegetational complexity in itself is frequently claimed to affect the number of potential niches available for animals and thus diversity (e.g. MacArthur & MacArthur, 1961; Rosenzweig & Winakur, 1969; Strong et al., 1985), while changes in structure and vegetation density may alter the nature and availability of food and cover offered to a dependent fauna. Marked differences were recorded between the two plots in the small mammal populations in 1983-84, and in the ground invertebrates recorded in 1985.

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Most animal species show distinct habitat preferences, selecting those which provide appropriate food supplies and the desired level of cover. For example, the British species of small mammals recorded in the study have all been shown previously to exhibit predictable variation in numbers in relation to available cover (e.g. Hoffmeyer, 1973; Corke, 1974; Schropfer, 1983). Vegetational differences effected by differing grazing pressures might thus be expected to result in changes in the mammal fauna associated with grazed and ungrazed woodlands. In grazed areas there is less structural diversity within the vegetation and little cover; suitable food for herbivorous or primarily insectivorous species will also be restricted. Within the structurally more complex habitat of the ungrazed plot a further four small mammal species were encountered, and A. sylvaticus populations were supported at much higher density. These results emphasise the importance of habitat structure in controlling the distribution and abundance of small mammals and also illustrate the potentially dramatic influences of grazing. By using pitfall traps to sample invertebrate fauna, we necessarily restrict consideration to particular guilds, primarily those of the forest floor. Active, wide-ranging species will be sampled more effectively than other groups and our samples cannot offer a clear picture of differences among, for example, phytophagous insects, which might also be expected to show major change. Despite this, differences in ground invertebrates between the two sites are clear and may relate to differences in vegetation structure. Abax parallelepipedus was recorded in both grazed and ungrazed areas, but Nebria brevicollis only in the grazed plot. Greenslade (1964) noted that A. parallelepipedus preferred habitats offering a high degree of cover at the ground level, particularly shrubs, while N. brevicollis preferred a leaf litter habitat with ground and shrub cover less than 20% and 50% respectively. The greater shrub cover in the ungrazed plot at all times may explain why although A. parallelepipedus was recorded in both plots, abundance was significantly higher in the ungrazed area, where this species comprised 55% of all beetles trapped. This same high degree of shrub cover, however, excluded N. brevicollis from the ungrazed plot. Grazing may of course produce other differences between the two sites not directly related to its influence on vegetational structure. Ocypus olens, also restricted in distribution to the grazed plot, is a dung feeder and its restricted distribution may depend on the presence of grazing animals. Other differences in the invertebrate fauna of the two areas are perhaps more difficult to interpret. The greater abundance of harvestmen recorded from the ungrazed plot, or the apparent concentration of spiders in grazed areas, may simply reflect differential sampling efficiency of pitfall traps in areas whose vegetation structure at ground level is already known to differ (Luff, 1975).

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The vegetational succession observed in the ungrazed plot differs from the process of regeneration of a woodland gap in that there was a welldeveloped scrub phase when the site became dominated for a few years by gorse, heather and sallow, and by tall grasses such as Deschampsia cespitosa and Molinia caerulea. In this respect the process resembled succession from grassland. However, an abundant tree cover developed very rapidly so that the scrub phase was very short-lived. The reason may partly have been the proximity of an abundant seed source, but may also reflect more suitable conditions for tree seedling germination in established woodland. Factors which may be important include the presence of the fungal partners of mycorrhizae, and suitable microsites for seed germination. Successful germination of many tree seeds requires conditions of high humidity (Fenner, 1985), for example, in woodland litter rather than in grassland. Woodland animals which bury seed, particularly jays and squirrels, may play an important role in promoting optimal conditions for seedling establishment (Watt, 1923; Jensen, 1985). The grassy rides were the only areas of the ungrazed site where a thicket of saplings did not develop and the scrub phase persisted. The animal communities which we have studied have increased significantly in diversity over the period since the relief of grazing. When diversity indices are calculated for both the small mammals and the ground invertebrates, species richness and overall diversity of both groups are seen to be higher in the ungrazed than in the grazed area. By contrast, the plant community, even after 25 years, still remains species-poor. Why is the recovery of vegetation in the plot released from grazing pressure so incomplete in terms of species composition? In the nearby Brockenhurst woods--a site on similar soil but without the same history of heavy grazing--a total of 203 herbaceous species and 56 species of trees, shrubs and climbers have been recorded. If incomplete recovery of such communities following perturbation is a general phenomenon, then it has important and wide-ranging implications. An important factor affecting the speed and the extent of the recovery is the degree of isolation of the system from potential colonisers. Our study area, while released from grazing in 1963, nonetheless remains surrounded by many thousands of hectares still heavily grazed, and is isolated from 'typical' deciduous woodlands which might act as a seed source. Perhaps this helps to explain the limited degree of recovery of the vegetation in terms of species richness. The different degree of recovery experienced in the flora and in the fauna may be due to the generally greater dispersal ability of many animal species. Finally in this discussion we must stress that we report here a study of secondary succession in woodland after grazing has ceased. It would be unwise to draw retrospective conclusions (however tempting it may be to do

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SO) about the effects of the grazing pressure in the first place on the species composition o f the grazed woodland. A C K N O W L E D G E M ENTS We would like to express our debt to the late Judy Rowe for allowing us to use the hitherto unpublished results of the 1969 survey and for her continued interest in the project until her death in 1985. We would also thank the Forestry Commission (New Forest) and Forestry Commission Wildlife and Conservation Research Branch (Forest Research Station, Alice Holt) for permission to work in the experimental plots at Denny Lodge. Finally, our thanks also go to D r Paul Vickerman for help with insect identifications. REFERENCES Bakker, J. P., de Bie, S., Dallinga, J. H., Tjaden, P. & de Vries, Y. (1983). Sheepgrazing as a management tool for heathland conservation and regeneration in the Netherlands. J. Appl. Ecol., 20, 541-60. Bakker, J. P., de Leeuw, J. & van Wieren, S. E. (1984). Micro-patterns in grassland vegetation created and sustained by sheep-grazing. Vegetatio, 55, 153-61. Bobek, B., Perzanowski, K., Siwanowicz, J. & Zielinski. J. (1979). Deer pressure on forage in a deciduous forest. Oikos, 32, 373-9. Corke, D. (1974). The comparative ecology of two British species of the genus Apodemus (Rodentia: Muridae). PhD thesis, University of London. Coupland, R. T. (1979). Grassland Ecosystems of the World: Analysis of Grasslands and Their Uses. Cambridge University Press, Cambridge. Crawley, M. J. (1983). Herbivory: The Dynamics of Animal-Plant Interactions. Blackwell Scientific Publications, Oxford. de Bie, S., Joenje, W. & van Wieren, S. E. (eds) (1987). Begrazing door vertebraten. Pudoc, Wageningen. Edwards, P. J. & Gillman, M. (1987). Herbivores and plant succession. In Colonization; Succession and Stability, ed. by A. J. Gray, M. J. Crawley & P. J. Edwards. Blackwell Scientific Publications, Oxford, pp. 295 314. Fenner, M. (1985). Seed Ecology. Chapman and Hall, London. Gist, C. S. & Crossley, D. A. (1973). A method for quantifying pitfall trapping. Environ. Ent., 2, 951-2. Grant, S. A. & Hunter, R. F. (1966). The effects of frequency and season of clipping on the morphology, productivity and chemical composition of Calluna vulgaris. New Phytol., 65, 125-33. Greenslade, P. J. M. (1964). The distribution, dispersal and size of a population of Nebria brevicollis (F.) with comparative studies on three other Carabidae. J. Anim. Ecol., 33, 311-33. Harper, J. L. (1977). Population Biology of Plants. Academic Press, London. Hill, S. D. (1985). Influences of large herbivores on small rodents in the New Forest, Hampshire. PhD thesis, University of Southampton. Hoffmeyer, I. (1973). Interaction and habitat selection in the mice Apodemus flavicollis and Apodemus sylvaticus. Oikos, 24, 108-16.

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How, R. C. (1986). An investigation into the vegetational and invertebrate differences between ungrazed and grazed areas of enclosed woodland in the New Forest. BSc thesis (Biology), University of Southampton. Jensen, T. S. (1985). Seed-seed predator interactions of European beech, Fagus sylvatica, and forest rodents Clethrionomys glareolus and Apodemus flavieollis. Oikos, 44, 149-56. Krefting, L. W., Stenlund, M. H. & Seemel, R. K. (1966). Effect of simulated and natural browsing on mountain maple. J. Wildlife Manag., 30, 481-8. Luff, M. L. (1975). Some features influencing the efficiencyof pitfall traps. Oecologia, Berl., 19, 345-57. MacArthur, R. H. & MacArthur, J. W. (1961). On bird species diversity. Ecology, 42, 594-8. Mann, J. C. E. (1978). An investigation into the vegetational differences between an ungrazed and a grazed portion of the New Forest, with special emphasis on the species composition, species diversity and productivity of the areas. BSc thesis (Biology), University of Southampton. McNaughton, S. J. (1979). Grassland-herbivore dynamics. In Serengeti: Dynamics of an Ecosystem, ed. by A. R. E. Sinclair & M. Norton-Griffiths. University of Chicago Press, Chicago, pp. 46--81. Moore, D. M. (1982). Flora Europaea Checklist and Chromosome Index. Cambridge University Press, London. Peterken, G. F. & Tubbs, C. R. (1965). Woodland regeneration in the New Forest, Hampshire since 1650. J. appl. Ecol., 2, 159-70. Pigott, C. D. (1985). Selective damage to tree seedlings by voles Clethrionomys glareolus. Oecologia Berl., 67, 367-71. Putman, R. J. (1986). Grazing in Temperate Ecosystems: Large Herbivores and the Ecology of the New Forest. Croom Helm, Beckenham. Rosenzweig, M. L. & Winakur, J. (1969). Population ecology of desert rodent communities: habitats and environmental complexity. Ecology, 50, 558-72. Schropfer, R. (1983). The effect of habitat selection on distribution and spreading in the yellow-necked mouse (Apodemus flavicollis). Proceedings of the 3rd International Theriological Congress, Helsinki. Shannon, C. E. & Weaver, W. (1949). The Mathematical Theory of Communication. University of Illinois Press, Illinois. Spedding, C. R. W. (1971). Grassland Ecology. Clarendon Press, Oxford. Strong, D., Lawton, J. H. & Southwood, T. R. E. (1985). Insects on Plants. Blackwell Scientific Publications, Oxford. Thalen, D. C. P. (1984). Large herbivores as tools in the conservation of diverse habitats. Acta Zool. Fenn., 172, 159-63. Tubbs, C. R. (1986). The New Forest. Collins, London. Watt, A. S. (1923). On the ecology of British beechwoods with special reference to their regeneration. J. Ecol., II, 1-48.