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Utilisation of carrion by Silphidae (Coleoptera) on lowland heathland, England. 2

R. I. M. Guy* 3

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* Corresponding Author: richardimguy@gmail.com 5

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Abstract: 7

1. The aims of this study were a) to identify Silphidae species utilising carrion in heathland habitats, b) to 8

determine if their use of different stages of heathland vegetation (open areas and mature heather 9

specifically) differed and c) to record and analyse the colonisation order of the species observed. 10

2. Heathland research frequently focuses on specialist species restricted to these habitats, while more 11

generalist species are frequently omitted. A gap in the published literature was observed regarding 12

invertebrate communities associated with carrion in heathland habitats and this study aimed to begin to 13

fill that gap by focussing on Silphidae, a group of beetles with many necrophagous species. 14

3. Silphidae were sampled using pit-fall traps at 32 sites baited with carrion (Rabbit carcases) split equally 15

between the two vegetation conditions. Each site was visited 3 times over the course of a 6 day period to 16

observe changes in species assemblage over the course of decomposition. 17

4. 940 Silphidae were found, from 10 species. Overall there was not a significant difference in abundance 18

between vegetation types; on an individual species level a majority of species were shown to be 19

significantly more abundant in heather areas. Heather hosted a more diverse range of species. Significant 20

differences were also observed in species succession of carrion. 21

5. These results fill gaps in Silphidae ecological understanding, especially how habitat features are used. 22

Some of the data may be of use in the field of forensic entomology. Perhaps most importantly portions of 23

Silphidae ecology which are unknown or poorly understood have been identified and suggestions for 24

further study made. 25

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Key Words: Necrophagous Coleoptera, Vegetation structure, Entomofaunal Succession, Heathland, 27

Preferential Habitat Selection. 28

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1. Introduction 29

Lowland Heathland 30

The area of lowland heathland in the UK has declined significantly over the last few centuries (Webb, 31

1989; Rackham, 2003); despite this UK heathland areas represents 20% of remnant European 32

heathland (JNCC, Undated). While a range of heathland types are recognised, lowland heathland is 33

generally considered to be a semi-natural mosaic of sub-climax vegetation stages, historically 34

prevented from succeeding to scrub woodland by human influences such as livestock grazing, peat-35

cutting and fuel wood harvesting (Webb, 1989; Gardner, 1991; Rackham, 2003). Dwindling commercial 36

use for these areas led to habitat degradation and a resulting loss of specialist species diversity 37

(Symes & Day, 2003; Cuesta et al., 2006), with many heathland sites destroyed through conversion to 38

agriculture or commercial forestry plantation (Rackham, 2003; Lin et al., 2007). Remnant areas are 39

often fragmented and isolated and many have deteriorated through lack of appropriate 40

management making these areas conservation priorities (Symes & Day, 2003). Statutory protection 41

has been granted for heathland across Europe and the UK. Five types of lowland heathland are listed 42

in Annex 1 of the European Habitats Directive (1992) and in the UK lowland heath was a BAP priority 43

habitat with 67% of sites designated as Sites of Special Scientific Interest (SSSI) (JNCC, Undated). 44

Current management methods are well established and include conservation grazing, scrub and 45

invasive species removal, rotational heather cutting or burning and turf stripping, among others 46

(Sutherland & Hill, 1995; Symes & Day, 2003). The heterogeneity these methods promote is essential in 47

providing the range of niches and habitat features occupied by heathland specialists (Kirby, 2001; 48

Symes & Day, 2003). Substantial guidance is available from governmental bodies and NGO’s alike on 49

appropriate management of these areas (e.g. Buglife, Undated; JNCC, Undated; Symes & Day, 2003 (RSPB); 50

Anon., 2013 (Buglife)). Projects to restore or recreate favourable conditions on former heathland sites, 51

now degraded or destroyed, are achieved by managing or manipulating soil conditions and 52

vegetation succession (Aerts et al. 1995; Van den Berg et al., 2003; Hawley et al., 2008). 53

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Heathland is sometimes considered a species poor habitat (Gardner, 1991). Webb & Hopkins (1984a) 54

suggest that high invertebrate species diversity indicates habitat deterioration (also Symes & Day, 55

2003). Specialist heathland species - including plant, invertebrate, bird and reptile species - often 56

have restricted distributions or specialist habitat requirements (Kirby, 2001; Symes & Day, 2003). While 57

heathland communities may be lower in species diversity than other habitat specific communities 58

the restricted range and precise requirements of many of these species makes the conservation of 59

their habitat essential (Webb, 1989; Symes & Day, 2003; Lin et al., 2007). 60

Heathland is of particular importance to invertebrates: of 133 BAP priority species found on 61

heathland in the UK, 82 are invertebrates and of these 47 are restricted or very restricted to 62

heathland (Webb et al., 2010). While UK BAP’s were superseded in 2010, the priority species lists are 63

still used to inform devolved conservation priority planning (JNCC, 2014). Kirby (1994) lists 133 Red 64

Data Book species and 210 scarce (notable) species of invertebrates associated with lowland 65

heathland. High quality heathland provides a diverse range of niches catering for an equally diverse 66

range of associated specialist species; many studies into heathland ecology and management focus 67

on the ecology and conservation of these species (e.g. Webb & Hopkins, 1984a; Gardner, 1991; Blake et 68

al., 2003; Dennis, 2003; Schirmel & Buchholz, 2011). While some of these studies appear repetitive they 69

nevertheless provide significant evidence for the importance of heterogeneity in heathland 70

environments (Price, 2003; Schirmel, 2010; Schirmel & Buchholz, 2011). 71

Habitat characteristics which are of significance to heathland invertebrates include: 72

- heterogeneous vegetation structure, 73

- areas of exposed soil (especially sandy soils), 74

- warm micro-climates associated with bare ground or very short swards, 75

- nectar resources from characteristic heathland flora, 76

- complex architectural structure of shrub and scrub species, 77

- soil moisture, 78

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- the gradients between extremes in the above features. 79

(Buglife, Undated; JNCC, Undated; Gardner, 1991; Usher 1992; Kirby, 2001; Symes & Day, 2003; Kirby, 2004; 80

Cuesta et al., 2006; Schirmel & Buchholz, 2011; Anon., 2013). 81

In contrast to upland heather moors, few lowland heathland species rely on heather as a food 82

resource (Kirby, 2001), although many species utilise it to some degree. In heathland settings it is 83

often of greater importance as an architectural feature, particularly to web spinning spiders (Webb & 84

Hopkins, 1984a). The effectiveness of different heathland management techniques, for the 85

conservation of favourable habitat conditions and heathland species, has been widely studied (Usher, 86

1992; Dennis, 2003; Lin et al., 2007; Schirmel, 2010). 87

Many of the above studies are focussed upon the same groups of invertebrates: ground beetles 88

(Carabidae: Coleoptera) and spiders (Araneae) being the most common and frequently studied 89

together (Webb & Hopkins, 1984ab; Gardner, 1991; Blake et al., 2003; Cuesta et al., 2006; Lin et al., 2007; 90

Schirmel & Buchholz, 2011). Aside from the specialist fauna of heathlands, they also provide important 91

resources for generalist species (Kirby, 2001; Symes & Day, 2003). Nectar resources are used by a 92

diverse range of species, especially at times of year when they are restricted elsewhere (Anon., 2013). 93

Some species will disperse onto heathland from surrounding habitats to exploit resources (Webb et 94

al., 1984). High densities of invertebrates, both generalist and specialist, attract predatory species 95

which are found in abundance (Kirby, 2001). 96

These generalist species receive little attention in heathland specific research and management 97

guidance: with such a diverse specialist fauna this prioritisation is understandable. The nature of 98

heathland habitats, with complex mosaics of different vegetation structures, can provide a useful 99

experimental setting in which to study the habits of generalist species. The complex succession of 100

heathland vegetation frequently produces succession gradients: Schirmel & Buchholz (2011) used 101

this graduating vegetation community to their advantage by studying invertebrates in five different 102

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stages of succession on the same site along a succession gradient and demonstrated significantly 103

different invertebrate assemblages in different stages of vegetation. 104

Carrion Beetles (Silphidae) 105

Heathlands have a close association, both historically and currently, with animals both wild and 106

domestic (Rackham, 2001; Dennis, 2003). It is therefore reasonable to hypothesise that heathlands 107

would support invertebrate communities associated with animals, including dung and carrion. 108

Several publications have alluded to the invertebrate communities associated with both carrion and 109

dung in heathlands being ‘rich’ (Kirby, 2001 pg. 77; see also Buglife, Undated) without reference to 110

published research or any description of these communities. Studies into these communities are not 111

readily available, if they have been conducted at all. 112

This research gap provides an opportunity to engage in original research into relatively well-known 113

species in well-known habitats. The chosen group for this study is Silphidae (Coleoptera), commonly 114

known as carrion beetles. Studies into this group most commonly fall into one of two categories: 1) 115

necrophagous (carrion feeding) species in this group are included in forensic entomology research; 116

2) the social behaviour of Nicrophorinae, a sub-family of Silphidae. 117

Necrophagous invertebrates are useful in forensic investigations for determining approximate time 118

of death or minimum post-mortem interval (PMImin) (Byrd & Castner, 2010; Huffman & Wallace, 2012). 119

One primary method for the calculation of this period is entomofaunal succession - the predictable 120

sequence in which different species colonise carrion (Dekeirsschieter et al., 2011b; Huffman & Wallace, 121

2012), this is widely studied for a range of invertebrate groups (e.g. Watson & Carlton, 2003; Watson & 122

Carlton, 2005; Sharanowski et al., 2008). Different species of necrophagous invertebrate specialise in 123

colonising carrion at different stages of the decomposition process: thus through a comparison of 124

observed species assemblages with the behavioural habits of the species found it is possible to 125

determine, in association with other recorded environmental variables, an approximate PMImin 126

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(Kulshretha & Satpathy, 2001; Midgley et al., 2010). In this field Diptera are far more widely studied 127

because they are considered to provide a more accurate estimation of PMImin due to faster 128

colonisation, greater exhibition of niche specialisation and a greater range of species (Huffman & 129

Wallace, 2012), but Coleoptera can provide useful information, particularly in later stages of 130

decomposition (Kulshretha & Satpathy, 2001). Existing studies must be applied with caution however, 131

as geographical, seasonal and environmental variables can all result in significantly different species 132

assemblages and colonisation patterns (Chapman & Sankey, 1955; Grassberger & Frank, 2004; 133

Dekeirsschieter et al., 2011b). 134

These geographical variations are reasonably well understood, but finer scale differences between 135

or within specific habitats are less well studied. Some studies comparing necrophagous Coleoptera 136

communities in different habitats have been conducted, however the habitat parameters are often 137

very broad and poorly defined (e.g. ‘woodland, agricultural and urban areas’ compared by Dekeirsschieter 138

et al. (2011a)). Some studies have been conducted with greater focus on different types of a certain 139

habitat (one example is different types of woodland as studied by Matuszewski et al. (2008)), but literature 140

of this nature in the UK is lacking. The above studies show significant variation in species diversity 141

and abundance. 142

The other common area of Silphidae study is the behavioural ecology of Nicrophorinae (a sub-family 143

within Silphidae often known as ‘Burying beetles’) which exhibit co-operative breeding in the form of 144

bi-parental care for their larvae, a behaviour very rare in Coleoptera species (Dekeirsschieter et al., 145

2011b). 146

While not all Silphidae specialise in carrion feeding, the Nicrophorinae as well as a number of 147

Silphinae species (another subfamily) require carrion to compete their breeding cycle (Dekeirsschieter 148

et al., 2011b; Ray et al., 2014). This association takes two forms: direct carrion feeding and predation of 149

other invertebrates feeding on the carrion. Some species exhibit both these behaviours depending 150

on the stage of the life cycle (Chapman & Sankey, 1955; Dekeirsschieter et al., 2011b). In the UK there are 151

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21 species of Silphidae (Booth, 2012). Of these 16 are known to be associated with carrion: all 7 152

Nicrophorinae and 9 Silphinae (Dekeirsschieter et al., 2011b). 153

Carrion is a rich albeit ephemeral resource and as such many organisms utilise it (Putman, 1983; 154

Wilson & Wilkovich, 2011), although many do so only as opportunists (Moreno-Opo & Margalida, 2013). 155

Seasonality is a significant factor in determining competition for carrion resources: during colder 156

seasons when invertebrates are inactive or less active, and in some geographical regions throughout 157

the year, vertebrate scavengers, primarily mammalian and avian, account for the majority of carrion 158

consumption (by biomass) (Putman, 1983; DeVault et al., 2004; DeVault et al., 2011). In warmer seasons 159

when necrophagous-specialist invertebrate species are active they contribute significantly to the 160

consumption of carrion, effectively competing with vertebrate scavengers (Putman, 1983). Some 161

estimates place invertebrate utilisation of carrion as high as 85% (Ray et al., 2014), with one study 162

(having excluded vertebrate scavengers) recording a 44kg carcase being consumed solely by 163

invertebrate and microbial activity in 3 weeks in a temperate environment (Grassberger & Frank, 164

2004). With this level of potential competition, both inter- and intra-specific, the ability to reduce 165

competitive pressure is an important mechanism (Milne & Milne, 1976; Putman, 1983) and provides 166

Nicrophorinae an important advantage in the utilisation of small vertebrate carcasses. 167

Decomposition of carrion progresses through four stages: Fresh, Bloated, Decay and Dry (Putman, 168

1983; Tantawi et al., 1996), although some consider the Decay stage in two separate stages - Active 169

and Advanced (Matuszewski et al., 2008; Castro et al., 2013), and count five stages overall. The onset of 170

these stages is affected by a huge range of environmental, climatic, faunal and bio-chemical factors 171

and as such is not consistent (Chapman & Sankey, 1955; Putman, 1983; Tantawi et al., 1996). Different 172

invertebrate species specialise in utilising carrion at different stages of the process which leads to 173

the observed entomofaunal succession described previously (Dekeirsschieter et al., 2011b). The two 174

subfamilies utilise carrion resources slightly differently, this will be discussed in detail in the context 175

of the study results. 176

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Research Aims 177

The overall purpose of this study was to begin to describe a species groups (Silphidae) use of a 178

specialist resource (carrion) in a specific habitat (lowland heathland). With no previous work in this 179

area it is hoped that the findings of this study may act as a base point for further study into Silphidae 180

in a range of habitats to fill the research gaps into their ecology identified above. 181

The aims of this specific research project were: 182

1. Record Silphidae species which are present and their abundance. 183

2. Compare how Silphidae use areas of bare ground and mature heather. 184

3. Record the sequence of entomofaunal succession. 185

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2. Materials and Methods 186

Study Site 187

The study was conducted on 90 hectares of SSSI designated heathland (Site of Special Scientific Interest 188

- Sutton & Hollesley Heaths; study site comprising blocks 11 & 12) located within the Suffolk Coast and 189

Heaths Area of Outstanding Natural Beauty (AONB), England (52.074’N, 1.388’E). The area is 190

representative of lowland dry heath (as described by Symes & Day (2003)), with acidic, sandy soil and 191

vegetation dominated by Calluna vulgaris, although unusually lacking in significant quantities of Ulex 192

europeaus (pers. comm.: B. Calversbert). The site is managed as a nature reserve with conservation 193

grazing by sheep and ponies alongside periodic heather cutting and bracken and scrub control 194

operations (pers. comm.: B. Calversbert). Natural grazing by Rabbit Oryctolagus cuniculus, and Fallow 195

Deer Dama dama and Muntjac Muntiacus reevesii (although only rabbits are present in high density) 196

is deemed beneficial in maintaining the desired complex mosaic of vegetation structure across the 197

site. 198

Open areas and areas dominated by mature heather were 199

chosen as two stages of heathland vegetation succession to 200

allow comparison for the research aims to be achieved (see 201

Box 2.1). Within the study area suitable sites (n = 32; see Fig 202

2.1) were identified using a combination of remote sensing 203

(satellite imagery: Google Maps) and site visits to ground truth 204

the satellite imagery (as a result of natural succession and 205

habitat management work the distribution of different 206

vegetation structures varies from year to year; satellite imagery was 2 years old so site visits were 207

essential). 208

Due to the nature of the site, placement of samples presented a problem. The site is used 209

extensively by recreational visitors as a result of open access rights, with dog walkers especially 210

Box 2.1 - Vegetation Type Description

Mature Heather - Vegetation dominated

by mature heather plants to a minimum

height of 25cm.

Bait point placement criteria:

≥ 80% ground cover mature heather with

height ≥ 25cm within 3m of bait point.

Open Ground - Bare soil or very short

sward height (≤5cm). Maintained through

grazing and / or management work.

Bait point placement criteria:

≥ 80% bare ground or close cropped sward

(≤ 5cm) within 3m of bait point.

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Fig 2.1 - Study site and

individual bait point sites

common. It was decided that bait points would not be sited within obvious view of the paths to 211

reduce the risk of disturbance by members of the public and dogs. Bracken dominated the 212

vegetation in large areas of the site, further restricting where bait points could be located. Further, 213

due to the research aim to compare specific stages of heathland vegetation, large areas of the site 214

did not meet the required conditions (see Box 2.1). This precluded truly random site location. In an 215

attempt to gather representative data without ‘cherry picking’ sites, areas which met the two 216

vegetation conditions were identified and the total suitable area divided into 18 sites (two of which 217

remained unused due to bait shortages). Within open areas, traps were located by roughly dividing 218

the block into an approximate 10 x 10 grid with the bait site being placed in a randomly selected grid 219

square. In mature heather areas the exact location of each bait point was physically limited to a 220

point where the bait and exclusion cage could be installed (this usually required a space between 221

heather plants). Due to the psuedoreplication exhibited by these site selection methods (Hurlbert, 222

1984), care must be taken in applying the results of this analysis to other sites. 223

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Carcase

Fig 2.2 - Pitfall trap arrangement, and

example of a bait point among heather

prior to the addition of a rabbit carcase.

Data Collection Methodology 224

Data collection was achieved using carrion bait (Rabbit 225

carcases: sourced from local pest control operation) with 226

pitfall traps. Bait was enclosed within wire exclusion cages 227

(460 x 330 x 200mm) to prevent disturbance by vertebrate 228

scavengers (Chick, 2008; Dekeirsschieter et al., 2011a). Mesh 229

size was approx. 30mm; the largest target species 230

maximum size is approx. 35mm length (Nicrophorus 231

humator), as such this mesh size should not have excluded 232

any target species from entering (Dekeirsschieter et al., 233

2011b). Four pitfall traps (plastic cups: approx. 50mm 234

diameter, 80mm deep) per bait point were located inside 235

the exclusion cage. Traps were orientated around the carcase with one each at the head and tail 236

ends, above the back and beneath the belly (see Fig 2.2) (based on Dekeirsschieter et al., 2011a). Each 237

bait point was checked, samples removed and traps refilled if necessary three times at 48 hr 238

intervals (+/- 2 hr) from initial placement of each carcase with the final check 6 days after initial 239

placement. Pilot studies showed that this time interval allowed most carcases to decompose to the 240

final ‘dry’ stage of decomposition (Tantawi et al., 1996). Putman (1983) showed that Silphidae were 241

most common during the ‘bloated’ and ‘decay’ stages with none found during the dry stage so this 242

was considered sufficient time for the purposes of this study. Due to the short interval between trap 243

checks no killing agent was used; traps contained water and a few drops of detergent only. The 244

content of all four traps at each bait point was considered as a single sample. Identification of 245

samples was achieved using a number of keys (Hackston, 2009; Wright, 2009ab, Hackston, 2012). 246

Due to the size of the species being dealt with no specialist equipment was required for 247

identification, with only a hand lenses being used to confirm diagnostic features in the smaller 248

species. 249

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Data collection was undertaken over a three week period in August 2014. For the first two weeks 250

twelve bait points were run simultaneously - six per vegetation type; for the final week eight bait 251

points were used - four for each vegetation type totalling 32 total sample sites, 16 of each veg type 252

(see Fig 2.1). This reduced third week was a result of problems sourcing carrion bait. This gave a total 253

of 96 collection events across the study period. 254

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3. Results 255

In total 940 Silphidae were found from ten species and six genera, representing 46% of British 256

Silphidae species (21 total - Booth, 2012). Sixteen species of Silphidae found in Britain are associated 257

with carrion (Dekeirsschieter et al., 2011b) of which nine (56%) were found; in addition one species not 258

specialising in carrion was also found - Silpha atrata. Of this total, 61% (577) were found in the 259

mature heather sites compared to 39% (363) in open sites. Individual species presence ranged from 260

34-100% (Heather) and 0-66% (Open) at species level. Only two species (Nicrophorus humator and 261

Thanatophilus sinuatus) were more abundant in open areas. Abundance of individual species ranged 262

from 2 to over 300 (see Table 3.1). Larval stages of Silphidae species were also counted, although 263

neither identification to species level or aging was attempted. In total 209 larvae were found, with 264

all but 2 (< 1%) found in heather areas. 265

The results of analysis using the independent samples t - test to determine the significance of these 266

data, collectively and individually, are shown in Table 3.2. Levene’s test for equality of variances was 267

employed to determine if equal variance could be assumed for each data set. Kolmogorov-Smirnov’s 268

test for normality showed that only the species abundance data (total number of species found at 269

each site) could be considered to be normally distributed (D(32) = 0.147, p = 0.76), with other data 270

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sets exhibiting pronounced positive skew and kurtosis. To avoid problems caused by violations of the 271

assumption of normality bootstrapping was used on all other data (using IBM SPSS Statistics v.22) to 272

ensure obtained results could be considered robust (Field, 2009). The size of the effect vegetation 273

type had on all variables was then calculated as a Pearson’s correlation co-efficient (r). 274

Despite a large disparity, the observed difference in abundance between vegetation types was not 275

significant (t(30) = 1.43, p = 0.162) and had only a small effect upon observed differences (r = 0.25). 276

Table 3.2 - Results of Independent samples t - test comparing vegetation types means

Table 3.3 - Total abundance over time

Table 3.4 - Species abundance over time

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Observed distributions for both larval abundance (t(15.011) = 2.88, p = 0.011) and species richness 277

(t(30) = 3.42, p = 0.002) were significant with a far greater measurable effect (r = 0.6 and 0.53 278

respectively). 279

Considered individually five species distributions were significantly different between vegetation 280

conditions (see Table 3.2). The distribution of the two species observed in greater numbers at open 281

sites was not significantly different (p = 0.162 and 0.141), with a correspondingly lower effect (r = 282

0.25 and 0.30). Three species sample sizes were too small for meaningful analysis, however two of 283

these species, Oiceoptoma thoracicum and Nicrophorus interruptus, were only found in heather sites 284

(see Table 3.1). Due to the number of separate tests performed in this analysis there is an 285

unavoidable risk of Type 1 statistical errors being present. 286

When data are considered over time (see Table 3.3) the majority of colonisation was observed at later 287

site visits corresponding with mid stages of decomposition; only 14% (Heather) and 8% (Open) 288

collected during the first visit (approx. 48 hrs after placement). While open ground collections show 289

Table 3.5 - Results of two-way repeated measures ANOVA

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consistent colonisation rates at the later collection events (Visit 2 & 3: 46% each) heather areas are 290

less consistent, showing a peak at the second observation (Visit 2: 53%; Visit 3: 33%). By assessing this 291

at species level much greater variability is observed, consistent with different preferences exhibited 292

by different species (Dekeirsschieter et al., 2011b). These data were analysed using two-way repeated 293

measure ANOVA (results in Table 3.5) to test the effect of vegetation conditions and time (related to 294

the stage of decomposition), and interaction between variables. This test assumes that the data 295

exhibits sphericity which is tested using Mauchlys test; requiring a correction if conditions of 296

sphericity are not met (Field, 2009). 297

This test was used to analyse total abundance (adults & larva) and six of the ten observed species. 298

Species with a small sample size (total abundance of < 20 from 96 collection events) were excluded. 299

As a test of variation between vegetation types, this analysis mirrored the earlier t-test results, 300

supporting the robustness of these tests. When comparing how observed abundance changed over 301

time, the results showed that both adult and larval abundance differed significantly (F(2, 30) = 13.58, 302

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p = 0.000 & F(2, 30) = 9.13, p = 0.001 respectively). Of the six species tested five showed significant 303

variation over time (Fig 3.1). Nicrophorus vespilloides (Visit 1: 32%, Visit 2: 45%, Visit 3: 23%) abundance 304

did not vary significantly (F(2, 30) = 1.43, p = 0.256). 305

Only larval abundance and Nicrophorus investigator showed a significance variation in the 306

interaction between the two variables (F(2, 30) = 9.18, p = 0.001 and F(2, 30) = 7.33, p = 0.003 307

respectively). Fig 3.2 shows the difference in species colonisations between vegetation conditions. 308

Fig 3.2 - Species colonisation rates; comparison between habitats

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Environmental variables were recorded for each site at each visit to allow comparison. These 309

variables were then compared using independent samples t-tests (see Table 3.6). Of the three 310

variables recorded, only Soil Temperature showed a significant difference between vegetation types 311

(F(1, 94) = -1.917, p = 0.000), with open habitats being significantly warmer than heather areas (21.0 312

OC (± 0.49) open; 19.1 OC (± 0.56) heather sites). It is recognised however, that other measurable 313

environmental and micro-climatic variables will affect invertebrate occupation of these areas, and 314

that these offer only a narrow perspective of differences between these areas. 315

Appendix I contains distribution maps of eight of the observed species; these show abundance of 316

species collected at each sampling site. (Necrodes littoralis and Nicrophorus interruptus distributions were 317

not mapped due to the small samples sizes of 2 and 3 respectively). 318

Tested Variables Levenes test result

Equal Var.

Assumed? Mean diff

Confidence Interval

(Bca 95%) Result

Significant

@ 95%?

Effect size

(r) *

Air Temperature F(1, 94) = 3.85, p = 0.053 Y 0.7604 -0.533, 2.085 t (94) = 1.10, p = 0.274 N 0.11

Soi l Temperature F(1, 94) = 0.11, p = 0.742 Y -1.917 -2.918, -0.930 t (94) = -3.86, p = 0.000 Y 0.37

Humidity F(1, 94) = 1.48, p = 0.226 Y -0.7584 -6.092, 4.187 t (94) = -0.304, p = 0.762 N 0.03

Table 3.6 - Results of independent samples t - test comparing measured environmental variables between vegetation types

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4. Discussion 319

Silphidae on heathland 320

The specific topic of this study has, so far as the author is aware, no precedent. This prevents critical 321

comparison with other directly comparable studies; however both heathland invertebrates and 322

Silphidae have been studied in sufficient detail to provide some context for the discussion of these 323

results. As such many points raised by this study may go unanswered, instead being a suggestion for 324

further study. 325

The results of the primary research aim - to record species presence and abundance - show that a 326

large proportion of necrophagous British Silphidae (56%) will utilise carrion in heathland areas. 327

Previous records exist for seven of the ten observed species in the 10km grid square in which the 328

study area falls (UK Grid Square TM34). Of particular note is the observation of Nicrophorus 329

interruptus, a ‘Nationally Notable B’ species not previously recorded in this grid square although 330

records exist in adjacent squares, of which three were found. Neither Thanatophilus sinuatus (334 331

found) nor Silpha tristis (91 found) had previously been recorded in this grid square, although 332

records did exist for one or more adjacent grid squares (NBN, Undated). It should be noted that one 333

necrophagous Silphidae species found in Britain, Thanatophilus dispar, is inactive at the time of year 334

the study was conducted (Active: May - July) (Dekeirsschieter et al., 2011b) and therefore may be 335

missed in this study, even if it were present on site. However, it is a rare species (Dekeirsschieter et al., 336

2011b) with no records within 100 miles of the study site (NBN, Undated) (for an assessment of 337

species overall abundance see Table 4.1). 338

Dekeirsschieter et al. (2011b) in reviewing Silphidae in Western Europe suggested habitat 339

preferences for species found in that geographic range (see Table 4.1) (also Martin-Vega & Baz, 2012). 340

The habitats described in this table are not further defined and are therefore difficult to use in great 341

detail. It can reasonably be assumed that heathland habitat, or elements thereof constitute an open 342

habitat; ‘field’ habitats conditions may be met by the areas of acid grassland on site; forest 343

20

conditions may be met by the small areas of semi-mature and mature trees on site, however these 344

are small areas. These assumptions may not fully explain the presence of these species. Some 345

possible explanations are discussed here. 346

Webb (1989) found that the vegetation communities and structure in habitats surrounding 347

heathland areas affects the diversity of invertebrates found there. In Webb’s study the diversity of 348

heathland invertebrates increased (a sign of habitat degradation through loss of specialist 349

communities (Webb & Hopkins, 1984a)) as a result of different habitats bordering heathland areas. 350

This effect was particularly noticeable in areas where heathlands were fragmented and interspersed 351

by modified or intensively managed habitats. The study site is a relatively small area of the 352

heathland in the region: even the full SSSI area of 461 hectares represents only a portion of the total 353

remnant heathland in the ‘Sandlings’ area (SSSI Citation, Sutton & Hollesley Heaths), although much of 354

what does remain is in poor condition. Formerly a much larger tract of heathland, significant 355

portions have been converted to commercial forestry, arable agriculture or commercial 356

development, or allowed to succeed to woodland habitats. Habitats adjacent to the study site 357

include deciduous woodland, coniferous plantation, arable agriculture, a road and unsurfaced tracks 358

and associated verges and other areas of heathland, with different management strategies. With 359

this range of bordering habitats, species not normally found in heathland habitats may use the study 360

site as additional, albeit marginal habitat, especially when there is a specific resource, in this case 361

carrion, available (Webb & Hopkins, 1984a). 362

Lin et al. (2007) found in a study of commercial forestry planted on former heathland in East Anglia 363

that a range of open forest habitats providing refuges suitable for overlapping Carabidae 364

(Coleoptera) communities associated with both closed canopy forest and heathland. If the reverse 365

could also be applied, that heathland provides some suitable habitat for species normally associated 366

with open forest areas, then the presence of those Silphidae deemed to be forest species by 367

21

Dekeirsschieter et al. (2011b) may be using small patches of suitable habitat or marginal habitats on 368

heathland, particularly those areas bordered by or interspersed with forest. 369

Milne & Milne (1976) using mark-release-recapture studies showed that some species of Silphidae 370

can detect and disperse to find carrion resources from as far as 4km. This is achieved through 371

detection of volatile organic compounds (VOC’s), including organosulphates, given off during the 372

decay process (Kalinova et al., 2009; Podskalsa et al., 2009; Forbes, 2014). These are detected by sensitive 373

olfactory glands in the beetle’s antennae (Milne & Milne, 1976). If beetles were drawn from this order 374

of distance to the bait on the study site then species occupying a wide range of habitats may be 375

present. This study has no way of determining distance travelled by individuals to exploit this 376

resource, and therefore it cannot be concluded how inter-habitat dispersal has influenced the 377

observed communities, but it should be borne in mind as a possible influencing factor. 378

There is opportunity for substantial additional study into this area of Silphidae ecology. Further study 379

into habitat occupation and preference could clarify understanding into what habitat features are of 380

greatest import. From the view point of forensic science, which is the motive for a large portion of 381

the study into Silphidae ecology, additional understanding into habitat occupation may be beneficial. 382

Aside from the calculation of PMImin, carrion entomofauna carrion can be beneficial in determining 383

whether a body has been relocated after death (Matuszewski et al., 2013). The presence on a carcase 384

of either larva or adults of species not found in a certain habitat may indicate that a body has been 385

relocated, but an in depth and consistent understanding of species habitat preferences is needed for 386

this to be reliable (Huffman & Wallace, 2012). 387

Variation between vegetation conditions 388

The secondary aim of research was to determine if differences in observed species use of habitat 389

features were significant, specifically areas of mature heather and open areas (see Box 2.1). The 390

results (see Table 3.2) show that significant differences were observed in most of the tested data. All 391

species exhibiting significant variation showed a preference (implied through higher abundance) for 392

22

heather areas over bare ground. Further, of the three species not tested due to insufficient sample 393

size, two were only found in heather areas, suggesting a preference, although untestable with these 394

data. No data shows this more clearly than the collection of Silphidae larva - of 209 collected all but 395

2 were from mature heather sites. 396

Pearson’s correlation co-efficient values for all data which exhibited significance was only less than r 397

= 0.5 (threshold for a large effect - Field, 2009) for one data set, that of Thanatophilus sinuatus (r = 398

0.48) (range: r = 0.52 - 0.60; see Table 3.2). This indicates that the difference in vegetation had a large 399

statistical effect on distribution. 400

Few studies have been published in regard to Silphidae habitat preferences at these small scales, 401

although some are mentioned in studies covering a range of arthropod species, therefore any 402

attempted discussion of causal factors for these habitat preferences by necessity must draw upon 403

non-species specific studies as a back ground. Significant differences in invertebrate communities 404

found in different vegetation structures are widely recorded (e.g. Gardner, 1991; De Bruyn et al., 2001; 405

Blake et al., 2003; Dennis, 2003; Cuesta et al., 2006; Schirmel & Buchholz, 2011; Martin-Vega & Baz, 2012). 406

There are a wide range of factors, unrecorded mostly in the restrictions of this study, which may 407

explain this disparity. Micro-climatic conditions (including but not limited to humidity, temperature 408

and shelter) are widely understood to dictate occupation and use of different habitats by 409

invertebrates even at very small scales (Thomas et al., 1999; Gillingham, 2010; Schirmel et al., 2011), but 410

there are other factors such as vegetation structure and species; presence of prey species; soil types, 411

content and moisture; aspect; elevation and bordering habitats which also play a role (De Jong & 412

Chadwick, 1999; Kirby, 2001). Only one of the three environmental variables measured (Soil 413

Temperature) showed a significant difference between vegetation conditions. 414

23

Silphidae habitat use 415

In light of these results a review of what is understood of Silphidae ecology, and to some extent, the 416

habits of other necrophagous species would be beneficial. Within the group Silphidae two 417

subfamilies, Nicrophorinae and Silphinae, exhibit different strategies for breeding and resource 418

selection (Dekeirsschieter et al., 2011b). In addition both habitat and food resource selection has been 419

shown to differ even within species depending on the level of reproductive maturity of individuals 420

(Lowe & Lauff, 2012). 421

Nicrophorinae: Also known as ‘Burying beetles’, this group are unusual in their breeding strategy. 422

Small vertebrate carcases are buried or covered with soil or organic litter, to a greater or lesser 423

depth dependant on species, to protect the resource from competition. This is done co-operatively 424

with a breeding pair often working together to achieve this. When interred the carcase is 425

manipulated, both physically and chemically, to provide optimum conditions for the development 426

and feeding of larvae (Milne & Milne 1976; Cooter & Barclay, 2006; Dekeirsschieter et al., 2011b). Soil 427

conditions suitable for burial are therefore a key determinant of Nicrophorinae presence (Scott, 428

1998). 429

Due to the described behaviour sexually mature Nicrophorinae show a marked preference for 430

smaller carcases which can be buried more easily (Matuszewski et al., 2008; Lowe & Luaff, 2012); both 431

Dekeirsschieter et al. (2011b) and Wilhelm et al. (2001) suggest that carcases smaller than 100g are 432

most favoured, although burial of carcases up to 300g have been observed. Scott (1998) does record 433

anecdotal evidence of larger carcases, including Rabbits as used in this study, being used by several 434

pairs of Nicrophorinae for breeding in the absence of more suitable resources. Typically however, 435

Nicrophorinae found on larger carcases (> 300g) tend to be sexually immature, or mature but 436

subordinate non-breeding individuals. Their presence is likely for their own food requirements, 437

either by feeding directly on the carrion or through predation of other species, especially Diptera 438

larva. Immature individuals occupying larger carcases are therefore less likely to conform to habitat 439

24

preferences because breeding efficiency is not a consideration in resource selection (Putman, 1983; 440

Dekeirsschieter et al., 2011b; Lowe & Luaff, 2012). 441

Without recording the sex or determining the sexual maturity of individuals in this study it cannot be 442

accurately determined whether these patterns were demonstrated, but it may allow the reasonable 443

assumption that a large number of Nicrophorinae species found in this study were sexually 444

immature. Supporting this assumption; carcases used were all well in excess of 300g (approx. 750 - 445

1500g), and no visual evidence of attempts to bury the carcase was observed. The highest number of 446

Nicrophorinae individuals found on a single carcase in a single visit was 61, from all 5 species: a 447

group of species which aim to limit competition, both intra and inter-specific, when seeking 448

reproductive habitats and resources, are unlikely to be found in these numbers when attempting to 449

breed. 450

Wilhelm et al. (2001) state that smaller Nicrophorinae favour damp soil conditions were burial is 451

more easily achieved and are therefore found more frequently in closed conditions such as 452

woodland; in contrast larger species tend to favour open habitats. In this study, the largest 453

Nicrophorinae species found, Nicrophorus humator, was also the only species not to show a 454

significant preference for heather areas (for species size ranges see Table 4.1). This potentially 455

supports the above statements. Heather dominated areas are a more closed habitat and with 456

greater moisture holding potential due to higher proportions of organic matter than present in bare 457

soil or very short grass sward areas (Gupta & Larson, 1979). However, this should be considered 458

tentatively: soil moisture was not recorded so this assumption cannot be considered conclusive. 459

Also, with the assumption that most individuals observed were sexually immature, preferentially 460

selection of habitat conditions may not have been a causal factor in the significance of these 461

distributional differences. 462

Wilhelm et al. (2001) also indicated that soil temperature affected larval development, with warmer 463

temperatures coinciding with faster larval development rates than in cooler conditions. They 464

25

concluded that this may lead to preferential habitat selection for warm soil conditions. The observed 465

results of this study, in so far as they can be applied, contradict these findings: Nicrophorinae 466

species, with the exception of N. humator were all significantly more abundant in mature heather 467

environments, which showed a significantly lower soil temperature. 468

To more accurately assess the above points, further study could be undertaken, where the sexual 469

maturity of individuals was identified to allow mature and immature individuals to be considered as 470

separate populations. 471

One feature of the soil conditions which is not made mention of in any relevant literature is the 472

presence of root networks and the effect of these on the ability of Nicrophorinae to effectively bury 473

carrion. The areas of mature heather exhibited often dense root networks. These were not 474

measured or recorded during the study, but did present a challenge in placing pitfall traps. Data 475

from this study cannot determine any conclusion to this informal hypothesis, but it again identifies 476

unanswered questions in this field of study. 477

Silphinae: In contrast to Nicrophorinae species, Silphinae do not bury carrion. This dictates a 478

significantly different, almost opposite, association with the resource. Larger carcases (> 300g) are 479

favoured by sexually mature individuals (Wilhelm et al., 2001; Martin-Vega & Baz, 2010). Silphinae eggs 480

are laid in the soil near to carcases allowing larva when hatched to colonise and utilise the food 481

resource, with no parental care (Dekeirsschieter et al., 2011b). Immature species meanwhile will utilise 482

a wider range of carcase sizes, including much smaller carcases than would be used as a site for 483

oviposition (Dekeirsschieter et al., 2011b).This implies that sexually mature individuals of the two 484

groups will not be in direct competition with each other for breeding resources, but that immature 485

individuals of the different subfamilies may compete for resources. Niche separation may be 486

achieved through a preference for different stages of decomposition (Dekeirsschieter et al., 2011b). 487

Without the need to bury carrion soil conditions are largely removed as significant feature, although 488

26

soil temperature may again affect early development as eggs are deposited into the soil - this is not 489

discussed in published literature. 490

Based on illustrations and descriptions in Cooter & Barclay (2006) and Dekeirsschieter et al. (2011b) 491

it is believed that all larvae found were Silphinae species although formal identification was not 492

attempted. Nicrophorus species are morphologically distinct and their typical breeding habit would 493

make it unusual to find these larvae feeding out in the open. 494

One interesting note is that in this study larvae were observed on carcases as early as 2 days after 495

carcase placement. Dekeirsschieter et al. (2011b) state that eggs hatch in 4 - 5 days. Even 496

discounting the time period needed for adults to colonise a carcase site and oviposit, this does not 497

allow sufficient time for egg development and hatching (far higher larval abundance was observed at 498

later collections: Visit 1: 38; Visit 2: 105; Visit 3: 66). This shows that larvae, as well as adults, must be 499

dispersing to the resource from the surrounding area: without flight it is certain that the dispersal 500

capability of these larvae is less than adults of the species, but no studies can be found suggesting 501

what dispersal distances are possible for larva. Instar number was not determined, nor were larvae 502

measured, but the range of sizes (approx. from <5mm to >25mm) suggested a range of instars from 503

across the developmental spectrum were present throughout the study. 504

This identifies another area of research of potential interest to forensic investigation: Silphinae are 505

of greater use than Nicrophorinae in forensic investigations because of their preference for larger 506

carcases (Dekeirsschieter et al., 2011b). However, if their larvae are used in this context then 507

understanding the dispersal abilities of these larvae could be a significant factor in accurately 508

determining PMImin. Lewis & Benbow (2011) have shown that a lack of understanding of dispersal 509

habits and capabilities in Diptera larva may have led to misinterpretation of forensic evidence 510

previously. It is believed that this could be an additional area where lack of published research may 511

lead to misinterpretation. 512

27

Matuszewski et al. (2013) conducted a study of necrophagous invertebrates across a gradient of 513

habitats from open areas to forest. Three Silphinae species also found in this study were observed: 514

Necrodes littoralis and Thanatophilus sinuatus were found across the range of habitats as in this 515

study. The final species, Oiceoptoma thoracicum, was considered to be a forest specialist, and 516

avoided breeding in open areas. In the current study O. thoracicum was observed only in heather 517

habitats, although in very low abundance, supporting to a degree the study in that they favoured 518

more closed vegetation conditions. However, at a landscape scale, heathland areas generally would 519

be classified as open. The above study used the findings to state that O. thoracicum found on a 520

carcase in open areas would be a sign of carcase relocation, but the findings of this study contradict 521

that at a wider habitat scale. This demonstrates the need for clarity in defining habitats in studies 522

such as these. 523

Entomofaunal Succession 524

The final research aim was to observe the colonisation patterns of the observed species or 525

entomofaunal succession. Fig 3.1 shows that differences were observed between species 526

colonisation rates; Fig 3.2 allows the colonisation rates to be compared between habitats showing 527

some differences although only Nicrophorus investigator demonstrated a significant interaction 528

between habitat and time; Table 3.5 shows which data exhibited significant differences over time. 529

Unfortunately the meaningful analysis of this data is limited due to the variance displayed in 530

decomposition rate. Entomofaunal succession is dictated not by time since death but stage of 531

decomposition which is dictated by biotic, abiotic and seasonal variables (Wilhelm et al., 2001; 532

Matuszewski et al., 2010). The scale of this variation was poorly understood to the author prior to data 533

collection and so no provision was made for recording the stage of decomposition. This has 534

compromised the usefulness of these data. 535

The two sub-families again exhibit behavioural differences and contrasting preferences between 536

stages of decomposition in which they colonise a carcase. Adults of both sub-families will occupy a 537

28

carcase to feed themselves; either directly from the carrion or by predating the other invertebrates 538

found there or to use carrion as a resource for reproduction (Chapman & Sankey, 1955; Putman, 1983). 539

Immature individuals seeking to feed themselves are less restricted to prime conditions so will 540

occupy carrion at a wider range of stages of decomposition than sexually mature individuals whose 541

focus is reproduction (Matuszewski et al., 2008). 542

Sexually mature Nicrophorinae species, as a result of their reproductive habit will colonise small 543

carcases early in the decomposition stage to prevent competition when the carcase is interred 544

(Dekeirsschieter et al., 2011b). All Nicrophorinae species (except N. interruptus with a total sample size 545

of 3) were found at the first visit just two days after placement and then throughout the study. The 546

carcases used in this study were larger than is preferentially chosen and so the colonisation habits of 547

these species cannot be accurately tested fully in this setting, although the results do seem to 548

support this behaviour. 549

In contrast, Silphinae species are more associated with mid stages of decomposition: bloated and 550

decay (Putman, 1983; Dekeirsschieter et al., 2011b). In this study Silphinae were found across the time 551

spectrum, although, because this cannot be reliably linked with a stage of decomposition, it cannot 552

be definitively stated whether or not this matches a specific stage of decomposition. 553

Different decomposition rates are the result of a variety of factors including the colonisation by 554

different invertebrates, especially Diptera (Putman, 1983; Matuszewski et al., 2008). The presence of 555

Diptera larvae and in some cases the larvae of other necrophagous species including Silphinae 556

species has a significant impact on the rate at which decomposition progresses (De Bruyn et al., 2001; 557

Matuszewski et al., 2010). Matuszewski et al. (2010) showed that decomposition progresses fastest in 558

more humid habitats, largely as a result of the increased Diptera colonisation. Therefore the 559

colonisation of carrion by Silphidae is also affected by the wider necrophagous invertebrate 560

community. 561

29

A diverse range of factors affect the behaviour of Silphidae in any habitat they occupy. This study has 562

attempted to test and expand current knowledge on a few of these factors in a habitat in which they 563

as a group are poorly studied. The gap in ecological understanding that was identified was far too 564

large for a single study to attempt to address; hence the aim of this study was largely to use a 565

research opportunity to identify additional research which could be undertaken to fill this gap. Some 566

further opportunities for study have been identified in the course of comparing the results of this 567

study with previously published work. 568

30

Acknowledgements 569

I would like to thank and acknowledge the assistance of: Dr P. Mitchell at all stages of project 570

planning, execution and write up; B. Calversbert on behalf of Suffolk Wildlife Trust, for allowing me 571

to undertake this research project at Sutton Heath Nature Reserve, Suffolk; P. Shires from Stoke-on-572

Trent City Council, for allowing me to undertake pilot studies at Park Hall Country Park; finally my 573

family, especially my wife, for numerous acts of support and assistance throughout this project and 574

all other study I have undertaken. 575

31

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Appendix I - Species Distribution and Abundance Maps 726

Appendix I: Species Distribution & Abundance Maps

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