Effects of disturbance on the biodiversity and abundance of isopods in temperate grasslands

European Journal of Soil Biology 42 (2006) S254–S268 http://france.elsevier.com/direct/ejsobi

Original article

Effects of disturbance on the biodiversity and abundance of isopods in temperate grasslands A. Moss, M. Hassall* Centre for Ecology, Evolution and Conservation, School of Environmental Sciences, University of East Anglia, Norwich NR4 7JT, UK Available online 26 July 2006

Abstract Connell’s ‘intermediate disturbance hypothesis’ was tested using a relatively simple, species poor isopod community in grass heaths and in a coastal sand dune grassland. Variation in diversity resulted from disturbance both to the soil profile and sward structure due to grazing. Predictions from a spatial survey were tested using a 20 years time series. These changes were related to changes in rabbit activity, anthropogenic soil disturbance and on one site, deposition of blown sand. Changes in the soil profile resulted in diversity initially increasing due to decreases in the density of the commonest species, leading to an increase in equitability. Prolonged disturbance to the soil profile both due to sand blowing onto one site and rotavating on another, lead to a reduction in diversity due to one of the species being eliminated. The isopod community was most diverse when least disturbed by grazing, of intermediate diversity under intermediate grazing intensity and least diverse when most heavily grazed. In these simple communities, differences in diversity were mostly determined by differences in equitability rather than in species richness. We conclude that maximising heterogeneity of sward structure could have advantages for the conservation of both invertebrate biodiversity and vertebrates that feed on them. © 2006 Elsevier Masson SAS. All rights reserved. Keywords: Diversity; Equitability; Grazing; Sward structure; Population dynamics; Conservation; Woodlice

1. Introduction In temperate regions most sites of conservation interest are disturbed by man to some extent. A central challenge of conservation management is to optimise the levels and patterns of disturbance for conservation objectives. In the Breckland district of East Anglia these objectives include the conservation of disturbance specialist species such as a suite of flowering plants characteristic of highly disturbed soils and the flagship conservation animal of the district—the stone curlew—that requires * Corresponding

author. Fax: +44 1603 591 327. E-mail address: [email protected] (M. Hassall).

open disturbed swards for nesting [38]. Invertebrates also form an important component of the fauna of Breckland grass heaths and, as in many other systems, comprise the majority of the biodiversity there. Disturbance can be defined as an event that disrupts community structure and changes available resources, substrate availability or the physical environment [58]. Disturbance often creates spaces more suitable for earlier successional species. If it is uniformly severe it can result in a relatively simple community of pioneer species with good colonising ability but when variable in time and/or space may result in a mosaic of habitat patches at different stages of succession. Such a patchy community is often more diverse than either one which is uniformly heavily disturbed or one completely undisturbed, dominated by fewer highly competitive species.

1164-5563/$ - see front matter © 2006 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.ejsobi.2006.07.013

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This principle is encapsulated in the ‘intermediate disturbance hypothesis’ [8,35]. Initially formulated in relation to tropical rainforests and coral reefs [8] the theory has subsequently been supported by studies of many other ecosystems: intertidal [47], streams [51], wetlands [3], alpine [20], deserts [26], forests [53] and planktonic communities [19]. In grassland ecosystems, herbivory (and vertebrate grazing in particular) is perhaps the most significant form of disturbance associated with changes in diversity [5,41,43]. The impacts of grazing vertebrates on grassland plant communities are generally consistent with the intermediate disturbance hypothesis [15,5,6], but for most taxa of above ground grassland invertebrates, species richness and/or abundance increases with a decrease in grazing pressure [43,37,13]. In many terrestrial ecosystems the majority of animals are soil invertebrates which have been studied much less despite being key system regulators that directly or indirectly modulate the biological, chemical and physical processes within the soil [54,39]. Most previous studies of the effects of disturbance on biodiversity of below ground communities have concentrated on the consequences for species richness [55,36]. In this paper we highlight the importance of the equitability component of diversity, in a community with relatively few species: terrestrial isopods in temperate grasslands. Isopods form suitable model soil invertebrates for such a study because their morphological [45] physiological [59] behavioural [34] and life history [7] adaptations to the terrestrial environment are well understood, as are their population dynamics [32]. This permits a reductionist approach to understanding changes in biodiversity in relation to changes in abundance of individual species that can be further resolved in relation to physiological and behavioural responses to their changed environment. We use this extensive background knowledge of isopod biology to analyse spatial patterns of diversity at one site. Then using these results we make predictions about the consequences of temporal changes in disturbance, caused by differences in grazing pressure and soil profile, that we test using four 20 years time series. This enables us to examine the intermediate disturbance hypothesis considering duration of disturbance, which is less commonly analysed than intensity. The results are discussed in relation to the conservation management of grasslands. As grasslands in the British Isles are plagioclimac communities, some form of disturbance is required continuously to prevent succession to scrub then woodland. This is particularly true

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of the Breckland district of East Anglia, of which the conservation interest is a direct result of historical cycles of grazing and soil disturbance [38]. The rare birds, plants and invertebrates characteristic of this district, all require extensive areas of very short sward with regular disturbance of the light sandy soils. We question whether application of such intense disturbance uniformly across all available sites maximises overall biodiversity, and hence whether it is the most appropriate management to achieve wider conservation objectives. 2. Materials and methods 2.1. Study sites and disturbance events Three grasslands in the east of England were studied. Spurn Head (53°34′N, 0°8′E) is a coastal sand dune site forming the northern tip of a peninsula between the mouth of the Humber estuary and the North Sea. The other two, Lakenheath Warren (52°23′N, 0°35′E) and Weeting Heath (52°28′N, 0°35′E), are inland grass heath sites in the Breckland district of East Anglia. The species composition and structure of the vegetation of the sites has been described by Hassall and Dangerfield [31,32], and history of sand blowing onto the Spurn Head site by Davis [11]. 2.2. Spatial analyses Effects of spatial differences in sward structure and soil disturbance on the isopod community at Weeting Heath were analysed, using abundance data for isopods collected during the summer of 1989 and presented by Hassall [30], who also describes the disturbance treatments on different parts of the site. For the conservation rationale of these treatments see Dolman and Sutherland [16]. In summary there were two sources of variation in sward structure, and two types of disturbance to the soil profile (Table 1). Sward structure was varied, due to: a) differences in rabbit grazing pressure from zero, in an exclosure established for 9 years (plot 4), through low (plot 3), to medium (plot 2), to high (plot 1) grazing intensity; and b) forage harvesting in the spring of 1989, i) on a heavily grazed area (plot 12) and ii) on a lightly grazed area (plot 6), both compared with adjacent comparably grazed central plots (13 and 7). High levels of soil disturbance were caused in Spring 1989, either by: a) ploughing, which completely overturned the surface layers of the soil (plot 10); or b) rotavating, which com-

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Table 1 Soil and sward disturbance regimes at Weeting Heath (for further details see Hassall [43]). Bold lines indicate controls paired with experimental plots Grazing intensity

Zero Low Medium High

Disturbance to sward Rabbit grazing Forage harvest 1989 Plot 4 Plot 3 Plot 6 Plot 2 Plot 1 Plot 12

Control

Disturbance to soil Past rotavation 1960– Rotavation (Ro) 1972 and 1980 1989

Plot 7 Plot 9 Plot 13

Plot 8

Ploughing (Pl) 1989

Plot 5 Plot 11

Plot 10

Table 2 Temporal variation in type, level and duration of disturbances on study sites 1968–2002 Site

Spurn

Type of disturbance Level of Zero disturbance Low Intermediate High

Rabbit grazing

Sand blow

1972–1994

1968–1972 1973–1994

1968–1972

pletely broke up the surface layers without burying them: (plot 11, in a heavily grazed area, and plot 5, in a lightly grazed area). A further plot, which had been rotavated annually from 1960 to 1972 and again in 1980 (plot 8), showed no evidence of soil disturbance, except that the sward was shorter here, due to nutrients having been lost, as a result of the previous repeated soil disturbance. All soil disturbance sites were compared to adjacent undisturbed ones with comparable levels of rabbit grazing (plots 13, 9 and 7) (Table 1). 2.3. Temporal analyses 2.3.1. Spurn head The coastal sand dune site was subject to two different types of disturbance: grazing by rabbits and deposition of sand from a sandy beach approximately 25 m from the edge of the study site (Table 2). Unlike the inland grass heaths, intensive rabbit grazing did not destroy the very tall, coarse, tussocks dominated by Ammophila arenaria and Arenatherium elatus characteristic of a fixed dune grassland [49]. In 1972 a rabbit proof fence was erected around the site, which eliminated grazing and resulted in the sward between tussocks growing longer and thicker. The morphology of this dune system changed during the study, due to changes in off shore current patterns. Between 1973 and 1975 the fore dunes, which had previously protected the study site from blown sand, eroded away, so that in the winters of 1973–1974 and 1974–1975

Weeting Open Heath Rabbit grazing 1985–1988 1982–1984 1989–1991 1981–1982 1991–2002

Weeting exclosure Rabbit grazing 1980–1989

Lakenheath Rabbit grazing

Cattle grazing

1981–2002 1990–1991 1992–2002

1999–2002

and subsequent years, sand was blown off the beach to cover the site with between 1 and 7 cm of sand per year [12]. This covered the litter layer, making it inaccessible to non-burrowing species and also resulted in significant direct mortality of terrestrial isopods [11]. 2.3.2. Weeting Heath A 20 years time series for the abundance and diversity of isopods for two of the plots from the spatial survey were analysed, one being the medium intensity grazing site, the other the zero grazing exclosure (Table 2). An index of sward height on the open heath site was derived for the whole period by first estimating an index of grazing intensity as devised by Grayson [21]. This involved estimating rabbit defecation rates by counting rabbit faecal pellets deposited in 100 × 0.25 m2 quadrats during 1 week intervals between 25th September and 30th October 2002. Stratified random sampling was used to place the quadrats in two grid systems each measuring approximately 60 × 20 m and positioned adjacent to the north and south sides of the 60 × 40 m study site described by Grayson and Hassall [22]. Pellets deposited during each period were distinguished from those deposited previously, using a reference collection of very freshly deposited pellets collected at the start of the observation periods and left under tethered wire mesh (to prevent the rabbits moving them), to weather for a week, after

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which they were distinctly lighter brown than the darker pellets deposited during the week. The index of grazing intensity derived from rabbit faecal pellet production rates was related to sward height and density (sward index) as measured using a “sward stick” [23] (90 mm disc diameter, 300 g disc weight). This relationship could then be used to convert data on faecal pellet production from 1979 until 1981 for this site [21] to estimates of sward length for that initial part of the time series. The index of grazing intensity was then related to visual estimates of the number of rabbits above ground in the southern half of the northernmost compartment of this nature reserve (approximately 5 ha) where rabbit numbers had been recorded during 1988 and 1990– 2002 by summer wardens on the site. For the missing year, 1989, faecal pellet and sward index data were obtained by Hassall [30]. 2.3.3. Weeting Heath exclosure A 60 × 40 m2 area of this grass heath was surrounded by rabbit proof fencing in April 1980 to experimentally exclude rabbits from grazing there [22]. By 1981 54% of the site was covered by tall rank tussocks [31]. At the start of 1990 this experiment was reversed when seven (five females and two males) rabbits were reintroduced into the fenced area where they rapidly bred. Numbers increased to over 20 individuals by the end of 1991 [60]. The associated increase in grazing, reduced the sward from a long tussocky structure (dominated by Festuca ovina and Avenula pratensis) to a very short sward [60]. Pellet production data for 1981 [21] and sward height data from 1989 to 1991 [60] were converted to an index of sward height/density using the same method as described above for the open heath site. 2.3.4. Lakenheath Warren The least disturbed site was Lakenheath Warren which from 1980 to 2000 was only very lightly grazed by hares, deer and a few rabbits [1,44]. In 1999 cattle were introduced to this site and rapidly reduced the long tussocky sward to a much shorter one of more even length. 2.4. Study species Three isopod species are examined in detail: Armadillidium vulgare (Latreille, 1804), Philoscia muscorum (Scopoli, 1763) and Porcellio scaber Latreille, 1804. These species are among the most common species

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found in Great Britain, overlapping substantially in their macro-distribution and commonly coexisting in calcareous grasslands [29] and dune systems [57]. Despite this coexistence they exhibit morphological, physiological and behavioural differences, which influence both abundance and distribution between and within habitats [56]. Following the terminology of Schmalfuss [45], P. muscorum is a ‘runner’ with long legs unsuitable for burrowing and with no pseudotrachea so the most susceptible of the three to moisture loss and consequently is an undisturbed sward specialist. P. scaber is a dorsoventrally flattened ‘clinger’ which aggregates more than the other two species as a way of reducing water loss but also has pseudotrachea to reduce moisture loss from respiratory surfaces. This species is found in the most open habitats and can be regarded as ‘a disturbed sward specialist’ [30]. A. vulgare also has pseudotrachea, is a ‘roller’ and burrows more deeply than the other two species to avoid adverse micro-climatic conditions [12]. It is adversely affected by high rainfall conditions [32] and found across the broadest range of sward heights and so can be termed ‘a sward height generalist’ although it peaks in abundance at intermediate levels of rabbit grazing [32] on these heaths. 2.5. Sampling and extraction Between 1981 and 2001, 20 × 0.038 m2 samples were taken from all sites as described by [32] and extracted in a high gradient extractor [33]. Prior to 1981, at the Spurn Head site, 14 × 0.1 m2 turf core samples were taken as described by Sunderland et al. [49]. 2.6. Analyses Mean densities m−2 for each species were calculated for each of the sites and for, on average, three to four sampling dates per year. From these seasonal means, annual mean densities were calculated. Diversity was measured using the Shannon index (H′) using the equation: S

H0 ¼
∑ pi log2 pi i¼1

where pi is the proportion of individuals of the ith species given by ni/N, where ni represents the number of individuals of the ith species, N the total sample abundance and S the total number of species in the sample. This index of species diversity is widely used to incor-

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Fig. 1. Weeting Heath spatial analysis. Experiment 1 Variation in grazing intensity: 1 high grazing (HG), 2 medium grazing (MG), 3 low grazing (LG), 4 zero grazing exclosure erected 1980 (Ex); Experiment 2 sward and soil manipulation under low grazing intensity: 5 rotavated Spring 1989 (Ro), 6 forage harvested Spring 1989 (FH), 7 low grazing control; Experiment 3 long-term rotavation under medium grazing intensity: 8 rotavated 1960–1972 + 1980 (Ro), 9 medium grazing control; Experiment 4 soil and sward manipulation under high grazing intensity 10–13 randomised experimental treatments: 10 ploughed (Pl), 11 rotavated (Ro), 12 forage harvested (FH), 13 high grazing control (HG); a) Shannon H diversity index, solid horizontal lines indicate the Shannon J equitability index for each site; b) relative abundance of isopod species at each site □ A. vulgare, ■ P. muscorum and P. scaber.

porate both the species richness and equitability components of diversity. Equitability was measured using Shannon J′ given by the following equation: J0 ¼

H0 log2 S

3. Results 3.1. Spatial variation in disturbance due to manipulation of the soil profile Isopod diversity in the spatially separated locations on Weeting Heath, which had been subject to different levels of disturbance to both the soil and the vegetation, varied between 0.5 and 1.5 (Fig. 1a). Anthropogenic disturbance to the soil profile, in the form of ploughing and rotavating 5 months earlier, (plots 10 and 11, respectively), resulted in significantly lower abundances but a higher diversity than in the control plot (plot 13). This is due to a significantly higher density of A. vulgare in the control dominating both the P. scaber

and P. muscorum populations and a much more even distribution of individuals between species in the experimental plots [30]. Similarly, lower densities but higher proportions of both these species in the spring rotavated plot (5) led to a higher diversity there than in the control plot (7) where A. vulgare occurred at the second highest density (600 m−2) of all the plots surveyed [30]. However the plot that had been rotavated annually between 1960 and 1972 (29–17 years previously) and in 1980 (9 years previously), then left undisturbed (plot 8), had a lower diversity than the control (plot 9) as there were no A. vulgare present on this old rotavated site. Ploughing (plot 10) resulted in a similar increase in diversity compared with the control (plot 13). 3.2. Spatial variation in disturbance due to differences in sward structure Forage harvesting (plot 12) resulted in an increase in diversity compared with the heavily grazed controls (plot 13). However, where the adjacent control (plot 7) was only lightly grazed, the forage harvested site (plot 6) showed a similar level of diversity.

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Fig. 2. Spurn Head time series 1968–1994: a) Annual mean Shannon H diversity index ± S.E. (solid line indicates 3 years running mean). Dashed line indicates Shannon J equitability index (3 years running mean); b) relative abundance based on annual mean densities. □ A. vulgare, ■ P. muscorum and P. scaber; c) annual mean densities ± S.E. Lines indicate 3 years running means. A. vulgare, P. muscorum and P. scaber).

With respect to grazing, isopod diversity was greatest in the ungrazed sward (4) and least in the medium (2) to high (1) intensity grazing plots with the low intensity one (3) having an intermediate level of diversity. Throughout this spatial series of plots, changes in total diversity were very closely mirrored by changes in

equitability (except for the one plot from which A. vulgare was absent altogether). From these results, concerning spatial differences in grazing intensity, it might be predicted: 1) if there was temporal variation in the soil profile on a site, where the vegetation and litter layer were buried under soil or

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Fig. 3. Weeting Open Heath time series 1981–2002: a) Sward height/density index; b) annual mean Shannon H diversity index ± S.E. (solid line indicates 3 years running mean), dashed line indicates Shannon J equitability index (3 years running mean); c) relative abundance based on annual mean densities □ A. vulgare, ■ P. muscorum and P. scaber); d) annual mean densities ± S.E. Lines indicate 3 years running means A. vulgare, P. muscorum and P. scaber.

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Fig. 5. Lakenheath time series 1981–2002: a) Solid line, 3 years running mean of annual mean Shannon H diversity index (± S.E.) and dashed line 3 years running mean of Shannon J equitability index; b) relative abundance based on annual mean densities □ A. vulgare, ■ P. muscorum and P. scaber; c) annual mean densities ± S.E. Lines indicate 3 years running means A. vulgare, P. muscorum and P. scaber.

Fig. 4. Weeting exclosure time series 1981–2002: a) Sward height/density index, 1981–1991 after Willott [61], 1991–2002 from photographic evidence and comparison with adjacent heath; b) solid line indicates 3 years running mean of annual mean Shannon H diversity index (± S.E.) and dashed line 3 years running mean for Shannon J equitability index; c) relative abundance based on annual mean densities □ A. vulgare, ■ P. muscorum and P. scaber; d) annual mean densities ± S.E. Lines indicate 3 years running means A. vulgare, P. muscorum and P. scaber).

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sand, diversity might initially increase but if it persisted might then decrease and 2) that if grazing intensity on one site were to vary over time then diversity of the isopod community would be higher when disturbance due to grazing was lower and reduced when grazing intensity increased. 3.3. Temporal variation in disturbance due to grazing and blown sand on the coastal site On the Spurn Head site diversity gradually increased between 1969 and 1972 (Fig. 2a) as A. vulgare immigrated onto the site while it was being heavily grazed. After the fence was erected, in 1972, and disturbance due to grazing eliminated, A. vulgare continued to increase for a further 2 years before declining steadily from 1975 until 1979, after sand began to be deposited on the site (Fig. 2c). The increase in A. vulgare on the site was inversely correlated with a decline in P. muscorum, which reached very low densities by 1974 and remained very low until 1979 when the population increased for 3 years, reflected by an increase in diversity. In 1980, the sampling regime was changed to a smaller core size. Grain size of sampling units can affect estimates of diversity, which can be reduced when in smaller samples [42]. However, in this case, the estimates of diversity increased after the change in sampling procedure so the observed trend was not an artefact arising from the change in protocol. Diversity declined again in 1983 as both A. vulgare and P. muscorum decreased until 1985, after which P. muscorum was almost entirely absent from the site. During the period 1985–1992 P. muscorum was replaced by an increase in the previously low-level population of P. scaber (Fig. 2b). 3.4. Temporal variation in high to medium disturbance at Weeting Heath The index of sward height/density (Fig. 3a) shows that grazing at Weeting Heath was most intense at the start of the study in 1981, then gradually declined during the 1980s with the swards reaching a maximum height in 1988. During this period the isopod community (Fig. 3c) consisted almost exclusively of A. vulgare and P. scaber with only very low numbers of P. muscorum in 1985 and 1986. The presence of a second species with a population comparable to the dominant A. vulgare is reflected in the diversity index, which remained between 0.6 and 0.9 from 1981 to 1988 (Fig. 3b). From 1989 onwards the rabbit population showed a steady increase with a consequent decline of

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the sward index. During this period diversity declined to below 0.2 as the P. scaber population rapidly fell to very low levels by 1991 (Fig. 3d). During the period from 1993 until 2001, A. vulgare also declined to such an extent that by the end of the study period the relative abundance (Fig. 3c) of the two species became more comparable with a parallel increase in the diversity index (Fig. 3b). From these temporal changes it could be predicted that, if grazing was eliminated altogether on this site, P. muscorum would increase, resulting in an increase in diversity, a trend which would be reversed if grazing was then re-introduced. 3.5. Temporal variation in disturbance in an experimental exclosure at Weeting Heath The exclosure experiment was used to test these predictions (Fig. 4). There was an initial increase in diversity once disturbance due to grazing was completely removed during the 1980s. This was a similar but steeper increase in diversity to that on the open heath where rabbit densities also decreased over this period. In the experimental exclosure the diversity index peaked at 1.5 in 1989 (Fig. 4b) mostly as a result of P. muscorum increasing markedly in the longer more tussocky sward. This trend was reversed rapidly when the rabbits were reintroduced, with P. muscorum declining to local extinction within 2 years of the grazing intensity increasing again, leaving A. vulgare as almost the only species of isopod present (Fig. 4c), resulting in a decline in diversity to less than 0.1. From the results for this experiment on the heavily grazed site it can be predicted that, on a site that never had high grazing intensity, A. vulgare would be the commonest species, P. muscorum next most abundant and P. scaber the least abundant. 3.6. Temporal variation on the low disturbance site at Lakenheath Warren The mean value of the Shannon–Wiener index at Lakenheath Warren over the whole study period was 0.94 and rarely dropped below 1.0 for the first 10 years (Fig. 5a). Between 1991 and 1995 diversity decreased, due to a decline in P. muscorum (Fig. 5c) (and increase in the relative abundance of A. vulgare [Fig. 5b]). P. muscorum recovered temporarily by 1997 then declined steadily again until 2002 with a consequent parallel decrease in overall diversity. The decline in the density of all three species seen at the end of the

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study period coincides with the introduction of cattle grazing to the site. 4. Discussion Terrestrial isopods form an important and dominant component of the soil macro-decomposer community in grassland ecosystems [48]. Indirectly their activities can have a considerable impact on decomposition, via: promotion of microbial respiration [64,65]; changes to detritus chemistry [63]; and facilitating shifts in microfaunal succession [28]. There is increasing evidence that not only abundance but isopod diversity [28,62] and species composition [64,63] could also impact upon these processes. It is therefore important to assess how disturbance affects the abundance and community characteristics of grassland isopods. In this study, use of both spatial analyses in one point of time and 20 years time series at four places on three spatially distinct locations, allows testing of the intermediate disturbance hypothesis with respect to two different types of disturbance. With respect to changes in the soil profile, both the spatial analysis of different anthropomorphic sources of disturbance at Weeting Heath and the temporal analysis of natural changes in the soil profile caused by blown sand at the coastal site, support the intermediate disturbance hypothesis. At Weeting Heath the isopod communities on both the recently rotavated and ploughed treatments were more diverse than on the corresponding control plots. This is because the dominant species in the control communities, A. vulgare, decreased as a result of the disturbance, while the other two species either remained the same or, in one plot, increased slightly, so that the equitability component of diversity increased while the species richness component remained constant. The plot which was rotavated for 14 years then left undisturbed had no A. vulgare at all so had a lower diversity than the sites which had only been rotavated once. At Spurn Head (from 1975 to 1980) there was an initial increase in diversity. During the first 5 years of sand deposition, as in the Breckland, disturbance reduced the density of the dominant species, A. vulgare, to levels more closely comparable to those for the other two species and hence increased the equitability component of diversity. These results thus again show some support for the intermediate disturbance hypothesis in that in the short term, this form of disturbance increases diversity but when more persistent, decreases it, as later prolonged inundation with blown

sand at the coastal site reduced the population of P. muscorum to extremely low levels so that it was not present in samples at all in some years. So as with the prolonged soil disturbance in the Breckland, prolonged disturbance at Spurn again reduced diversity. In both cases, thresholds in disturbance, which exceed the capacity of the system to return to predisturbance levels, appear to be defined more by the duration of disturbance rather than its intensity. As a ‘runner’ [45], P. muscorum has long legs which carry the body well clear of the substrate but which are very poorly adapted to burrowing. Therefore, both obtaining shelter from micro-climatic extremes, and reaching buried foods, would have become increasingly difficult following consecutive sand deposits. A. vulgare, in contrast, as a rolling species [45], which burrows through several centimetres of sand during its annual vertical migrations on this site [12], might be expected to cope with this form of disturbance better. It did maintain populations at levels of above 100 m−2 after 1971, but also declined steeply during the few years after sand started to be deposited on the site, probably as a result of increased mortality directly due to an inability to right itself when overturned in loose sand [11]. The only one of the three species to remain relatively unchanged, and even increase in density following deposition of sand, was P. scaber. This species is a ‘clinger’, with a flattened morphology enabling it to clamp tightly to a solid substrate to reduce water loss [45] and aggregates more strongly than either of the other species which further limits evaporation of moisture from the body [50,56]. It is also the only one of these species regularly to be found on fore dunes and even the strandline of sand dune systems, thus maintaining diversity of the isopod community on this site even when P. muscorum had almost disappeared from it. With respect to disturbance due to rabbit grazing, analysis of neither the spatial nor temporal variation on any of these grasslands supports the ‘intermediate disturbance hypothesis’, as diversity on all three sites was highest when grazing was lowest, intermediate at intermediate grazing levels and lower when grazing was most intense. Reductions in sward length and three dimensional tussock structure due to more intense grazing resulted in changes in the isopod community as described by Hassall [30] with P. muscorum being most abundant in the longest, most tussocky swards. This is possibly because it is morphologically the least well adapted to

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reduce moisture loss in the terrestrial environment [30]. As at Spurn Head, P. scaber was the commonest species on the most exposed sites with the shortest swards, while A. vulgare was able to occupy the widest niche in relation to sward height gradient. The analysis of such a simple community highlights the importance of considering the equitability component in analyses of diversity. Analysis of all the sites shows that if the disturbance affects a dominant species, then the equitability rises and there is a corresponding increase in the diversity index. If, however, the disturbance differentially affects a subdominant species, then the equitability and diversity decrease. There is some evidence to suggest that the importance of the equitability contribution declines with length of time from significant disturbance, whilst the importance of species richness increases. At Lakenheath (the site with the longest period of low disturbance), the fluctuations in the diversity index correspond with the periodic local extinctions of P. scaber. This is supported by Tramer [52] who suggested that in unpredictable environments, diversity predominantly changes through variations in equitability and in more predictable environments, through changes in species richness. Ferreira and Van Aarde [18] also observed this pattern in a similarly species-poor community. Of all the attributes that can define a disturbance event (frequency, extent, intensity and duration) it is the duration that is the least commonly considered [46]. Analysis of all four 20 years time series, however, reveal that it is this attribute that can have the most significant impact on these simple isopod communities. On both Weeting Heath sites the first 5–7 years of high grazing disturbance significantly reduced the isopod diversity. In the following 5 years, however, when the high disturbance persisted, the eventual decrease in the abundance of the dominant sward length generalist (A. vulgare) and a small increase in the abundance of the high disturbance specialist (P. scaber) resulted in an increase in the equitability index. The importance of duration also applies to periods of low disturbance as shown at Lakenheath and in the Weeting Heath exclosure, as the extended period of low disturbance allowed the establishment of the long sward specialist population to rival the dominance of the generalist. In these communities, the persistence of disturbance at given frequencies or level is as important as the temporal alterations themselves. Furthermore, the experiment at Weeting gives some insight into how long it takes for the community to return, after a period of disturbance, to the levels of

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diversity and evenness that apply in the undisturbed condition, as it took 10 years for diversity in the ungrazed exclosure to reach levels comparable with those on the relatively undisturbed site at Lakenheath. This highlights the significant contribution that longterm data sets can make to the study of disturbance and diversity as they provide a dimension that snapshot studies lack. The importance of context for snapshot studies is illustrated by the 1989 study at Weeting Heath. In the comparison of the grazing disturbed sites, the zero grazing site (exclosure) showed the highest diversity. Were this study to have taken place 5 years earlier, the diversity index for this plot would have been less than half its 1989 value. The primacy of duration disturbance complicates the application of the intermediate disturbance hypothesis as, of all the attributes, it is perhaps the hardest to assign the definition of “intermediate”, an inherently subjective term [46]. There are a number of implicit requirements for the “intermediate disturbance hypothesis” to operate, one of these being the presence of competition within the community, such that at times of no or low disturbance competitive exclusion occurs [46]. This small community may not be highly structured by competition as the relative abundance of the three component species are clearly determined by differences in their physiological, morphological and behavioural adaptations to restricting moisture loss, leading to their three different resource utilisation curves along a gradient of rabbit grazing as described by Hassall [30]. The consistent pattern in this community of higher diversity in less disturbed sites is potentially relevant to the management of swards for conservation objectives. In a parallel study of spatial variation of spiders and beetles collected from precisely the same traps at the same times as in this spatial study on Weeting Heath, very similar patterns were found [2] with some species e.g. the spider Lepthyophantes insignis and the carabid beetle Calthus fuscipes, characteristic of short swards while others e.g. several of the orb spiders and the beetle Lycopordina succinta were restricted to longer vegetation. Similarly the diversity of grasshoppers was greater in the less intensively grazed sward at Lakenheath than the heavily grazed sward at Weeting [21] where both abundance [22] and species richness [60] increased inside the exclosure. Although for all these groups of invertebrates, the highest biodiversity occurred in the least disturbed sites, we do not suggest that the sites should be managed by completely removing grazing from the whole

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area, which would create a more uniformly undisturbed sward and would not be compatible with managing plant diversity and sward structure [6,61]. A uniformly ungrazed sward would favour only one set of each taxonomic group, the long sward specialists, at the expense of the short sward specialists. Biodiversity of invertebrates would therefore be favoured by maximising heterogeneity in sward height. This could be relatively easily achieved if rabbits were the primary grazers because most of their foraging is restricted to within a radius of 50 m from their burrow entrances [17] and the position of their main burrows can potentially be manipulated by digging new ones where required [9], while their burrows can be filled and they can be trapped and removed, or temporarily electrically fenced, from areas where a longer sward is required. Such a management recommendation to increase sward heterogeneity for Weeting Heath is not compatible with the current practice of sheep grazing in addition to rabbit grazing. This combination produces a more uniformly short sward designed to improve the suitability of sites for some rare Breckland plant species [14], but is also driven by trying to maximise potential for breeding stone curlews, which require a very short sward for nesting [24,25]. However, a stone curlew’s diet consists largely of soil invertebrates, principally earthworms but with isopods, myriapods and diptera forming up to a third of the total diet for both adults and chicks during late spring and summer, when earthworm availability declines with decreasing soil moisture [25]. Intensive grazing reduces the input of organic material into the litter soil profile and hence the resource base upon which earthworms and other macro-decomposers depend. While increasing the favourability of the site for nesting, current management does not therefore maximise the biomass of these groups of invertebrates, the densities of which increase with sward height [2,10]. Greater spatial heterogeneity of sward height could therefore increase foraging efficiencies of both juvenile and adult stone curlews, potentially resulting in a reduction in the time parent birds have to fly from the site to forage elsewhere, leaving the juveniles more vulnerable to predation. A more heterogeneous sward could also be of benefit to other rare ground feeding birds that occur on these heaths, such as woodlark, which need long swards in which to nest but forage on short ones [4]. It would also retain suitable habitat for some of the rarest invertebrates recorded from the site, including the rarest species encountered in the extensive survey conducted by

Barker and Bowell [2] on the sites used for the spatial analysis on Weeting Heath. This was the beetle L. succinta, a Breckland specialist and ‘red data book 2’ species found in the longest sward where it feeds on fungal fruiting bodies occurring where there is more organic material entering the litter and soil because less is removed by the herbivores. In conclusion, while isopods only form a very small component of the biodiversity on Breckland grass heaths, they do illustrate in microcosm, the importance of considering the systems on appropriate scales of time and space. It is essential to consider diversity at appropriate scales relative not only to the graininess of undisturbed habitats and size of disturbed patches, but also in relation to the mobility of the animals concerned [27, 40]. In this case, if a prime conservation priority is to increase habitat favourability for a flagship bird species, it is important to consider the scale of its daily movements and how best to increase its foraging efficiency, as well as creating more favourable nesting habitat. If both objectives could be achieved simultaneously using, for example, temporary electric fences to vary grazing intensity across the sites, there could be an added advantage for the conservation of greater invertebrate biodiversity. Acknowledgements We are very grateful to Stephen Sutton for initiating and running the sampling programme at Spurn Head, to Keith Sunderland, Bob Davies, Angela Wilkins, Steve Rushton, Mark Dangerfield, Laurie Cartwright, and Jenny Stevenson for assistance with sampling, Jenny Stevenson for processing the extractor samples, Bill Block for introducing us to the sampling sites in the Breckland, Harry Bowell and Mike Barker for help with the spatial survey and for permission to quote their results for other invertebrate groups; the Yorkshire Wildlife Trust, the Norfolk Wildlife Trust and the Elveden Estate for permission to sample from Spurn Head, Weeting Heath, and Lakenheath, respectively; the BES and NWT for financial support, NERC for provision of a research studentship to A.M., Rosie Cullington for secretarial support and Gale and David Curry for assistance in proof reading. References [1]

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