Professional Documents
Culture Documents
DOI 10.1007/s10661-009-0919-4
Received: 15 July 2008 / Accepted: 6 April 2009 / Published online: 7 May 2009
© Springer Science + Business Media B.V. 2009
Abstract Ground vegetation (GV) is an impor- sampling seasons (depending on the phonological
tant component from which many forest biodi- stages) should be specially considered and eval-
versity indicators can be estimated. To formulate uated in the results. The proposed indicators are
policies at European level, taking into account based on composition at different levels of sam-
biodiversity, European National Forest Invento- pling intensity for each life form and on coverage
ries (NFIs) are one of the most important sources measurements.
of forest information. However, for monitoring
GV, there are several definitions, data collec- Keywords Ground vegetation · Ground
tion methods, and different possible indicators. vegetation components · Ground
Even though it must be considered that natural vegetation attributes · Forest biodiversity ·
conditions in different countries form very differ- National forest inventory · Sampling methods ·
ent understory types, each one has its own cost- Volume calculations
efficient monitoring design, and they can hardly
be compared. Therefore, the development of gen-
eral guidelines is a particularly complex issue. Introduction
This paper is a review of data collection methods
and consequently a selection of the best available There are many biodiversity definitions; the Ar-
methods for the set of indicators with an em- ticle 2 of the Convention on Biological Diversity
phasis on GV sampling methodologies in NFIs. (UNEP 1992) offers an objective and clear one:
As a final result, recommendations on GV defini-
...the variability among living organism from
tions and classifications, sampling methodologies,
all sources including, alia, terrestrial, marine
and indicators are formulated for NFIs. Different
and other aquatic ecosystems and the eco-
sampling areas are recommended for each life
logical complexes of which they are part;
form (shrubs, herbs, etc.). Inventory cycles and
this includes diversity within species, between
species and of ecosystems.
The quantification of biological diversity is an
important objective in the assessment of nontim-
I. Alberdi (B) · S. Condés · J. Martínez-Millán
ber resources in forest surveys (Groombridge and
ETSI Montes, Universidad Politécnica De Madrid,
Ciudad Universitaria s/n. 28040 Madrid, Spain Jenkins 1996). Forest inventories have principally
e-mail: IFNBiodiv@mma.es been aimed at estimating the standing volume
650 Environ Monit Assess (2010) 164:649–676
of wood in forests and for monitoring changes Ground vegetation has been identified as a
in growth. Nevertheless, supplemented with rel- specific target for the calculation of critical loads
evant measurements and observations (Newton or levels. It has been used to detect changes in
and Kapos 2002), forest inventories can also be a the ecosystem as air pollution, particularly nitro-
useful tool to estimate forest biodiversity. gen deposition, and climate change. These vegeta-
As most forest plant diversity occurs in the tion studies have the advantage of their low cost
ground layer, it is particularly important to sample comparing with analyzing air or soil chemistry
this community (Johnson et al. 2006). (Thimonier et al. 2003).
The ComMon project—Comparison and eval- Individual species can be very important indi-
uation of methods for monitoring of dead wood, cators of a size potential productivity, economi-
vegetation, epiphytic lichens, and stand structure cal value, wildlife forage, and shelter. Changes in
in European forests—has been carried out by composition and spatial arrangement of vascular
a consortium of people from Austria, Belgium, plants in a forest may indicate the presence of
Italy, Spain, and Sweden under the umbrella of chronic stresses such as discrete site degradation
the “European National Forest Inventory Net- (COST E43, technical report, 2005).
work” (ENFIN). The ENFIN comprises most of Ground vegetation in the surroundings of the
the European NFIs. Four determinant topics for forest stands could also provide information about
biodiversity estimation were defined (stand struc- the history of the place like natural forests in
ture, dead wood, ground vegetation, and epi- the area, harvesting intensity and methods, main
phytic lichens), and each member country was ecological alterations, etc.
the responsible for each one. This review of data
collection methods aims at identifying the best
available methods for the set of indicators. Can- Definitions of ground vegetation
didate inventory methods are selected as a final and its components
result. The candidate methods are evaluated in
terms of their costs and reliability in plot level To describe major terrestrial plant communities,
assessments. a definition of different life forms is needed
This paper is focused mainly on National Forest (Bonham 1989). Major life forms are usually des-
Inventories needs and limitations, and the classifi- ignated by “trees,” “shrubs,” and “grasses.” Also,
cations, data collection methods, and biodiversity “ferns” and “bryophytes” are sometimes moni-
estimation will be chosen based on them. tored. There are different classifications depend-
ing on the plant ecology needs and the objectives
of each inventory.
It is quite difficult to achieve a common defi-
Importance of the ground vegetation and its role nition for ground vegetation. The main problem
in the forest ecosystem is that “ground vegetation” is a vague expression,
and it may include many different life forms and
Ground vegetation information is a key parameter each project considers a different one.
for biodiversity. It can provide information about One of the clearest “ground cover” definitions
the forest types and structure. Each forest type that include life form concept (Hubbard et al.
usually has associated a specific understory. The 1998) is “all herbaceous plants and low growing
diversity of plant communities offers an opportu- shrubs in a forest or open area.” The main objec-
nity to efficiently collect data on the community tion is that not all the strata are integrated in the
that provides the structure and productive base definition. Also bryophytes, lianas, bigger shrubs,
for all other organisms (Johnson et al. 2006). Be- or even small trees (as some riparian trees) or
sides the distribution and indicator, species can tree regeneration could be considered as ground
be used to estimate site conditions like drainage vegetation. For this reason, most of the references
and fertility. They can be also applied to provide to ground vegetation are related to the different
information about the forest stage, maturity, etc. vertical strata under the tree cover.
Environ Monit Assess (2010) 164:649–676 651
Two points of view are usually chosen, the forbs, wildflowers and ferns”. Plants lignification is
botanical definition or a practical one, the aggre- considered to distinguish groups.
gation of different life forms into layers. The Australian Biocondition (Eyre et al. 2006)
The European projects BIOFOREST and defines shrubs as “woody plant multi-stemmed
FOREST BIOTA define layers according to from the base (or within 200 mm from ground
height and life forms. level) or if single stemmed, less than 2 m”. This re-
The FOREST BIOTA report (Granke 2006) port makes a differentiation between ground cov-
defines three different vertical strata (below er, where grasses, herbs, and forbs are included,
tree layer) based on height: shrub layer, herb and weed cover. For field purposes, it would be
layer, and moss layer. This criterion is practi- necessary to use trained personnel due to the need
cal for analysis and assessment purposes. The to distinguish weeds from native herbs.
BIOFOREST PROJECT (Smith et al. 2005) dis- Ecological Monitoring and Assessment Net-
tinguishes six different layers considering the work (EMAN; Roberts-Pichette and Gillespie
growing habits and also the height: large shrub 1999) provides accuracy in its definition based
layer, subshrub layer, bramble layer, graminoid on diameter at breast height and growing form
layer, forb layer, and bryophyte layer. criteria. Shrubs are defined in this document as
Referring to shrub, in BIOFOREST defini- “usually multi-stemmed woody plants less than
tions, they distinguish between large shrub layer 4 cm dbh with most of the stems originating at or
(“woody vegetation below the upper tree stratum near the ground. Saplings under 4 cm dbh will be
and in the 2–5-m height range”) and subshrub measured with the shrubs in the shrub and small
layer (“woody vegetation under 2 m tall. Such tree stratum. Shrubs are usually present in forests,
vegetation includes tree seedlings, small shrubs, they dominate in heath communities, they may
bramble and climber species are not included”); form the canopy in riparian strips in the ecotone
while in FOREST BIOTA, only one shrub layer between forests and alpine or arctic tundra, and
is defined (“ligneous, including climbers >0.5 m in bogs or other high-water-table communities.
height”). Shrubs may also be found scattered in large or
The FAO report (2005) defines shrub as small clumps in grassland communities”. For the
“woody perennial plants, generally more than herb layer, they use the term field layer vegetation
0.5 meters and less than 5 meters in height at (“comprising all herbaceous vegetation regardless
maturity and without a definite crown. The height of height, and all woody plants under 1 m in
limits for trees and shrubs should be interpreted height”).
with flexibility, particularly the minimum tree and The bryophytes and lichens are also consid-
maximum shrub height, which may vary between ered in some reports as a layer of ground veg-
5 meters and 7 meters”. Others life forms are not etation. Mosses and liverworts are considered as
mentioned. No allusion to any ground vegetation one layer in the BIOFOREST project (Bryophyte
life form is made when defining forest. layer: Mosses and liverworts while lichens are not
There are also many differences when compar- included) and in FOREST BIOTA and EMAN
ing herb layers definition; the FOREST BIOTA projects, mosses are considered together with
herb layer definition is “all non-ligneous and lig- lichens. In FOREST BIOTA the moss layer is the
neous <0.5 m height” but in the BIOFOREST “terricolous bryophytes and lichens”. In EMAN,
PROJECT, two different layers could be inte- this layer is called ground layer vegetation, and
grated in the herb layer: graminoid layer (grasses, it is defined as “layer comprising mosses, lichens,
rushes, and sedges) and forb layer (vascular herbs, and fungi growing on the ground, together with
excluding graminoids, climbers, woody species, or small trailing and rosette plants.”
ferns). The different strata and substrata considered
The Forest Terminology from the University in the detailed reports and its height thresholds if
of Florida differentiates between shrub layer and considered are described in Table 1.
herbaceous layer. The herbaceous layer is defined According to the different purposes when
as “all the non-woody plants, for example, grasses, defining ground vegetation, it is necessary to
652 Environ Monit Assess (2010) 164:649–676
describe the included layers. There are many vari- relations between the structure of standing mate-
ations between the considered ones; how they are rial and other species such as ground vegetation,
grouped and its thresholds. To be able to stan- insects, fungi, and mosses; Rondeux 1999).
dardized layers, it is necessary to analyze and com- Remote sensing techniques provide an efficient
pare also the NFIs definitions (see “Definition” in tool for assessing and monitoring forest biotypes
NFIs). A proposal of GV definition and structure and their structural diversity (Holopainen and
is at the end of this article (“Conclusions and Guangxing 1998). They propose indicators that
recommendations for NFIS”). are measurable directly from the images as frag-
mentation indexes and others when truth data are
available (rarity of biotopes, key biotopes, etc.).
Photointerpretation and geographic Also, a methodology for assessing and mon-
information systems itoring European forest biodiversity, using sat-
ellite remote sensing, has been developed as a
Forest biodiversity is a very complex concept; on part of the Forest Information from Remote
one side, it is not possible to measure all the forest Sensing Project (McCormick and Folving 1998):
components, and on the other, there are several determines indicators of forest biodiversity for
dimensions which may characterize it as genes, composition (identity, distribution and relative
species, structural aspects, or landscape compo- proportions of forest patches), structure (spatial
nents (Vanclay 1998). pattern of forest patches), and development (tem-
In order to ensure a good inventory in terms poral changes in forest composition and struc-
of precision, remote sensing provides relatively ture). The main objective of this study is to detect
cheap objective information in many inventories areas at high risk of deterioration.
to classify the different habitats or vegetation There are several studies related with ecosys-
types as a previous phase to sampling design. tem changes at large scales (e.g., Gould 2000), but
However, the use of remote sensing (Poso et al. they are usually applied for grasslands or shrub
1995) is an increasingly useful tool. As indirect land, not for forest (e.g., Qi et al. 2000).
measurements are needed, it is necessary to focus It is also very important that the available in-
on key variables and habitats in order to quantify formation on biodiversity be stored within geo-
and qualify biodiversity (for example, study of the graphically referenced databases if it is to be made
Environ Monit Assess (2010) 164:649–676 653
quickly accessible for mapping, analysis, or mod- pling areas are essential (Roberts-Pichette and
eling purposes. For this information to be really Gillespie 1999).
usable, it must also be integrated with a great There are a great variety of different shapes
deal of other information on environments, so- and sizes of the plots. There is not a unique size
cioeconomic conditions, types of natural resource, or shape useful to measure the cover vegetation.
potential risks of degradation, etc. Geographic Shape and size of the plots are fixed by the mea-
information systems can be keys to integrating surements, field works, data analysis, and costs
information with the desired degree of detail involved.
(Jeffers 1996). If the aim of the inventory is to delimit units
defined by plant associations, the plot size will be
conditioned by the minimal area. This minimal
area can be defined as the minimal area in which
Sampling design: field methods the qualitative composition (number of species)
has an adequate representation (Aguilo et al.
The first step for sampling design is always to 1992). Therefore, to analyze a homogeneous plant
define the different homogeneous strata. It is very community, the function relating the number of
useful to relate ground vegetation strata with for- species with the monitoring area should culminate
est types. There are European Forest types ap- in an asymptote. This minimal area must be de-
proved by the European Environmental Agency cided for each inventory, but there are indicative
(Barbati et al. 2006) which are appropriated for a values for temperate ecosystems areas (Ellenberg
European common reporting. and Mueller-Dombois 1967b) shown in Table 2.
The number of sampling plots and their sizes The Canadian Central National Agency for
will mostly determine the accuracy of the inven- Inventory and Monitoring, EMAN has prepared
tory. The main variable in NFIs is usually wood biodiversity monitoring protocols for terrestrial
volume so this inventory design normally prede- vegetation (Roberts-Pichette and Gillespie 1999).
termines the monitoring of other variables such as This protocol is recommended for intensive re-
ground vegetation attributes. search projects. There are for each layer two or
The plot features are defined for each inven- more sizes. They may substitute for one another
tory. To define correctly the location, plot num- or may be used together depending on the forest
ber, size and shape, or transects is essential. The ecosystem (Table 2).
location in the forest will depend on the inven-
Small tree and shrub layer:
tory method (systematic, stratified, etc.). To mon-
itor long-term changes in plant biodiversity in 5 × 5 m (25 m2 )
different ecosystems, permanently marked sam- 2 × 2 m (4 m2 ) for densely packed shrubs
Ground vegetation (all herbaceous vegetation and In the same way, if the study includes phyto-
all woody plants under 1 m in height, mosses, sociological grasslands data is recommended a
lichens and fungi growing on the ground, together plot size around 100 m2 (Dierschke 1994; Chytrý
with small trailing and rosette plants): and Otýpková 2003; Dulamsuren et al. 2005) be-
cause a standard plot size was preferred for both
1 × 1 m (1 m2 ) woodlands and grasslands to ensure unlimited
0.50 × 0.50 cm (0.25 m2 ) or 0.25 × 0.25 cm comparability in statistical analyses (Dulamsuren
(0.0625 m2 ), smaller quadrats for numerous et al. 2005)
and densely packed individuals.
• In the second case, the study concentrates
If the aim is to measure quantitative variations on population dynamics (expansion or regres-
of the present plant species, the minimal area sion) on a smaller area. Small sampling units
concept is not usually used. Instead, in the esti- (in general fewer than 10 m2 ) are used for a
mation of variables such as number of individuals, more accurate estimation of species cover.
abundance, frequency, cover, height, diameter,
and biomass, the sample size is decided follow-
ing traditional inventory methodologies depend- In these studies, it is normal to use subplots,
ing on characteristics as the distance between the especially in surveys of ground-bryophytes and
individuals, their size, or the density (Aguilo et al. ground-lichens. The shape can be different circles
1992). Oosting (1956) determined in 1956 some (Mäkipää and Heikkinen 2003; Hokkanen 2006)
recommendations: or squares (Saetre 1999) with a surface around
1–3 m2 (Ford and Newbould 1977; Kühlmann
et al. 2001).
Shrubs h < 3 m: square plots of 4 × 4 m Circular plots are usually cheaper than rec-
(16 m2 ) tangular ones. However, it should be noted that
Herbs layer: square plots of 1 × 1 m (1 m2 ) rectangular shapes allow more species to be found
(Stohlgren 1994).
Usually, when monitoring different life forms,
The Expert panel on Ground vegetation assess-
plots of different sizes are nested.
ment (Dan Aamlid et al. 2002), in the “Manual
Permanent plots are recommended for use in
on methods and criteria for harmonized sampling,
plant communities where no obvious vegetation
assessment, monitoring and analysis of the effects
gradients are present, but where vegetation gradi-
of the effects of air pollution on forest. Part VIII.
ents are obvious, permanent transects are recom-
Assessment of ground vegetation” defines a mini-
mended (Roberts-Pichette and Gillespie 1999).
mal area of 400 m2 to achieve the comparability
Sometimes, transects are designed as a comple-
of results between countries. They describe two
ment to the plots (Kupferschmid and Bugmann
different sampling designs that could be used for
2005). Transects can establish plots along them or
monitoring ground vegetation in Europe. These
to use only the width.
two cases lead to a more qualitative or quantita-
The EMAN protocol on ground vegetation rec-
tive characterization:
ommends the following permanent transect di-
mensions:
• In the first case, the dynamics are assessed by
monitoring changes in the species composition Transects organized as contiguous 5 × 5-m
of a large number of species over a large area, plots (when trees, small trees, or large shrubs
utilizing sampling units around or greater than are dominant)
100 m2 , with a low to medium accuracy in Transects organized as contiguous 1 × 1-m
estimates of changes in cover for each of these plots (when low-shrub and ground vegetation
species. dominate)
Environ Monit Assess (2010) 164:649–676 655
2002), for instance, Swiss NFI has an independent others life-forms are not. The recommended scale
inventory for ground vegetation. is in Table 8.
Cover
Frequency
Cover is determined by projecting aerial parts
Frequency describes the distribution of species in of vegetation onto the ground (foliage cover) or
a community and is a useful index for monitoring by vegetation in contact with the ground (basal
changes in vegetation over time and comparing area). It can be calculated for all of the existing
different plant communities (Bonham 1989). Fre- vegetation for determinate layers or groups or
quency is the percentage of species present in a for each species. Canopy coverage of species life
sample unit. It is influenced by size and shape forms is useful to indicate the amount of sunlight
of sample units also sensitive to abundance and interception (Bonham 1989).
pattern of plant growth (Bonham 1989).
Size (height, basal area) and biomass
Abundance and density
There are several dimensional factors as height,
Abundance is generally referred to an estimation thickness, or weight that can be measured of each
of the present species; it is usually expressed in individual or estimated as averages of a group
relative numbers, as rare, seldom, frequent, or of individuals. Vegetation biomass is the weight
abundant species. of plants per unit of area, express in dry weight,
Density can be defined as the number of species kilocalorie, or in carbon grams (Gounot 1969).
per unit of area (see Table 3). That attribute Biomass indicates the quantity of resources as wa-
requires that individuals be countable (Bonham ter or nitrogen (Thimonier et al. 2003) used by a
1989). Woody species are easily counted while species in the community and so how much of the
communities resources are tied up with different Line intercept is most useful for open-grown,
species. It also indicates the forage available for woody vegetation while point intercept is
animals. Browse is sometimes measured if large more useful for pastures and grasslands.
herbivores are present. Another very important These methods are much more efficient that
fact to determine this attribute is to know the charting methods and as accurate as them.
quantity of combustible in case of forest fire.
Shrub biomass is usually estimated from di- Areas
mensional analysis while herbaceous biomass is
frequently measured clipping or guessing amounts Plot
of biomass (Bonham 1989). Biomass of other life
forms is not usually monitored. Areas are commonly used to estimate species
richness, frequency, density, cover, and biomass.
For long-term monitoring of plant species diver-
sity circular, quadrangular, or rectangular plots of
Methods for measure the different attributes
given areas (see “Sampling design”) are the most
inside the plots
used and recommended areas. A minimal area
must be determined depending on the inventory
All the composition and structure attributes can
objectives but the smaller the sampling area, the
be estimated by plots, some of them also by lines
higher the accurate estimation. It is also a useful
(as line intercept method) and others by points (as
process to divide the plot into smaller subunits.
point frames) too. Points are considered to be the
most objective way of estimation while areas are
Scales or class methods
often biased (Bonham 1989) but all variables can
be measured by plots, and they are considerate the
Abundance and density There are several abun-
optimal cost-efficiency methods. Line transect is
dance classifications and they usually correspond
also a very used method and adequate for some
with density values. In Table 3, some frequent
variables. Plots and line intercept are the most
scales are shown (Shimwell 1971).
commonly used methods in the large-scale inven-
tories. The methodologies are described below.
Frequency The most common methods for fre-
quency estimation are counting individuals into
Line: line intercept nested plots or complementary plots (Bonham
1989). Frequency data usually follow the Poisson
This method is mostly used to estimate vegetation or binomial distribution.
cover, but it is also used some times for frequency
data collection. It can be obtained from a line Cover scales Cover range comprises generally
placed to contact plants. If basal cover area is values from 0% to 100%, and they are arbitrarily
needed, then the line is placed at ground level divided into a number of categories, and each cat-
(Bonham 1989). The length of each intercepted egory is assigned a rating or scale value (Bonham
plant i part is measured. 1989). As they are visual estimations it is neces-
sary to have trained technicians to avoid bias. The
di most used ones are shown on Table 4. In all these
Percentcover = × 100
length scales, it is important to decide about excluding or
including, major heterogeneities (big rocks, paths,
In general, cover in herbaceous communities can water streams, cliffs, fences, etc.) and as well the
be estimated with short lines (less than 50 m), global cover of bare soil, litter, and other elements
while long lines (more than 50 m) should be used of the surface.
with shrubs. Some methods also take into account the num-
Bonham (1989) elaborates several conclusions ber of individuals of each species, in addition to
between the monitoring cover methods: the area occupied by them, to obtain the “species
658 Environ Monit Assess (2010) 164:649–676
magnitude” (Braun-Blanquet 1932) or species sig- a small unit of the plant (e.g., a small branch) as a
nificance (Bonham 1989). reference, clip, dry, and weigh it and estimate the
There are some studied transformation be- number of the references that form the shrub.
tween scales and percentage for the estimation To estimate shrub biomass from dimensional
of species cover. There is a well-known trans- analysis, crown diameter has been used with not
formation between Braun-Blanquet and Domin- bad correlations, but crown volume is considered
Krajina scales. The Expert panel on Ground an adequate predictor of the total leaf biomass
vegetation assessment (Dan Aamlid et al. 2002), (Bonham 1989). To get the volume–weight re-
in the “Manual on methods and criteria for har- lation is necessary to establish the crown shape
monized sampling, assessment, monitoring and (conical, spherical, etc.) and to measure at least
analysis of the effects of the effects of air pollu- one diameter (two in irregular shapes) and height.
tion on forest. Part VIII. Assessment of ground The European FORSEE project (2004–2007) is
vegetation” proposed a transformation between working in this way. Porté et al. (2005) in the
Braun-Blanquet, Braknam, Schmidt, and Londo project “Détermination de la biomasse aérienne
scales and the percentages for the estimation of du sous-bois de peuplements adultes de Pin mar-
species cover (Table 5). itime: contribution à la quantification des stocks
de carbone forestier à l’aide d’indicateurs de
couvert” made biomass measurements per spe-
Biomass (height, diameter) Biomass is consid-
cies group (woody species, fern, herbaceous
ered by several authors as a primary vegetation
species, and mosses). They collected total aerial
measure (Bonham 1989; Somogyi et al. 2006).
living biomass for a small number of samples.
Tree and shrub biomass is usually estimated
In a high number of samples and also in the pre-
from dimensional analysis (indirect method).
viously described small number of samples, they
Through other measures such as total height,
calculated a volumetric index per species group
DBH, basal area, or crown diameter, it is possible
(IFN estimation) with the following equation.
to predict biomass from regression equations. But
shrub biomass is sometimes estimated by the “ref-
erence unit technique.” It consists in considering VI= % cover × height
660 Environ Monit Assess (2010) 164:649–676
And finally, they calculate total biomass by a rela- used to calculate a regression to estimate the large
tion VI-dry weight. sample biomass.
In the same project, Silva et al. (2006) deter- For National Forest Inventories (due to the
mines the forest shrub biomass with the following costs and the extension), only nondestructive
formula: methods are recommended (See “Attributes
measured” and “Conclusions and recommenda-
Bj = δb s × Pcsi × Ai tions for NFIS”). Somogyi et al. (2006) point at the
i
factor that forest inventories can provide repre-
Where B j is the shrub biomass in plot j (Kg/m2 ), sentative dimensional data such as volume, height,
δbs is the apparent density of the s specie (Kg/m3 ), or diameter, but the biomass factors or equations
Pcsi is the coverage of the specie “s” in the height used are in most cases not representative because
class “i,” and Ai is the height of class “i.” they are based on local studies.
Anyway, to measure herbaceous or mosses bio-
mass, the most frequent methods are to clip or
to harvest (destructive methods) or guess amount
of biomass in quadrats (indirect method; Bonham Areas: mapping and charting methods
1989). In the destructive methods is to weight and
dry the vegetation is needed. In large-scale sur- Cover Plant cover is determined by drawing to
veys, a few samples of each species can be dried; scale the outline of the crown or basal areas of
the “weight estimates and double sampling” is plants on a sheet of graph paper. Charting or
one of the most common used methodologies. In mapping may be done with a grid quadrat or
this method, the visual method is combined with a pantograph. This method is used successfully
the destructive method. There is a large sample into grasses communities (Bonham 1989), and it is
that contains only observations and a small one less efficient than intercept techniques (Bonham
that contains clipped weights. The small sample is 1989).
Environ Monit Assess (2010) 164:649–676 661
Areas: photographic methods some of the species. These two conditions are not
always possible in large-scale inventories. Species
Cover Photographic techniques based on verti- list with a short number of them are usually used
cal stereophotography are objective, rapid, and in NFIs.
does not need a trained field worker, but they With floristic composition, there are several
require a later analysis. A software program can indicators or factors that can be deduced as the
be used to obtain the covers. This method is not following ones (8.1.3, 8.1.4, 8.1.5).
suitable when vegetation has several layers ex-
cept to determine dominant species composition Endemic species, introduced species, key species,
(Bonham 1989). threatened (extinct, endangered, rare, and vulner-
able) species Taxonomical studies are needed to
determine presence of certain species that must be
Data process recognized for its meaning. Those data could be
used for example to protect certain areas. It must
Ground vegetation biodiversiy indicators
be noted that for threatened species, inventories
There are three basic indicator functions: sim- must be design in a different way; plots or tran-
plification, quantification, and communication. sects must be normally located be deliberated.
Indicators generally simplify in order to make
complex phenomena quantifiable so that infor- Species richness There are many indices based
mation can be communicated (Delbaere 2003). on species number and its abundance. All these in-
Biodiversity indicators support communication dexes (e.g., Margaleff, Menhinick, Berger-Parker,
about the state of biodiversity in a selected region. Simpson, and Shannon) are commonly used, but
The target group for biodiversity indicators con- they have been highly criticized as they heavily
sists of two groups: those providing the data on depend on plot area. The ICP FOREST experts
the indicators and those making policy decisions (2003) recommend, in addition to species number,
on the basis of the message expressed by the evenness index (Pielou 1969) because it is almost
indicators (Delbaere 2003). unbiased by different sampling areas.
There are several institutions defining biodi-
versity indicators as European Topic Center on Ecological succession To estimate forest biodi-
Nature Protection and Biodiversity (ETC/NPB). versity status is essential to know forest natural-
But, it is necessary to define the indicators each ness. When there is enough information about
project can provide and the reliability. The pro- vegetation, succession phase is very important to
posed selection indicators have been selected know how far the current forest is to the potential
considered large-scale inventories. vegetation. This is also related with the stability
degree.
Composition Ecological sequence or natural succession can
be defined as the dynamic process of coloniza-
Forest types The identification of forest types tion of a virgin biotope by living organisms that
depending on species composition is the first in- in progress increase their biomass. At the same
dicator, and all the rest will be conditioned by this time, by autoregulation, mechanism and control
classification. That is why it is so important to have recourses get a higher degree of complexity in
a standardized classification. Ground vegetation is their structure. The final process culminates in
directly related with forest types. stable equilibrium in the biotope conditions, the
climax. That vegetal component is called poten-
Floristic composition Ground vegetation studies tial vegetation. The potential vegetation would be
are based on the analysis of the determination forest evolved as a sequence of natural succession
of all the present species. Therefore, to make in a relative large period without anthropogenic
complete monitoring is necessary to have experts influences (Aguilo et al. 1992). It is very important
and to go in certain season periods of the year for to realize that climax stage of a natural forest
662 Environ Monit Assess (2010) 164:649–676
ecosystem is not constant but a mosaic of different vide complementary information (Maurer 1999;
phases consisting of different plant communities, Walker 2005). What are needed are coordinated
different species of flora and fauna as well as programs that simultaneously examine communi-
hanging soil development stages (Schuck et al. ties from multiple scales (Maurer 1999).
1994). Climax stands could have natural or an-
thropogenic disturbances suffering degradation or Structure
regression stages.
Ground vegetation is a key component to de- Number of layers There have been many pro-
termine the succession stage and to be able to posals to classified vegetation. Raunkiaer (1934)
define how close is to the climax vegetation. defines five categories (phanerophytes, chamae-
To consider the development of the succession phytes, hemicryptophytes, cryptophytes, and tero-
theory, it is important to differentiate between the phytes) from which many studies used them.
holism and the reductionism. Walker (2005) gives Danserau (1957) divide biotypes into six cat-
a good description of both in the article “Margalef egories: trees, shrubs, herbaceous, bryophytes,
and ecological succession”: epiphytes, and lianas (of course, trees and epi-
phytes are not a part of ground vegetation).
...Holists focus on changes in diversity, pro-
Ellenberg and Mueller-Dombois (1967a) devel-
ductivity, biomass, nutrient cycling efficiency
oped Raunkiaer classification. Küchler (1967)
and other ecosystem characteristics as well as
made a classification based in the main physiog-
the general directionality and predictability
nomic characteristics and a subdivision depending
of succesional trajectories that end in a sin-
on height and cover.
gle climax. Reductionists emphasize distur-
There have been also classifications based on
bance, stochasticity, species life histories and
height as the one proposed by Godron et al. (1968)
species interactions, believing hat succession
in ten different classes (six of them can be con-
is a largely unpredictable consequence of
sidered form by GV) or the one proposed by ICP
each species’ unique interactions, with its
experts (see “Photointerpretation and geographic
abiotic and biotic environments (Gleason
information systems”).
1926; Glenn-Lewin et al. 1992). The two
approaches can be integrated, sequentally Sociability of each group of species or each species
or simultaneously, as when one begins by Qualitative and descriptive aspect are derived
focusing on particular species responses but from vegetation pattern. The most popular clas-
ends by integrating the details into a general sification is the one establish by Braun-Blanquet
energetic framework (McIntosh 1985).... (1932):
There is, therefore, a story of two competing 1. Species growing solitary
research traditions, holistic, and reductionistic. 2. Species forming clumps or dense groups
The holists believe that ecological systems exhibit 3. Species forming small patches or cushions
order, structure, and regularity at population, 4. Species growing in small colonies
community, and ecosystem levels of organization 5. Species growing in large, almost pure stands
while reductionists believe that ecological systems
are nothing more than assemblages of individual Cover of each group of species or each species It
species populations whose behavior is primarily is one of the most indicative measurements of veg-
determined by response to local environmental etation structure. Due to its estimative character,
conditions (Odenbaugh and de Laplante 2006). a learning period for the technicians is needed.
As Maurer (1999) suggests, holistic studies This estimation is cheap and very useful accepting
might be used to design specific management that it will never be exact measurement.
plans while reductionistic focus might suggest how
to apply the experimental results to a wider group Biomass of each group of species or each species
of organism. The two approaches contribute infor- This is an expensive and no realistic parameter
mation about the communities; in fact, they pro- for large-scale inventories with a direct method
Environ Monit Assess (2010) 164:649–676 663
but due to the needs of studding carbon pools, DCA is supposed to be an efficient ordination
it would be a very interesting indicator. It should technique when species have bell-shaped response
be calculated with dimensional analysis and estab- curves or surfaces with respect to environmental
lishing functions of dry weight. It could be very gradients and is, therefore, more appropriate for
useful in future to use “Forsee projects” results. analyzing data on community composition and en-
vironmental variables than CCA (ter Braak 1986).
Calculation of the variables, including statistics It is important to consider that unlike PCP and
estimations CA, DCA does not produce the arch or horseshoe
effect. Anyway, there are many authors against
The variables used can be directly the cover val- this method; Palmer (1993) indicates that CCA is
ues, values from any scale, biomass influence po- immune to most of the problems of DCA and for
tential (Kuuluvainen and Pukkala 1989; Økland instance, Wartenberg et al. (1987) recommends
et al. 1999; Saetre 1999), ground vegetation pro- reporting the arch unscaled in two dimensions,
duction (Ford and Newbould 1977), gross pho- even though it is a one-dimensional form.
tosynthetic production (Kolari et al. 2006), and At present, the importance in some surveys
carbon balance (e.g., Goulden and Crill 1997; Law of the ground vegetation is developing software
et al. 1999). programs (BioCalc software) to facilitate the cal-
If the data are in ranges, majority of the times, culation of the variables; also it is possible to use
it is necessary to convert them in unique values general vegetation computer programs [PC-Ord
(e.g., the average of the range). If measurements 4 (McCune and Mefford 1999)]. In other cases,
are not in the appropriate form for the statistical the proper researchers develop their own software
analysis, they will be adapted. (Evans et al. 2006).
Usual statistic analysis like ANOVA (Zenner
et al. 2006; Zobel 1998) and correlation studies Model chains for assessing impacts of biodiversity
can be applied over the pieces of information from
the field works. Each survey must decide which Nitrogen (N) and sulfur are the main pollutants
analysis is better to reach its own aims. causing acidification, eutrophication, and changes
Anyway, when multiple measurements are in biodiversity. Sulfur deposition can be quantified
made, there are often correlations among the with geoquemical models. But the majority of N
measurements. It is this dependence that differ- transformation processes are biologically medi-
entiates multivariate from univariate analysis, in ated (Rowe et al. 2005).
which is assumed that the observations are inde- Rowe et al. (2005) indicates that estimations of
pendent one from another. Unless the homogene- N availability are needed as an input for biodiver-
ity of treatment differences variance assumption sity modeling and that to predicting responses to
is met, one should turn directly to multivariate nitrogen pollution is better divided into two parts:
procedures (Gurevitch and Chester 1986).
Ordination methods are widely used in ecology Predicting changes in N availability as a con-
for gradient analysis or the study of species disyti- sequence of N deposition and soil and plant
butions along gradients. Some of these analyses processes
are: detrended correspondence analysis (DCA; Predicting changes in species composition as a
Hill and Gauch 1980); Spearman’s Rank Corre- consequence of this level of N availability
lation Coefficient (Scott 1970); principal compo- There are some methods for predicting soils, wa-
nent analysis (PCA; ter Braak and Smilauer 1998; ter, and plant responses to N pollution. Some
Zobel 1998), and canonical correspondence analy- chains also include a model of vegetation succes-
sis (CCA; ter Braak 1986). sion. There are four main model chains mentioned
PCA provides solution to the multidimensional by Rowe et al. (2005):
linear ordination problem if the errors are inde-
pendently and normally distributed with constant 1. FORSAFE-VEG
variance across species and sites. 2. SMART2-SUMO-MOVE-NTM
664 Environ Monit Assess (2010) 164:649–676
Fig. 1 List of countries assessing the different ground vegetation life forms
be considered as GV group by consensus with graphical region (Table 6). As height appears as
the COST E43 experts. e.g.: Germany con- the most common criterion used to differentiate
sider them as “sample trees dbh < 7” cm or the strata, it should be the major parameter, but
Romania “small, perennial, woody plant, with it could not be enough. Maybe also the main bio-
7–15 m height at maturity.” In some others logical characteristics could be added like growing
countries, the concept is not clear. parameters, ligneous or not, etc.
• Shrub layer. Shrubs attributes are measured Different definitions on NFIs and its thresholds
in every country, but the definitions are also are shown on Table 7.
different. The criteria used are based on height
mostly, on a species list or if it is ligneous or – Herbaceous layer: this layer is not been as-
not or a combination of them. It is also impor- sessed for every country. For most of the
tant to distinguish between the ones based on countries the definition could be the same
potential height (e.g., France, Romania) and as given by Germany NFI “herbaceous seed
the ones based on real-present height (e.g., plants (nonwoody or only woody at the base
Austria, Belgium, Germany, and Italy). of the shoot)” but there are some countries
that include only the “nonwoody species” as
The harmonized definition would imply an agree- France or Austria. There are also some coun-
ment on the threshold or a complete species list. tries that subdivide this layer into:
There could be some species determined as shrubs
in some countries and in other layers in others. • Grass and herbs: Austria, Germany, and
Also, in some cases, the same bush species could Ireland
have different height depending on the biogeo- • Forbs, graminoids: Estonia
666 Environ Monit Assess (2010) 164:649–676
– Terrestrial liverworts and mosses: Both lichens and bryophytes form all together
classes, when measured, are usually grouped a group. In Germany and UK, the group
into the bryophyte layer or even form a is formed by bryophytes species. Belgium
unique layer with lichens, generally recorded also records some terricolous bryophytes,
as a group for cover measurements (Austria, especially indicator species. Czech Republic,
Belgium, Germany, Spain, and UK). In Spain, Sweden, Slovakia, and France are determining
several of this life-form species.
Fig. 4 Countries 16
assessing GV cover and
its exhaustiveness 14 Cover by GV groups
Cover by GV sub-groups
12
Cover by GV species
10
No Countries
8
0
YES YES YES YES YES YES
Year seasons Bushes and shrubs have been measured for longer
series but in many countries, the first survey is still
In most of the countries, there is not an intensive in progress for nonwoody species, mosses, lichens,
ground vegetation-monitoring program because and liverworts. There are only five countries that
it would need several visits per year. Another indicated they had a ground vegetation inventory
important datum related with it is if the period of finished cycle: Czech Republic (finished in 2004),
the year is fixed or not. In Austria, Belgium, Czech France (2005), Germany (2002), Slovak Republic
Republic, France, Germany, Spain, and Sweden, (2006), and Sweden (2002).
there is not a fixed period, while in Estonia,
Italy, Norway, Romania, Slovak Republic, and Attributes measured
Switzerland, there is (Fig. 2).
Sampling biodiversity on NFIs is a relatively Within the countries that assess each GV classifi-
new issue; the available data for ground vegeta- cation (bushes, ferns, mosses, etc.), the attributes
tion depends on the country and on the life form. measured are the ones shown in Fig. 3.
The coverage gets the higher value on every height at maturity and without a definite crown.
life form followed by occurrence. Coverage and The height limits for trees and shrubs should be
occurrence get the same percentage sampling in interpreted with flexibility, particularly the mini-
liverworts, as cover is the most used parameter mum tree and maximum shrub height, which may
is necessary to study the degree of each NFI vary between 5 meters and 7 meters” (FAO 2005).
sampling (Fig. 4). And also woody non perennial plants, between 5
Next step is to know each country used cover and 7 m approximately.
scale and to propose a unique one. Most of Herbs: nonwoody vascular plants excluding
the countries are using Braun-Blanquet scale or ferns.
Braun-Blanquet modified scale. NFIs cover scales Ferns: Pteridophyta species
when used and proposed scales are shown in Bryophytes: Nonvascular, terrestrial green
Table 10. plant, including mosses, hornworts, and liverworts
(National Vegetation Classification Standard
1997, Vegetation Classification Standard).
Conclusions and recommendations for NFIS
The first step is to get an agreement of ground The recommended sampling plot area by ICP For-
vegetation definition and its components. The ob- est Expert Panel is S > 400 m2 (Granke 2006).
jective is that the most representative networks And by its recommendations, it could be com-
would be able to report and be comparable. posed by different subsamples (subplots). The
The proposal for ground vegetation definition problem in NFIs is the very high costs due to the
is a very simple one: “all types of no epiphytic high number of plots sampled in each country.
vegetation life forms living under the tree layer.” Thus, exhaustive studies should be made on each
Ground vegetation components could be struc- forest type to determine the minimal area of each
tured by the following double classification: one. The ICP forest plots are a very good possibil-
ity to test those minimal areas.
Moss layer (terricolous bryophytes and lichens) The ICP proposed area could be adopted in
• Terricolous bryophytes and NFIs for determining the cover of each one of the
• Terricolous lichens proposed components of GV, but it is not possible
for determining GV composition. That is because
Herb layer (all non-ligneous, and ligneous < 0.5 m of the high cost, the high number of species that
height) could be expected (what would mean the need
• Regeneration/Plantation (trees) of very specialized teams), and the difficulty of
• Herbs having a reliable sample.
• Shrubs/no perennial As it was exposed in this paper, for each GV life
form, there are different size recommendations.
Shrub layer (only ligneous, incl. climbers) >0.5 m If for each life form or layer sizes would be dif-
height ferent, costs could be reduced. Only Sweden has
• different sizes determined for different studies.
Regeneration/Plantation (trees)
• The average sizes for monitoring shrubs of 13
Herbs
• European countries (Austria, Belgium, Cyprus,
Shrubs/no perennial
• Czech Republic, Estonia, France, Germany,
Climbers
Lithuania, Norway, Romania, Slovakia, Spain,
Life-forms categories included and its defini- and Sweden) is 317,09 m2 with a standard devi-
tion could be the followings: ation of 193,32 what gives an idea of the great
Shrub: “woody perennial plants, generally variation. For other life forms, standard deviation
more than 0.5 meters and less than 5 meters in gets higher (less countries assessing them).
Environ Monit Assess (2010) 164:649–676 671
It would be necessary to maintain same sizes by Levels and approaches are based on the differ-
same forest types all around Europe. The great ent NFIs exhaustiveness.
influence by different climates and habitats in As the majority of NFI are working with species
optimal plot sizes is obvious. list which contain only partial species, it would
necessary to homogenize national lists.
Inventories cycles and year seasons To codify the different species, it could be pos-
sible to use ICP codes related to Flora Europaea.
It is very important to consider inventories cycles. They have 12 digits in three groups (separated by
The NFIs cycles used are 1, 5, 10, and 12 years dots) meaning the family the first group, genus the
what will detail vegetation composition and dy- second one, and specie the third one.
namic in different scales.
It is important also to notice that some coun-
tries as Belgium, Czech Republic, France, or Spain Herbs and bryophytes: indicator species The ob-
sample all the year round while others as Estonia, jective would be to determine indicator species
Italy, Romania, and Slovak Republic samples in for each forest type or try to create standards at
a fixed period of the year (in different months, European level. Each country or/and each bio-
respectively). geographical region could have their own species
It is unrealistic to impose a standard NFI cycle. indicators; they maybe will not be the same.
There is too many information that would be First question to answer in NFIs would be: what
loss for every country. Comparisons would not be species we would like to find and which ones we
possible. And of course, NFI are conditioned to would not like for each FT? Species lists have also
many others variables. great variations related to the number of selected
species, and in some cases relates just genus while
Attributes measured and proposed indicators in others is at species level. Coordination with ICP
forest would be extremely useful to determinate
Main parameters used to assess ground vegeta- the searched species list.
tion are dominant or common species identifi- It is not possible to use richness indicators as
cation, diversity indices, and the ground cover. number of species, evenness index, or Shannon
Nevertheless, there are many differences between index as lists are not reflecting the real richness.
countries selected species criteria, e.g., Germany
record particularly important forest plant species Ground vegetation structure
which cause forest management problems.
Cover is a widespread measured attribute and a
Ground vegetation composition good structure descriptor. The proposed indica-
tors related to cover are the followings:
It is obvious that there woody species can be
recorded in a more intensive way than nonwoody Indicator 1: GV class and subclass defined (see
species. Woody species do not have season moni- “Definition”) cover
toring problem. Indicator 2: Bare soil and litter cover (GV ab-
sence)
Indicator 3: Shrubs genus or species average
Woody species Proposed composition indicator cover.
would be comprised by two different levels:
• There are several cover scales. Taking into ac-
Catalog of the present shrubs species or/and
count NFIs used scales and the utility of using
genus by forest type.
• more detailed ranges in low coverage, the pro-
Probability of finding each species/ha.
posed cover classes for harmonization are the fol-
And it will contain two approaches: (1) genus; (2) lowings: <1%, 1–5%; 5–10%; 10–25%, 25–50%;
species. 50–75%; 75–100%.
672 Environ Monit Assess (2010) 164:649–676
But there are some advantages using Braun- quirement of specialist technicians in NFIs. To
Blanquet lower classes classification due to the have specialized teams would increment costs and,
description of species magnitude. It is possible to therefore, it is important to reduce and to study
determine rare species and sparsely and seldom the optimal plot number and area to reach the
species (both with cover smaller than 1%). So the marked objectives.
proposed scale would be: r, +, 1–5%, 5–10%, 10– To determine all GV species are not possi-
25%, 25–50%, 50–75%, 75–100%; but the ade- ble in large-scale inventories. Species list (with a
quate one for harmonized would comprise the first short number of them) are usually used in NFIs.
two classes into one (<1%). Species GV lists should be revised and homoge-
nized. The criteria to elaborate plant list depend
Indicator 4: Sociability classes
on the objectives; they can be chosen because
Only Belgium is recording sociability and dis- they are the most frequent ones, or rare plants,
persion of each species. Belgium is using Braun- or key species. Again, different biodiversity NFIs
Blanquet scale (see “Areas: mapping and charting objectives should be defined. In ICP plots, where
methods”) and is the one proposed. They also add intensive soil and climate variables have been
one useful class: Individuals unnaturally distrib- monitored, plant responses to them could be an-
uted (plantation). This last one is generally not alyzed and consequently elaborate species selec-
very frequent for shrubs and no woody species. tion by established criteria and ecological factors.
Ground vegetation dynamic: Elleberg indices Acknowledgements This work was performed within the
ComMon project funded (75%), by the European com-
mission through the Forest Focus program. The COST
In future, it could be useful to use indices as E43 forest biodiversity (WG3) network provided valu-
Ellenberg’s with of course Levels I and II network able input to understand the National Forest Inventories
studies collaboration. In ICP, plots greater moni- methodologies. We thank Jose Antonio Villanueva re-
toring intensity is possible, and they could deduce sponsible of the Spanish NFI for all the provided data
and for his inestimable suggestions, and Cristina Viejo and
indicator species attending to common criteria. Sebastian Montoya for their very helpful assistance in the
Besides, this kind of indices allow not to having data analyses and Aitor Gaston for his useful comments.
to measure all present species. But once again, We are particularly grateful to ComMon members Anna-
the main step would be to define common NFIs Lena Axelson, Elmar Hauk, Jacques Rondeux, Cristina
Sanchez, and Thomas Puissant reviewers for their helpful
objectives. observations on the manuscript. And also to all the COST
E43 members remarkably to Erkki Tomppo (chairman
General indications and recommendations of the Action), Gherardo Chirichi (leader of the WG3
network), Susanne Winter (deputy leader of the WG3
network), and to all the WG3 participants, especially to
In the last years, there is having a change in NFIs the members of the Ground vegetation subgroup, András
objectives. Society demands other kind of request. Szepesi, Paulo Godinho, and Loizou Lizos who provided
It is necessary to adapt them to new requirements. extremely helpful ideas of harmonization.
Therefore, reliable investigations are needed to
determine minimal number of sampling plots and
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