Assessing Forest Naturalness

Ronald E. McRoberts, Susanne Winter, Gherardo Chirici, and Elizabeth LaPoint
Abstract: The concept of naturalness has been proposed and used for describing the ecological value of forest ecosystems, evaluating management efforts to conserve biodiversity, and identifying natural, old-growth forests for purposes of establishing protection areas. Because the concept is not globally familiar, a literature review was conducted to document the ecological basis for the concept. In addition, the necessity for harmonized reporting motivated an investigation of variables that can be used to quantify and assess forest naturalness. National forest inventories (NFIs) are sources of the most comprehensive and extensive data available for assessing naturalness. However, the variety of NFI plot configurations, sampling designs, definitions, and measurement protocols greatly impedes the utility of NFI data for purposes of producing compatible estimates. As a component of a pan-European harmonization project, a three-phase investigation of harmonized approaches to assessing forest naturalness using NFI variables was conducted. Although the project was primarily European in scope, forest inventory data for an American ecoprovince were used because of their availability, comprehensiveness, and consistency. The primary result is that NFI features such as minimum dbh and plot size affect estimates of indicators of naturalness, and accommodation of their differences may be necessary if harmonized estimates of indicators of naturalness across countries are required. FOR. SCI. 58(3):294 –309. Keywords: harmonization, biodiversity indicators, hemeroby

relates to the degree to which forest ecosystems are characterized by natural processes and/or the absence of human influence. Although the concept is increasing in importance in some parts of the world, it is almost completely unfamiliar in other parts of the world. Thus, a review of the naturalness concept and an investigation of methods for harmonized estimation of indicators of naturalness is warranted. The overall objectives of the study were twofold: to review the forest naturalness concept by documenting the literature on the topic, describing the ecological development of the concept, and addressing the increasing importance of harmonized estimation of indicators of naturalness and to investigate methods for estimating harmonized indicators of forest naturalness using data obtained for national forest inventory (NFI) variables. The sections that follow immediately address the first objective. Specific intermediate objectives for a threephase study to address the second objective are provided at the end of the Introduction section.


The Forest Naturalness Concept Ecological Integrity
Historically, the evolution and dispersal of species has been thought to keep pace with environmental changes on a geological time scale (Pickett et al. 1992). However, recent opinions are that the pace of human influence on the environment may fundamentally alter that relationship (Crumpacker 1998). In response, conservation biol-

ogy has emerged as the application of scientific principles to address the effects of human disturbance on ecological systems (Soule 1985). This view emphasizes ´ maintenance of the natural integrity of ecosystems and is guided by the principles that biotic diversity, ecological complexity, and succession are results of natural processes, are intrinsically good, and are valuable management objectives (Soule 1985, Angermeier and Karr 1994, ´ Crumpacker 1998) and that naturally evolved ecosystems are of greater value and quality than disturbed or artificial systems (Liira et al. 2007). The term ecological integrity has been used to ascribe value to older, natural forest stands (Karr 1991, Woodley et al. 1993, Angermeier and Karr 1994, Ohlson et al. 1997, Angermeier 2000). The first reference to integrity in the ecological sense may have been Aldo Leopold’s (1949) famous statement, “A thing is right when it tends to preserve the integrity, stability, and beauty of the biotic community. It is wrong when it tends otherwise.” More recently, Cairns (1977) defined integrity as maintenance of the community structure and function characteristic of a particular locale. Angermeier and Karr (1994) stated that integrity refers to a system’s wholeness including the presence of all appropriate elements and occurrence of all processes at appropriate rates over spatiotemporal scales. Noss (1990a) asserted that communities have integrity when they are dominated by native species, are relatively stable, and show attributes of healing. Angermeier and Karr (1994) attributed the most influential definition of biological integrity to Frey (1975), who stated that integrity is “the capability of supporting and maintaining a balanced, integrated, adaptive community of

Manuscript received June 15, 2010; accepted June 1, 2011; published online May 3, 2012; Ronald E. McRoberts, US Forest Service, Northern Research Station, Forest Inventory and Analysis, 1992 Folwell Avenue, St. Paul, MN 55108 —Phone: (651) 649-5174; Susanne Winter, Technische Universitat Dresden— Gherardo Chirici, Univer¨ sita degli Studi del Molise— Elizabeth LaPoint, US Forest Service, Northern Research Station— ` This article was written by U.S. Government employees and is therefore in the public domain.


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organisms having a species composition, diversity, and functional organization comparable to that of natural habitat of the region.”

Angermeier (2000) asserted that the foundation of ecological integrity lies in the concept of naturalness. Definiˇ tions of naturalness vary (Saudyte et al. 2005), but all relate ˙ to a continuum with entirely natural and entirely artificial at the extremes (Angermeier 2000). With respect to forests, terms used to describe regions of the continuum, progressing from natural to artificial, include primeval, pristine, virgin, or undisturbed (Lindenmayer and Franklin 1997, ˇ Angermeier 2000, Saudyte et al. 2005, Liira et al. 2007, ˙ Ministerial Conference on the Protection of Forests in Europe [MCPFE] 2007), which refer to forests that have evolved without any human intervention and that have structures encompassing all stages and dynamics of the forest life cycle; near-natural, which refers to naturally regenerated forests composed of native tree species that have been managed in the past but have now experienced a relatively long period of minimal human interference (Mountford 2002); intact, which indicates the presence of all the critical ecosystem components and structure and with processes functioning within natural limits (Anderson 1991); semi-natural, which indicates forest development influenced by human activities using ecological principles with the result that species composition and forest structure are similar to those of the natural forest (Hansen et al. 1991, ˇ Saudyte et al. 2005, MCPFE 2007); conventionally man˙ aged, which indicates levels of intense management (Liira et al. 2007); and plantations of either native or introduced species. The thresholds separating these regions are nebulous and assignment of a forest to a particular region of the continuum depends on the evaluation approach and local conditions. For this study, a paraphrase of S. Winter’s (manuscript in preparation, 2011) definition of naturalness, whereby an ecosystem is characterized as more natural if its current state is more similar to its expected natural state, is used. The concept of naturalness has been proposed and used for multiple forest-related purposes. First, naturalness is used to describe the ecological value of forest ecosystems (Usher 1986, Lane and Tait 1990, Crumpacker 1998, ˇ Saudyte et al. 2005) so that planning and management ˙ practices can be applied to maintain and/or increase those values (Smith and Theberge 1987). Second, because of its strong linkage to biological integrity, naturalness is used as a basis for judging management efforts to maintain and conserve biodiversity (Harris 1984, Hansen et al. 1991, Hoerr 1993, Angermeier and Karr 1994, Norton 1996, Lahde et al. 1999, Trass et al. 1999, Angermeier 2000, ¨ Norden and Appelqvist 2001, Bartha et al. 2006, Liira et al. ´ 2007). Third, naturalness is used to identify natural, oldgrowth forests for purposes of establishing protection areas (Smith and Theberge 1987, Gustafsson 2002, Uotila et al. 2002, Branquart and Latham 2007). Two specific studies illustrate these uses. The Biodiversity Evaluation and Assessment Research (BEAR) project, subtitled “Indicators

for Monitoring and Evaluation of Forest Biodiversity in Europe,” focused on developing tools for evaluating forest biodiversity and included measures related to naturalness among the key factors (Larsson et al. 2001). An assessment by the MCPFE (2003) of the current state of European forests relative to the criteria and indicators of sustainable forest management used areas and percentages of semi-natural and undisturbed forests as measures of the degree to which forest biodiversity was maintained and conserved (MCPFE 2007, Criterion 4). Two perspectives on naturalness serve as bases for approximately complementary approaches to its assessment. The first approach is based on an assessment of ecosystem processes (Peterken 1996). The advantage of this approach is that the assessment focuses on the subject of primary concern, the ecosystem (Forest Resources Association [FRA] 2000). The disadvantages are the difficulties in defining and measuring parameters that relate to ecosystem processes and that can be evaluated in a globally consistent manner at broad geographical scales. The second approach is based on the degree of human influence (Rolston 1990, Anderson 1991) and focuses on human activity as the driver of ecosystem disturbance. Jalas (1955) introduced the term hemeroby, from the Greek hemeros meaning cultivated, tamed, or refined, as a measure of human impact on ecosystems. Sukopp et al. (1990) and Kowarik (1990) characterized hemeroby as a measure that integrates the effects of past and present human influence on ecosystems. Although hemeroby has been used mostly in Central Europe (Kowarik 1990, Sukopp et al. 1990, Grabherr et al. 1995, Kim et al. 2002), the idea was also used by the Global Forest Resources Assessment (FRA 2000), which defined naturalness as “lack of anthropogenic disturbance.” Although no single variable has been found adequate for assessing all aspects of forest naturalness, assessment of all variables is not only impossible but also would not produce policy-relevant information for nonexperts (Branquart and Latham 2007). Thus, a small set of appropriate indicators is required where an indicator is defined as a feature of a biological system whose occurrence contributes to assessing the most important aspects of forest biodiversity (Larsson et al. 2001). For the hemeroby approach, proposed indicators primarily relate to evidence of human activity and include the number of cut stumps (FRA 2000, Uotila et al. 2002, ˇ Saudyte et al. 2005), signs of slash and burn (Uotila et al. ˙ 2002), absence of deadwood, growing stock volume (Uotila et al. 2002), and signs of silvicultural management such as site preparation, artificial regeneration, and thinning. For the ecosystem approach, variables that have been proposed include numbers of old and large trees (McComb et al. 1993, Gustafsson 2002, Nilsson et al. 2002, von Oheimb et al. 2005), number of canopy or height layers (McComb et al. 1993, Uotila et al. 2002), the presence and/or amount of deadwood (McComb et al. 1993, FRA 2000, Gustafsson 2002, Nilsson et al. 2002, Christensen et al. 2005, Liira et al. 2007), shapes of diameter distributions (Koop and Hilgen 1987, Buongiorno et al. 1994, Kuuluvainen et al. 1996, 1998, Linder et al. 1997, Lahde et al. 1999, Maltamo et al. ¨ 2000, Uotila et al. 2002, Siipilehto and Siitonen 2004, von
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Oheimb et al. 2005, Westphal et al. 2006), species composition (Gustafsson and Hallingback 1988, McComb et al. ¨ ˇ 1993, Cochrane and Schulze 1999, FRA 2000, Saudyte et ˙ al. 2005, Bartha et al. 2006), number of microhabitats (Winter and Moller 2008), growing stock volume (Kuulu¨ vainen et al. 1998, Uotila et al. 2002), and forest structural diversity (Hansen et al. 1991, Burschel 1992, McComb et al. 1993, Buongiorno et al. 1994, Larsen 1995, Kuuluvainen et al. 1996, Peterken 1996, Lahde et al. 1999, McComb and ¨ Lindenmayer 1999, Uotila et al. 2002, Winter et al. 2010). Multiple criteria have been proposed for determining the utility of indicators of naturalness. Useful indicators must distinguish between natural and anthropogenic features (Hardt and Swank 1997, Lindenmayer and Franklin 1997, Nowacki and Abrams 1997, Angermeier 2000), they must be reliable in the sense that they are objective (Uotila et al. 2002) and produce consistent and precise results (Smith and Theberge 1987, Liira et al. 2007), they must be readily calculable from available data (Bartha et al. 2006, Liira et al. 2007), they must be sensitive to a large range of effects (Angermeier and Karr 1994), and they must be appropriate at multiple spatial scales (Bartha et al. 2006). The national forest inventories (NFIs) conducted in Europe and North America and increasingly in Asia and South

America are sources of the most comprehensive and extensive data that can be used to assess forest naturalness. Although the assessment of naturalness is much more common in Europe than elsewhere, even in Europe, consistent objective multicountry assessments are impeded by four factors. First, not all countries assess naturalness as part of their NFIs (Figure 1); of the 19 European countries submitting data as part of a European harmonization project (COST E43 2007), only 11 countries assess naturalness. In general, countries with the least amount of forest area characterized as natural or close to natural are the countries that do not assess naturalness. Second, among countries that conduct such assessments, consistent data and common approaches are not used. Of the European countries whose NFIs assess naturalness, the most commonly used criterion is signs of silvicultural management; other criteria include tree species composition and tree or stand age, and the presence and/or amount of deadwood is also used (Figure 2). This disparity among approaches to assessing naturalness can be partially attributed to differences among NFIs with respect to variables assessed, definitions of those variables, sampling designs, plot configurations, measurement protocols, and analytical methods. Third, few forested areas in either Europe or North America remain that could be

Figure 1.

European countries whose NFIs assess naturalness.


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Figure 2. ness.

Criteria used by European NFIs to assess natural-

coverage. For beech forests in Germany, Winter (2006) reported three indices with average thresholds for distinguishing managed and near-natural forest: 1.8 living trees/ha with dbh 80 cm, albeit with diminished vitality; more than half the standing and fallen deadwood pieces with length 10 m; and 3 trees/ha with dbh 60 cm and with the fungus, Fomes fomentarious. Winter et al. (2010) presented an assessment approach using a metric based on ordinal and presence/absence data for numerous ecologically relevant variables rather than for a minimum set of variables. Despite the difficulty in assessing naturalness, international interest in silvicultural practices that mimic natural forest ecosystem processes has increased in recent years (Lahde et al. 1999). In most European countries, a close¨ to-nature silvicultural approach is becoming the norm (von Oheimb et al. 2005, Ciancio et al. 2006), and forest ecosystems with a high degree of naturalness are becoming the forest management standard for comparison (Peterken 1996, Lahde et al. 1999). In addition, European countries ¨ have committed to implementing guidelines for sustainable forest management that conserve biodiversity and promote naturalness (Loiskekoski et al. 1993, Ratcliffe and Peterken 1995).

construed as natural. Branquart and Latham (2007) reported that ratios of the areas of nearly natural forest to the total areas of forest and other wooded lands for Europe are 0.001 for Western Europe (Belgium, Denmark, France, Netherlands, and the United Kingdom), 0.013 for Southern Europe (Cyprus, Greece, Italy, Portugal, and Spain), 0.025 for Central Europe (Austria, Bulgaria, Czech Republic, Lithuania, Macedonia, Romania, Slovenia, and Switzerland), and 0.083 for Northern Europe (Finland, Norway, and Sweden). They attributed the greater ratio for Northern Europe to the chronologically later onset of human influence. The MPCFE (2007, Criterion 4), reported that the ratio for undisturbed forest in Europe in its entirety, excluding the Russian Federation, is nearly 0.05 with half the undisturbed area in Sweden. Fourth, protected or reserved areas whose forest attributes might be considered references for naturalness comparisons are often located on relatively unproductive sites that may have low natural levels of biodiversity (Recher 1996) and may lack important forest plant and animal species (Lindenmayer and Franklin 1997). Reports in the literature of attempts to construct objective, quantitative indices of forest naturalness are few, and those reported are specifically adapted to individual cases (Machado 2004). Although European NFIs base their assessments on observations of a variety of variables, the assessments are often visual or subjective. Scholes and Biggs (2005) proposed a biodiversity intactness index, but it is still subjective because it relies heavily on expert judgments. Petriccione (2006) proposed a more quantitative approach based on comparing observed and potential vegetation types. If the two types are different, a naturalness value of 0.0 is assigned; if they are the same, then the naturalness value is based on the average of six indices characterizing disturbance and species types, richness, and

International Reporting
The increased interest in forest biodiversity and its essential features, including naturalness, have led to numerous international agreements that include reporting requirements. The Convention on Biological Diversity (2007) requires that countries identify and monitor components of biological diversity for purposes of conservation and sustainable use. The primary forestry sustainability conventions, Forest Europe, formerly the MCPFE (2003), and the Montreal Process (2005) require that member countries ´ report on sustainability and biodiversity indicators. Within this international reporting context, McRoberts et al. (2009) documented recent increased attention to harmonized reporting. Monitoring guidelines developed by the Intergovernmental Panel on Climate Change (IPCC) addressed issues of transparent and harmonized reporting (IPCC 1997). The Good Practice Guidance (GPG) (IPCC 2003, Eggleston et al. 2006) for Land Use, Land Use Change and Forestry(LULUCF) provided detailed guidance for some aspects of reporting. The United Nations Economic Commission for Europe (UNECE) and the Food and Agriculture Organization (FAO) of the United Nations jointly compiled the Temperate and Boreal Forest Resources Assessment (TBFRA) covering the forest resources of North America, Europe, the Commonwealth of Independent States, Australia, New Zealand, and Japan. For the TBFRA 2000 assessment, the UNECE/FAO team compiled international definitions and then harmonized national data to conform to these definitions (UNECE and FAO 2000). Kohl et al. (2000) described two approaches that can be ¨ used to increase the consistency of forest resource estimates among countries. The first, standardization, is a top-down approach that requires a common system of nomenclature and focuses on common standards with respect to NFI
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definitions and methods. Although standardization of NFIs would produce the most direct route to compatible estimates, other factors must be considered. For example, NFI features such as sampling designs and plot configurations for individual countries have been developed over time to accommodate their unique topographies, climates, forest types, and economic conditions. Thus, standardization is often not a realistic option. The second approach, harmonization, is based on the assumption that the unique features of individual NFIs are justified and are unlikely to be changed. Harmonization, therefore, focuses on developing methods for producing comparable and compatible forest attribute estimates despite the lack of standardization. In contrast to standardization, harmonization is a bottom-up approach that begins in divergence and ends in comparability (Kohl et al. 2000). ¨ The most comprehensive effort directed toward harmonization of estimates of forest biodiversity using NFI data for international reporting was conducted by COST Action E43, Harmonisation of National Forest Inventories in Europe: Techniques for Common Reporting (COST E43 2007, Tomppo et al. 2010, Chirici et al. 2011, Tomppo et al. 2012). Within COST Action E43, a primary task of Working Group 3 (WG3) was to evaluate the utility of NFI variables and field methods for estimating components of biodiversity and to develop methods for harmonizing estimates (Chirici et al. 2011). The WG3 investigations of naturalness focused on investigating and recommending quantitative methods using NFI data for characterizing and identifying natural forest data and for producing harmonized estimates of indicators of naturalness. The immediately preceding sections document the current understanding of the naturalness component of biodiversity and methods for its assessment as reported in the literature, thus achieving the first overall objective. The primary conclusions are that the naturalness concept is not well defined in the sense that no rigorous definition has been generally accepted and that no completely objective method for quantifying naturalness is available. Thus, an underlying objective implicit in any study of naturalness must be to motivate additional study to increase the maturity of the naturalness concept and methods for its assessment.

indicators based on NFI variables selected from the first phase were evaluated with respect to their potential for harmonized estimation, particularly their sensitivity to NFI sampling features such as minimum dbh and plot size, which differ considerably among the NFIs of different countries. The second-phase objective was to determine the degree to which NFI variables selected from the first phase could readily be harmonized for use in a common approach for assessing naturalness. In the third phase, a multidimensional approach based on NFI variables satisfying the firstand second-phase criteria was investigated for estimating the degree to which conditions observed on NFI plots correspond to more natural forest. The third-phase objective was to assess the utility of the multidimensional approach. A consequence of the sequential nature of the analyses is that the organization of the remaining sections of this report deviates from the traditional data-methods-results sequence. Instead, following the Data section, methods and results are reported sequentially for the respective phases.

Data Study Area
The study area is the portion of Bailey’s (1976) ecological province 212 in the northcentral region of the United States (Figure 3). The study area extends approximately 700 km north to south and approximately 775 km east to west and includes 265,000 km2. Most of the province has low relief with rolling hills, lakes, poorly drained depressions, and glacial features. Elevations above sea level are mostly in the range of 175 to 550 m, mean annual precipitation ranges from 560 mm in the northwest to 850 mm in the southeast (National Oceanic and Atmospheric Administration 1974), mean minimum winter temperature ranges from 20 °C in the northwest to 9 °C in the southeast, and mean maximum summer temperature ranges from 21 °C along the Great Lakes on the northern boundary of the province to 28 °C in the southeast. The province lies between boreal and broadleaf deciduous forest zones with soils that vary greatly and include peat, muck, marl, clay, silt, sand, gravel, and boulders in various combinations. The forests in ecological province 212 were first harvested by European descendants in the mid to late 1800s with earlier dates in the east and later dates in the west. Tree species in the province generally have rapid early growth and reach economic maturity in approximately 50 years. Thus, the province is experiencing its third and fourth cycle of forest harvest.

Harmonized Estimation of Naturalness Indicators
A three-phase study was designed to achieve the second overall objective, investigation of methods for estimating harmonized indicators of forest naturalness using data obtained for NFI variables. The investigations were sequential in the sense that results obtained from a previous phase were used to design analyses for subsequent phases. In the first phase, NFI variables proposed in the literature for constructing indicators of naturalness were analyzed with respect to the number of countries participating in COST Action E43 that measure the variables and with respect to the features of the variables that make them desirable or undesirable as indicators. The first-phase objective was to select a subset of the variables proposed in the literature that are assessed by NFIs and that satisfy indicator criteria. In the second phase, 298
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Forest Inventory Data
The Forest Inventory and Analysis (FIA) program of the US Forest Service conducts the NFI of the United States. The FIA program has established field plot centers in permanent locations across the country using a sampling design that is assumed to produce a random, equal probability sample (Bechtold and Patterson 2005, McRoberts et al. 2005). The sampling design is based on a tessellation of the United States into 2,400-ha (6,000-ac) hexagons and features a permanent plot at a randomly selected location

Figure 3. located.

Bailey’s (1976) ecoprovince 212 (black) where the NFI plots of the aspen forest type group are

within each hexagon. The average distance between plots is approximately 5 km, and over a complete 5-year measurement cycle, the sampling intensity is approximately 1 plot/2,400 ha. Each plot consists of four 7.31-m (24-ft) radius circular subplots for a total area of 672 m2. The subplots are configured as a central subplot and three peripheral subplots with centers located at 36.58 m (120 ft) and azimuths of 0, 120, and 240° from the center of the central subplot. FIA data were acquired for all plots on forestland in ecological province 212 (Figure 3) that were wholly in the aspen forest type group. The FIA requirements for forestland are at least 0.4 ha (1.0 ac) in size, at least 10% stocked (Husch et al. 2002), at least 36.58 m (120 ft) in crown-tocrown width, and use as forestland. Observations of species, height, and dbh were acquired for 82,059 trees on 5,771 NFI plots in the aspen forest type group and were augmented with distances from all trees to plot centers. FIA field crews measure trees with 2.54 cm dbh 12.70 cm on 2.07-m radius subplots and trees with dbh 12.7 cm on 7.31-m radius subplots. Trees of 74 species were observed with Quaking aspen (Populus tremuloides), Balsam fir (Abies balsamea), Bigtooth aspen (Populus grandidentata), Red maple (Acer rubrum), and Paper birch (Betula papyrifera) being the most common species. Three species (Norway spruce, [Picea abies], Scotch pine [Pinus sylvestris], and Russian olive [Elaeagnus angustifolia]) with 121 total observations were species introduced from another continent, three species (Eastern redcedar [Juniperus virginiana], Black walnut [Juglans nigra], and Blackgum [Nyssa biflora]) with 27 total observations were species observed

beyond their original North American natural geographic range, and one species (Ailanthus [Ailanthus altissima]) with two observations was introduced from China and is now considered invasive because of its rapid colonization properties. All plots were measured between October 1999 and September 2004.

Phase 1 Methods
Based on the literature review and the survey of European NFIs conducted by COST Action E43, 10 categories of variables with potential as indicators of forest naturalness were considered. The variables were further categorized with respect to the assessment approach, hemeroby or ecosystem processes, for which they are used (Figure 4). Two categories of variables relate primarily to the hemeroby approach: (1) signs of harvest such as cut stumps and slash, and (2) signs of silvicultural management such as site preparation, artificial regeneration, and thinning. Six additional categories of variables relate primarily to the ecosystem processes approach: (3) number of microhabitats, (4) species diversity including native versus non-native species and species mixes, (5) tree age, (6) numbers of large trees, (7) vertical structural diversity, and (8) horizontal structural diversity. Two additional categories, (9) growing stock volume and (10) deadwood, have been proposed for both the hemeroby and ecosystem processes approaches. For the latter two categories, greater relative growing stock volume has been identified as a characteristic of managed stands, whereas the presence of deadwood indicates more natural
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Figure 4.

Potential indicators.

forests because absence indicates either removal or harvest before death, both of which characterize human influence. Of the variables comprising these categories, several are less than ideal as indicators of narturalness. Among hemeroby variables, signs of harvest and signs of silvicultural management only partially satisfy the reliability criterion. Although these signs clearly indicate human influence, absence of them does not necessarily indicate lack of human influence (Anderson 1991). With the possible exception of stands of short-lived species, the time necessary for stumps and slash to disappear is much less than the time necessary for the effects of human influence to disappear from the ecosystem. von Oheimb et al. (2005) asserted that several generations, possibly comprising hundreds of years, are necessary for a beech forest with an initial highly differentiated age structure to exhibit characteristics of virgin forests. Rademacher and Winter (2003) conducted 5,000-year simulations of natural processes in beech forests for an initial stand structure reflecting current management practices. They found that the influence of the initial stand structure persisted in the ecosystem for as long as 2,000 years, an extremely long interval for a species whose natural maximum lifespan is approximately 450 years. Multiple variables associated with the ecosystem processes approach are also less than ideal as indicators of naturalness when they are used with NFI data. First, the number of microhabitats is measured by the NFI of only one country participating in COST Action E43. Second, because tree age is difficult to determine accurately for many species and because tree age is highly correlated with both dbh and height, it can be eliminated in favor of tree size (Lahde et al. ¨ 1999). Third, comparisons of degree of naturalness based on the amount of growing stock volume are unreliable because of the effects of site, climate, and phenology on plot-level growth dynamics. Further, whereas Kuuluvainen et al. 300
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(1998) and Uotila et al. (2002) report less volume on unmanaged stands in Finland and northeastern Europe, Meyer et al. (2003) found greater volume on unmanaged Albanian beech (Fagus sylvatica) stands. Although regional differences are to be expected, inconsistency in general trends makes a variable less desirable for use as an indicator whose estimates are to be harmonized across regions. The remaining variables all relate to either deadwood or forest structural diversity. Although the presence and/or amount of deadwood is regarded as an important feature of more natural forests, few reports of specific amounts required for a forest to be characterized as more natural or less natural have been published. Some researchers simply refer to the presence of either deadwood in general or large amounts of deadwood (Gustafsson 2002, Uotila et al. 2002, Liira et al. 2007), some refer to “large snags and logs and deep forest litter” (McComb et al. 1993), and some are quite specific, referring to proportions of standing trunks that are dead and proportions of dead trunks that are standing (Nilsson et al. 2002). Of the few reports of specific thresholds, Winter (2006) characterized near-natural beech forest as having more than half the standing and fallen deadwood pieces with length 10 m. Nevertheless, von Oheimb et al. (2007) reported that information gained for some regions and forest types do not transfer to other regions or forest types, that deadwood volumes in the virgin forests of Europe vary greatly, and that climate, site productivity, and competition all produce considerable differences in deadwood volume. This finding is consistent with the strong recommendation by Larsson et al. (2001) that the management and assessment of all components of biodiversity be conducted by forest type using a classification such as that proposed by the European Environment Agency (2006). Thus, despite its important contribution to naturalness (Laarmann et al. 2009), deadwood was not used in this study because development of harmonization bridges was beyond the scope of the objectives. However, Chirici et al. (2011) reported a similar study that does use deadwood. Species diversity, vertical structural diversity, and horizontal structural diversity together comprise forest structural diversity (Pommerening 2002, Varga et al. 2005) which, in turn, constitutes one of three primary components of biological diversity (Noss 1990b). Fortunately, the primary variables necessary to assess forest structural diversity (tree species, height, and dbh) are the most commonly observed NFI variables (Winter et al. 2008). Of these three tree-level variables, height may be less useful because it is difficult to measure precisely, particularly in closed canopy deciduous forests, it is not measured on all trees by all NFIs, and model predictions for trees not measured are imprecise and may also be subject to model bias. However, height measurements are usually obtained for the tallest trees, and sufficient measurements are usually available to determine numbers of height layers, a measure of vertical structural diversity. Horizontal structural diversity is usually assessed using estimates of parameters of dbh distributions, and tree species diversity is frequently assessed using any of several common indices.

Results and Discussion
The results of the phase 1 analyses are threefold. First, hemeroby variables may be useful as indicators of managed stands but not necessarily as indicators of more natural stands. Second, although the presence of deadwood may be potentially useful as an indicator of more natural forest, its absence is not necessarily useful as an indicator of less natural forest. In addition, quantitative thresholds for amounts of deadwood necessary to distinguish between more natural and less natural forest are generally not available. Further, even if they were available, they would be expected to vary greatly with climate, topography, and other factors, even within the same forest type (Larsson et al., 2001). Third, for the ecosystem processes approach, the availability of observations of tree species, height, and dbh have the potential to make indicators related to species and vertical and horizontal diversity good candidates for assessing natural forest. Thus, tree species, height, and dbh satisfy the criteria for indicators and are commonly measured by NFIs, and their selection for further evaluation in phase 2 constitutes satisfaction of the phase 1 objective.

Phase 2 Methods
The phase 2 analyses focused on evaluating the effects of two NFI sampling features, minimum dbh and plot size, on potential indicators for distinguishing less natural and more natural forests. For the hemeroby approach to assessing forest naturalness, proposed indicators have been based primarily on dichotomous variables: presence/absence of cut stumps, presence/absence of slash, presence/absence of deadwood, and presence/absence of signs of management. With the exception of deadwood, these variables are not sensitive to size thresholds such as minimum dbh. However, they are extremely sensitive to plot size; in particular, the probabilities of detecting signs of human influence and deadwood are proportional to the square of the plot radius. Therefore, their utility is limited when one is attempting to harmonize estimates of naturalness for NFIs that use sample plots of different sizes and configurations. For the ecosystem processes approach to assessing forest naturalness, indicators related to species and vertical and horizontal diversity were constructed using observations of tree species, height, and dbh. As a measure of tree species diversity, the Shannon index is calculated as

species diversity for diptocarp and nondiptocarp stands in ¨ Indonesia (Onal 1997): P. sylvestris-dominated forests in Finland (Kuuluvainen et al. 1998); montane broadleafconifer- and conifer-dominated stands in Austria (Neumann and Starlinger 2001); and single- and mixed-species conifers in western Canada (Varga et al. 2005). H has been selected as a measure of species diversity by WG3 of COST Action E43 and has been used to assess tree species diversity for a large region of the United States (McRoberts et al. 2008). Vertical structural diversity was assessed using numbers of layers and numbers of tall trees. For each NFI plot, height layering was assessed in four steps: (1) the mean height of the proportion ptall 0.005 tallest trees represented in the dataset was determined, where ptall 0.005 is acknowledged to be an arbitrary choice; (2) three height layers, which is the most commonly used number by NFIs (Chirici et al., 2011), were defined by dividing the mean height of the ptall tallest trees into thirds; (3) each tree on each NFI plot was assigned to a height layer; and (4) the specific height layers represented on each plot were determined. More natural forests are expected to include multiple height layers; thus, a plot was characterized as satisfying the LAYERS criterion if it included trees in multiple height layers of which one was the tallest layer. In addition, an NFI plot was characterized as satisfying the TALL criterion if it included at least one tree among the ptall tallest trees. Measures of horizontal structural diversity were based on two parameters of dbh distributions, SD and skewness. The SD, , of the distribution of dbh observations on a plot is estimated as 1 n 1


i 1

dbh)2 ,

j 1


where nsp is the number of species observed on a plot and pj is the proportion of total plot basal area in trees of the jth species (Shannon 1949). For this study, pj was based on basal area to circumvent problems with large numbers of very small trees (Staudhammer and LeMay 2001). The Shannon index is 0 when all trees are of the same species, increases when more species are observed, and is maximized for a given number of species when the proportions are equal. The Shannon index has been used to estimate

where i indexes trees measured on the plot, n is the number of trees measured, and dbh is the mean dbh of measured trees. The advantages of sdbh are that it is easy to calculate and easy to interpret. Minimum values of sdbh are realized when all dbh observations are similar, whereas maximum values are realized when half the observations are at the lower extreme and half are at the upper extreme. In addition, sdbh has been selected as a measure of forest structural diversity by WG3 of COST Action E43 and has been used to assess horizontal structural diversity for a large region of the United States (McRoberts et al. 2008). Diameter distributions for unmanaged or natural forest stands are often characterized as having a reverse J-shape, i.e., large numbers of small diameter observations to the left of the mean and smaller numbers of trees with large, scattered diameter observations to the right of the mean (Koop and Hilgen 1987, Korpel 1995, Kuuluvainen et al. 1996, Linder et al. 1997, Uotila et al., 2002, Siipilehto and Siitonen 2004, von Oheimb et al. 2005, Westphal et al. 2006). The essence of this characteristic is a positive skewness in the diameter distribution with an extended upper tail. A common and easily computed measure of the skewness of a distribution is its third moment which is defined as
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1 (dbhi ni 1





where dbh is mean plot dbh (Snedecor and Cochran 1967). Large, positive values of indicate a reverse J-shape distribution (Figure 5). For this study, the cube root of the estimate of skewness, gdbh

1 (dbhi ni 1


dbh)3 ,

where dbh is the mean dbh of measured trees, was used as a transformation of skewness in the same manner as SD is used as a transformation of variance. The effects of minimum dbh and plot size on the LAYERS and TALL criteria, H , sdbh, and gdbh were estimated. Each indicator was calculated for each plot using levels of minimum dbh and plot radius in the ranges reported by NFIs to COST Action E43. In addition, for each indicator and each combination of minimum dbh and plot radius, the effects of the minimum number of trees per plot, ntree, were evaluated.

Results and Discussion
For purposes of harmonized estimation of naturalness via NFI variables, the utility of the three indicators, H , sdbh, and gdbh, cannot be directly assessed because so little natural forest exists for direct comparison purposes. Nevertheless, the three indicators are based on variables reported in the literature, satisfy indicator criteria, and are the most commonly assessed NFI variables. Thus, this indirect approach is the best that can currently be achieved. However, the results of the phase 2 analyses suggest that harmonization of estimates of the indicators may be difficult apart from a common minimum dbh, a common plot size,

and a common ntree. H , sdbh, gdbh, and satisfaction of the LAYERS and TALL criteria were all somewhat sensitive to minimum dbh, quite sensitive to plot radius, and often sensitive to ntree (Figures 6A–D, 7A–D, and 8). The TALL criterion does not depend directly on minimum dbh, although the latter affects the total number of trees observed and indirectly the number of trees represented by ptall. Harmonization to accommodate differences in some NFI features can be accomplished using bridges that convert estimates based on national definitions and features to estimates that conform to common definitions and features (McRoberts et al. 2009, Ståhl et al. 2012). With reductive bridges, some data are simply discarded. For example, harmonization to accommodate differences in minimum dbh can be accomplished by simply disregarding all trees with dbh less than a common dbh. Likewise, a requirement for a common ntree can be satisfied by disregarding all plots with numbers of trees less than ntree. However, a reductive bridge to accommodate differences in plot size is more difficult. In this case, the essence of the bridge would be to disregard all trees whose distances from plot centers are greater than the common minimum radius. Unfortunately, the bridge requires ancillary data in the form of distances from plot centers to individual trees, information that is often not collected or is not readily available from NFIs. Pairwise correlations among H , sdbh, and gdbh are generally small, indicating that none of these three indicators can easily be replaced by one or a combination of the other two. In addition, although large values of sdbh and gdbh suggest at least some large dbh observations, trees satisfying the TALL criterion were not necessarily found on plots with the largest values of sdbh or gdbh. The relative independence of the three indicators suggests that each addresses a different dimension of naturalness and that, when combined into a single assessment approach, they may provide a more comprehensive assessment than any of them separately. Thus, the phase 2 objective of determining the degree to which variables selected in phase 1 can be harmonized for use in a common approach for assessing naturalness has been achieved, although the results could have been more positive.

Phase 3 Methods
The emphasis of the third phase was development of a procedure for identifying plots representing conditions expected to be characteristic of more natural forest. Because so few natural forest areas remain for use as references and because hemeroby may be difficult to recognize, the best that can be achieved is to identify plots with characteristics similar to those that would be expected for natural forest (Freedman 1989). The procedure for identifying plots representing more natural forests is based on a proposal by Loidi (1994) that the degree of naturalness can be expressed in terms of a conceptual distance between observed plot conditions and conditions regarded as not measurably influenced by humans. Given the consensus from the literature that naturalness has multiple components or dimensions and that the

Figure 5. Proportion of trees per ha versus dbh based on aggregated observations for the five plots with greatest skewness (gdbh) reveals reverse J-shape dbh distribution.


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Figure 6. (A) Mean Shannon index (H ) versus minimum dbh for plot radius of 14.5 m. (B) Mean SD (sdbh) versus minimum dbh for plot radius of 14.5 m. (C) Mean skewness (gdbh) versus minimum dbh for plot radius of 14.5 m. (D) Proportion of all plots satisfying LAYERS criterion for plot radius of 14.5 m ptall 0.005.

phase 2 analyses identified three relatively independent indicators, Loidi’s proposal was investigated by constructing a distance measure in the multidimensional space of the indicators from phase 2. Before construction of the distance measure, plot-level values of H , sdbh, and gdbh were scaled to a [0-1] interval to weight them equally when used in combination. The scaling procedure for H consisted of three steps: step 1, the plots were ordered with respect to H ; step 2, the mean of the proportion pH 0.005 largest values was calculated, where pH 0.005 is acknowledged to be an arbitrary choice; and step 3, for each plot, the ratio, RH, of H and the mean of the pH largest values from step 2 was calculated with the constraint that RH 1. Similar procedures were used for sdbh and gdbh with ps 0.005 and pg 0.005 and Rs and Rg defined in a similar manner. Plots with more natural forest conditions would be expected to have ratios closer to 1; i.e., distances from (RH, Rs, Rg) to (1, 1, 1) would be smaller.

The procedure for identifying plots representing conditions expected to be characteristic of more natural forest consisted of two primary steps, each with subordinate steps: 1. Eliminate specified classes of plots with less natural forest: a. Eliminate plots with one or more trees of non-native species; b. Eliminate plots that fail to satisfy the LAYERS criterion; c. Eliminate plots that fail to satisfy the TALL criterion; d. Optionally, eliminate plots with signs of human influence such as thinning, harvest site preparation, human damage, non-natural regeneration, cut stumps, slash piles, and others; e. Optionally, eliminate plots with no observed deadwood. 2. For the remaining plots:
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Figure 7. (A) Mean Shannon index (H ) versus plot radius for minimum dbh of 2.5 cm and pH 0.005. (B) Mean SD (sdbh) versus plot radius for minimum dbh of 2.5 cm and ps 0.005. (C) Mean skewness (gdbh) versus plot radius for minimum dbh of 2.5 cm and pg 0.005. (D) Proportion of all plots satisfying LAYERS criterion versus plot radius for minimum dbh of 2.5 cm and ptall pH ps pg 0.005.

a. Eliminate all remaining plots with fewer than ntree trees to assure reliable values for H , sdbh, and gdbh; b. Calculate the Euclidean distance, Dplot, from the three-tuple (RH, Rs, Rg) to the three-tuple (1, 1, 1); small distances indicate that the ratios RH, Rs, Rg, are closer to their maximum values, which represent more natural forest; c. for selected distances, D, determine the percentage, pD, of all plots for which Dplot D. For this study, the optional steps 1d and 1e were not used because deadwood information was available for only a small percentage of plots and distances from plot centers to signs of human influence were not available.

Results and Discussion
The cumulative effects of small values for ptall, pH, ps, and pg reflect the assumption that few plots may be found that represent natural forest. Further, pD was not particularly sensitive to values of ptall, pH, ps, and pg. The proportions of 304
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the total number of plots remaining after step 1 ranged from 0.100 to 0.175, depending on minimum dbh and plot radius. Of the remaining plots, none had Euclidean distance from the three-tuple (RH, Rs, Rg) to the three-tuple (1, 1, 1) less than 0.1, meaning that no plots had maximum naturalness values for all three indicators. This result is consistent with the previous finding that H , sdbh, and gdbh were not highly correlated. Relationships between pD and D were affected by plot radius more than by minimum dbh, although differences were negligible for D 0.40 (Figure 9). The specific plots identified as having the most natural forest conditions on the basis of values of Dplot were not the same for different dbh minima, plot sizes, and choices for ntree (Table 1). However, despite the effects of minimum dbh and plot size on the selection of plots in step 1 and Dplot in step 2, the values of H , sdbh, and gdbh for the plots with the smallest values of Dplot were similar, regardless of minimum dbh and plot size (Table 1). These generally favorable results suggest that the multidimensional approach for assessing

Table 1.

Characteristics of plots with smallest Dplot1. Rank2 Plot No. no. trees Dplot H 2.5 cm; 14.5 m 1,848 288 2,230 31 742 5.0 cm; 14.5 m 1,637 259 1,767 1,971 80 2.5 cm; 10.0 m 1,491 546 1,015 200 229 5.0 cm; 10.0 m 1,175 447 806 188 1,103
10; ptall

sdbh gdbh

Figure 8. Proportion of plots satisfying TALL criterion (at least one tree among ptall tallest trees) versus proportion, ptall, of trees defined as tall trees.

Minimum dbh plot radius 1 2 3 4 5 Minimum dbh plot radius 1 2 3 4 5 Minimum dbh plot radius 1 2 3 4 5 Minimum dbh plot radius 1 2 3 4 5
1 2

29 21 50 55 17 27 20 35 49 18 13 23 22 25 14 11 20 21 13 15

0.14 0.21 0.29 0.33 0.34 0.11 0.19 0.32 0.33 0.36 0.18 0.20 0.31 0.34 0.34 0.17 0.19 0.34 0.34 0.35

1.8 1.7 1.9 1.8 1.5 1.8 1.7 1.6 1.9 1.7 1.6 1.6 1.5 1.3 1.4 1.6 1.6 1.5 1.4 1.4

13.5 12.8 13.3 12.3 13.5 14.5 13.4 13.0 13.0 11.2 13.8 13.2 12.2 15.8 11.6 16.4 15.2 12.7 12.3 13.3

17.5 19.4 13.2 13.2 14.1 17.6 19.9 14.3 12.5 13.8 19.4 17.4 15.5 16.1 19.5 20.6 17.2 15.6 20.2 15.9

Minimum trees per plot Rank based on Dplot.

Figure 9. Proportion, pD, of all plots with Dplot < D and that satisfy LAYERS and TALL criteria; ntree 10.

naturalness as originally conceived by Loidi (1994) performed as expected, thus satisfying the phase 3 objective. Regarding this approach, Chirici et al. (2011) comment that, “Even if the number and particular subindicators used change, the general approach and the manner in which the data are aggregated to derive a complex naturalness index have future potential for operational applications.”

Six primary conclusions may be drawn from the study. First, forest naturalness lacks objective assessment methods.

Second, hemeroby indicators of naturalness such as signs of harvest and management are sensitive to plot size. Therefore, although they may be good indicators of managed forest, they are not necessarily good indicators for distinguishing less and more natural forest when the objective is harmonization over a large range of plot sizes. Third, ecosystem process indicators based on tree species, height, and dbh observations are useful for developing indicators related to species and vertical and horizontal components of forest structural diversity. However, the selected indicators (Shannon index, H , for species diversity; LAYERS and TALL criteria for vertical diversity; and SD, sdbh, and skewness, gdbh, of dbh distributions for horizontal diversity) were sensitive in varying degrees to minimum dbh, plot size, and ntree. The fourth conclusion is that few plots were identified as reflecting all conditions expected to be associated with more natural forest. The proportion of plots remaining after step 1 of the procedure was less than 0.175. In addition, the proportion of remaining plots whose three-tuples (RH, Rs, Rg) were within a Euclidean distance of 0.1 from the three-tuple (1, 1, 1) was less than 0.001, and the proportion within a Euclidean distance of 0.4 was less than 0.005. These results are consistent with the general consensus from the literature that few areas of natural forest remain in the study area (Penna 1999). Chirici et al. (2011) reported similar results for a study using European NFI data. The fifth conclusion is that the procedure for identifying plots with attributes that are similar to those expected for
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natural forest selected plots with similar values for H , sdbh, and gdbh, regardless of minimum dbh, plot size, and ntree. However, although their attributes were similar, the specific plots selected varied greatly for different minimum dbh, plot size, and ntree. Thus, harmonization would be difficult apart from standardized values for those NFI features or reductive bridges to accommodate the differences. The sixth conclusion is that construction of reductive bridges to accommodate differences in minimum dbh and ntree is fairly easy, but construction of bridges to accommodate differences in plot size requires ancillary data in the form of distances from trees to plot centers, information that is usually not readily available. Further, naturally functioning ecosystem processes that have not been subject to human disturbance should be expected to produce rather different conditions that could all be characterized as natural forest, particularly in different forest types, a factor that was not included in this study (Larsson et al. 2001). Finally, we note that Chirici et al. (2011, Section 5.8) document multiple recommendations that would facilitate harmonization of all biodiversity estimates, not just those pertaining to naturalness.

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