¹Department of Zoology, University of Oxford, Oxford, UK

²Forest Research, Northern Research Station, Roslin, UK

³Department of Agricultural Sciences, University of Helsinki, Helsinki, Finland

⁴School of Biological Sciences, University of Edinburgh, Edinburgh, UK

Email: moya.burns@zoo.ox.ac.uk

Copyright © 2014 Moya L. Burns et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. In accordance of the Creative Commons Attribution License all Copyrights © 2014 are reserved for SCIRP and the owner of the intellectual property Moya L. Burns et al. All Copyright © 2014 are guarded by law and by SCIRP as a guardian.

Restoring deadwood habitat is vital in order to recreate fully functioning forest ecosystems. Letting this process occur naturally can take in excess of one hundred years, thus management practises typically try to accelerate this via the artificial addition of deadwood. Since the species which rely on deadwood often have poor dispersal abilities, restoring deadwood habitat rarely results in the full restoration of the sa- proxylic fauna. Furthermore, standard deadwood monitoring protocol only records the amount and type of substrate available and is not capable of determining whether saproxylic insects have been restored. Full species inventories are time-consuming, costly and require great expertise. We present a rapid biodiversi- ty assessment tool which we believe is the first protocol for measuring saproxylic activity which is ac- cessible to non-specialists. Utilising the exit bore holes which saproxylics create on deadwood can pro- vide an indication of the density, richness and diversity of species present; we call this the Saproxylic Ac- tivity Index. We show that this index can detect differences in the activity of insects between substrates. As saproxylic insects provide important ecosystem functions, such as aiding in the decay of deadwood and recycling nutrients, a measure of their activity levels may indicate the rate of restoration of these ecosystem processes. We believe that further exploration of this method provides an exciting opportunity for the functional restoration of saproxylic fauna to become incorporated into mainstream forest management.

Keywords: Citizen Science; Temperate Forest; Beetles; Bioindicators; Volunteers; Coleoptera; Biodiversity; Surveys

Introduction

Saproxylic insects, those which depend on deadwood or the fungi and microorganisms associated with it (Speight, 1989), are among the most endangered forest species worldwide (Grove & Stork 1999; Horak et al., 2012). In Europe, natural forest cover has been reduced to a tiny proportion of its original post-glacial area due to the proliferation of agriculture and urbanisation (Peterken, 1996). In addition, the amount of deadwood in remaining forests has been dramatically reduced due to thousands of years of human use of wood for timber and fuel and in more recent times, forest management practises which remove deadwood for safety and aesthetic reasons (Hagan & Grove 1999). These factors combined mean that the saproxylic fauna of Europe is being lost at an alarming rate (Wallenius et al., 2010). It is assumed that similar processes are occurring to reduce the saproxylic fauna worldwide, though sufficient data and long-term records are lacking (Grove, 2002).

As saproxylic species have been shown to account for any- where between 20% to 56% of all forest-dwelling species (Grove, 2002) the establishment of deadwood habitats during forest restoration is vital in order to restore biodiversity

(Humphrey, 2005). The success of forest restoration treatments often have to be assessed using rapid biodiversity surveys due to limitations on time and funds (Abate, 1992). However, de- spite their threatened nature, saproxylic insects, along with most other invertebrates, are rarely included in these assess- ments (Kim, 1993). This is in part due to the difficulty of sur- veying the saproxylic fauna compared to other insect groups and the continued decline in the number of skilled taxonomists able to identify these species (Hopkins & Freckleton 2002). Thus, deadwood volume and levels of decay are often surveyed as a surrogate (Rondeux & Sanchez, 2010), despite the fact that deadwood availability has not been proven to be correlated with diversity or rarity of saproxylic species (Lassauce et al., 2011). Moreover, as many saproxylic species have poor dispersal abil- ities (Hodge & Peterken 1998), an increase in deadwood avail- ability during forest restoration will rarely be able to make up for a loss of deadwood habitat in the past. Thus, using current measures of deadwood availability can lead to inaccurate as- sumptions about the potential restoration of saproxylic fauna to a site.

A more accurate rapid biodiversity assessment tool for sa- proxylic beetles is therefore needed; one which can directly measure recent saproxylic activity and not simply habitat available. Monitoring vertebrates through indirect indicators of activity is already commonplace: e.g. dung or faeces counts (Webbon, et al., 2004; Harrington et al., 2008; Cromsigt et al., 2009), tracks (Reynolds et al., 2004) and nests (Laing et al., 2003). In contrast, the potential of signs of invertebrate activity as bioin- dicators has rarely been investigated, though with a few exceptions (Schlick-Steiner et al., 2006; Gollan et al., 2010).

Many groups of insects are difficult to sample at large spatial and temporal scales, and often require specialist knowledge. Recently, using “citizen scientists” to overcome these problems has gained momentum. While such programmes have existed for many years for the sampling of vertebrates (Silvertown, 2009; Dickinson et al., 2010), only recently has the use of volunteers to collect data on insects been fully utitised (Kuhn et al., 2008; Kaartinen et al., 2013; Slade et al., 2013). Involving citizen scientists allows for large quantities of data to be col- lected at scales often not possible for a single scientist or habitat manager alone. However, in order for volunteers to make a meaningful contribution, studies and methods need to be carefully designed and accessible to the non-scientist (Lovell et al., 2009).

Many members of the public know very little about the importance of saproxylic invertebrates or even their existence, simply regarding old trees as a hazard (Speight 1989). Thus, finding a tool which could be beneficial to forest managers in assessing saproxylic activity, and which could be extended to members of the public through engagement in citizen science, has the potential to bring this fascinating group to a whole new audience. This in turn could have a long-term impact on the restoration of saproxylic species in general. To quote Daniel Janzen, “If you don’t know it, you can’t love it, if you don’t love it, you won’t save it” (Cardoso et al., 2011).

Developing management tools which can assess the activity of saproxylic invertebrates is not only important for the moni- toring of biodiversity, but also for the assessment of ecosystem functioning. It has been highlighted recently that the restoration of ecosystem functioning should be a core management goal alongside the more traditional aims of recovering biodiversity and structure (Ruiz-Jaen & Aide 2005; Benayas et al. 2009; Suding, 2011). Saproxylic insects perform a vital ecosystem service by accelerating the decay process of wood which re- leases nutrients back into the soil (Swift, 1977; Ulyshen, 2013; Ulyshen & Wagner, 2013). There is now recognition that a more functional approach to saproxylic insect conservation, one which highlights the role this group of organisms play in nu- trient and carbon cycling, could be a fruitful area of future re- search (Ulyshen, 2013).

Here we present a new tool for rapidly assessing saproxylic functioning by non-specialists, through a direct measure of their activity. Saproxylic invertebrates produce wood bore holes of varying size and shape (Ehnstrohm & Axelsson, 2002; Speight, 2005), and thus the diversity of bore holes has the potential to be used as an indicator of saproxylic diversity (Angelstam & Doenz-Breuss, 2004). Bore hole densities have already been successfully used as a measure of bark beetle attack rates (Lo- zano et al., 1997, Kelsey & Joseph 2001); the methodology we present expands on this idea of measuring saproxylic activity directly by incorporating a surrogate of community diversity.

We investigated whether factors which are known to affect saproxylic invertebrate diversity also affect bore hole diversity within an oak wood pasture. We hypothesise that some of the factors that affect species diversity of saproxylics will be found to also affect bore hole diversity, indicating the potential for this method as a surrogate to monitor the restoration of saprox- ylic activity in a site.

Methods

Study Site

The study was carried out over 4 weeks in late January to early February 2006 in Dalkeith Old Wood, 11 km south of Edinburgh, Scotland (55˚54'17.25"N, −03˚03'52.67"W). The site is an ancient oak-wood pasture bordered with semi-natural woodland on the banks of the North and South Esk rivers, cov- ering an area of 26.4 ha within Dalkeith Country Park. The site is an ancient wood pasture, which is defined by the presence of open-grown, old or “veteran” trees in a habitat which is kept open by grazing animals (Hol & Smith, 2002).

The dominant species in the woodland is oak, a mixture of mature sessile oak (Quercus petraea (Matt.) Liebl.) and pe- dunculate oak (Quercus robur L.). Ash (Fraxinus excelsior L.), hawthorn (Crataegus monogyna Jacq.) and birch (Betula pen- dula Roth) are also present in small amounts within the wood- land boundary (Johnston, 2002).

Survey Methods

The sampling area consisted of approximately 1000 oak trees tagged from previous studies. Since trees were tagged linearly, with neighbouring trees bearing similar numbers, stratified random sampling was used to ensure a spread of trees was se- lected from across the site. Each set of 100 numbered trees was considered a stratum from which 5 trees with rot sites were selected using a random number table, resulting in a total of 45 surveyed trees. At the time of year the study was conducted it was not possible to distinguish between Quercus petraea and Quercus robur and therefore the ratio of each in the survey is not known. In addition, five pieces of fallen deadwood were selected within each stratum using random coordinates.

Substrate characteristics

Three factors known to affect saproxylic invertebrate diver- sity were surveyed; diameter, rot type and rot site orientation.

Diameter is one of the factors most frequently presumed to affect saproxylic invertebrate diversity on standing or fallen deadwood substrates. There is thought to be greater saprox- ylic species richness and greater saproxylic abundance on trees and logs with larger diameters (Ranius & Jansson 2000). The diameter at breast height (dbh, measured at 1.3 m from the ground) was recorded for all trees surveyed. For fallen deadwood the diameter at the thickest point was measured.

Wood rot is caused by fungal mycelium. There are two main types of wood rot: red/brown rot and white rot. Red/ brown rot fungi decompose wood by primarily using the carbohydrates (cellulose) of the cell walls, where as white rot fungi utilise both the lignin and carbohydrate components (Patton, 1990). These differences are important as they will affect the success- sive utilisation of the wood by invertebrates (Speight, 1989). All rot site encountered on fallen logs were surveyed and on trees all rot sites below two metres from the ground were sur- veyed. The rot type was classified using the English Nature Veteran Trees Initiative which defines rot types based on colour and texture and assigns them into categories lettered from A to O (Fay & De Berker, 1996).

Rot site orientation has been observed to affect the densities of certain saproxylic species (Ranius & Nilsson 1997), as ori- entation of rot sites affects sun exposure and microclimate. For this reason direction of rot site (divided into 8 categories NW, N, NE, E, SE, S, SW and W) was recorded.

Saproxylic Activity Index

Bore holes were surveyed using 5 cm × 5 cm quadrats. For each rot site, five quadrats were surveyed from random points on the rot area. If the rot site was small as many quadrats as could cover the area were surveyed.

Within each quadrat the number of bore holes was counted and recorded according to their diameter and shape. We used three possible shape categories: oval, round and D-shaped, and six size categories: <1 mm, 1 mm < 2.5 mm, 2.5 mm < 5 mm, 5 mm < 7.5 mm, 7.5 mm < 10 mm, >10 mm. This resulted in 18 categories into which bore holes could be classified―referred to as saproxylic activity units (Figure 1). For analysis means were calculated for each rot site, to account for the variation in the number of quadrats among different rot sites, and results scaled to values per m².

The 18 categories of bore holes, or activity units, were then used to calculate a measure of bore hole density, bore hole richness (overall richness of different types of activity units, analogous to species richness) and a bore hole diversity index using the Shannon-Weiner index. The bore-hole diversity index was calculated using the Shannon-Weiner index as the species accumulation curve demonstrated that all species likely to occur at the site had been sampled (Figure 2) (Magurran, 2004). Together we refer to these measures as the Saprox- ylic Activity Index.

Statistical Analysis

Rot sites were treated as independent samples as Ranius and Jansson (2002) argued that each rot site could be viewed as a local population due to the fact that there may be many cycles

of generations within one rot site and these populations exist independently of their neighbours. Analyses were carried out using R version 15 (R core team, 2013). Bore hole density, richness and diversity were assessed in relation to substrate di- ameter using linear regression. Bore hole density, richness and diversity in relation to rot direction and rot type were assessed using one-way ANOVAs. Bore hole density was log-trans- formed to meet the model requirement of normality.

Results

Distribution of Insect Bore Holes

The majority of bore holes were round, accounting for 96% of bore holes surveyed. Bore holes were far more frequent in the smaller size categories with 81% of all bore holes having a diameter of less than 1 mm. The most prevalent type of bore hole category in both standing and fallen deadwood was round <1 mm diameter, accounting for 80% of all bore holes surveyed. There were large variations in the density of bore holes between rot sites. The minimum density of bore holes was 320 per m², the maximum 28,160 per m² and the average 6495 per m². Bore hole richness at the study site was 11 out of a possible 18 cate- gories. On fallen deadwood all 11 categories were present; on standing deadwood only nine categories were recorded. Accu- mulation curves indicated that the sampling effort was suffi- cient to record all categories likely to be present at the study site (Figure 2).

Factors Affecting the Distribution of Insect Bore Holes

Bore hole density and diversity showed no relationship with the direction of rot site or the diameter of the substrate (Figure 3(a): log(bore hole density)~diameter: df = 1, F = 1.43, p = 0.23; Figure 3(b): bore hole diversity~diameter: df = 1, F = 0.003, p = 0.95; Figure 3(c): log(bore hole density)~rot site direction: df = 7, F = 0.38, p = 0.91, Figure 3(d): bore hole diversity~rot site direction df = 7, F = 0.365, p = 0.92).

Saproxylic activity index recording card and quadrat.