Pedobiologia 50 (2006) 347356

Soil formation on green roofs and its contribution

to urban biodiversity with emphasis on
Collembolans
Stefan Schrader
a,
, Matthias Boning
b
a
Institute of Agroecology, Federal Agricultural Research Centre, Bundesallee 50, D-38116 Braunschweig, Germany
b
Institute of Zoology, Technical University, Spielmannstrasse 8, D-38106 Braunschweig, Germany
Received 11 April 2006; received in revised form 22 June 2006; accepted 27 June 2006
KEYWORDS
Green roof;
Collembola;
Soil formation;
Urban biodiversity;
Succession
Summary
In urban areas, green roofs are part of the so-called environmental green lung
providing important environmental, economic and technical advantages compared
to conventional at roofs. We hypothesised that soil formation occurs in the
growing medium of extensive roof greening, and that the successive development in
the growing medium promotes urban biodiversity and counters habitat loss. To
demonstrate this, we selected 10 representative green roofs of two different age
classes within the inner urban area of Hanover (Germany). Old roofs were
constructed between 1990 and 1994 and young roofs between 1998 and 1999.
During summer 2002, the roofs were sampled to determine abundance and species
diversity of collembolans and to measure selected soil properties. Discriminant and
cluster analyses, considering abiotic properties only, separated the growing media of
the roofs into the groups young roofs and old roofs. The results indicated a
more stable environment in the substrate of old roofs due to advanced soil formation
and improved niche occupancy of collembolans. In the mature growing media of old
green roofs, pH was lower, while C
org
and N
t
contents, as well as dehydrogenase
activity, were higher compared to young green roofs. The cluster analysis on the
substrate properties revealed young roofs to be more similar compared to old roofs,
which are characterised by increasing dissimilarities. The collembolan densities
were only slightly higher on old roofs (57,000 ind. m
2
) compared to young roofs
(55,000 ind. m
2
). Also, differences in species richness were small with 26 and 24
species on young and old roofs, respectively. However, differences became obvious
at the species level. Species diversity was highly dynamic over time, undergoing
successive development comparable to that occurring in extreme soil environments
ARTICLE IN PRESS
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doi:10.1016/j.pedobi.2006.06.003

Corresponding author. Tel.: +49 531 596 2514; fax: +49 531 596 2599.
E-mail address: stefan.schrader@fal.de (S. Schrader).
like newly reclaimed mining areas. We conclude that extensive roof greening
promotes urban biodiversity but does not replace nature.
& 2006 Elsevier GmbH. All rights reserved.
Introduction
During the last century, an extreme increase
in the urban:rural population ratio has occurred. In
1900, about 10% of the world population lived in
cities, whereas the present urban:rural ratio of
people is estimated to be 1:1, and it is predicted
that the urban population will reach 60% worldwide
by 2030 (Platt 2004). Many of the well-known
environmental problems in urban areas are caused
by loss of biodiversity and natural habitats, mainly
as a result of surface sealing through construction
measures, increased loads of heavy metals and
organics, and the emission of green house gases.
For this reason, concepts have been developed to
preserve, restore or even create green areas to
counter the negative environmental impacts of
rapid urbanisation (overview in Platt 2004). Pro-
gressive densication of the human population,
supportive infrastructure and the growing complex-
ity of cities have led people to look more closely at
buildings themselves and especially at their roof
surfaces.
Green roofs are part of the so-called environ-
mental green lung in urban and suburban areas.
They provide important technical, climatic, ecolo-
gical, economic and social advantages in residential
and industrial areas compared to conventional at
roofs. Ofce buildings, residences, hotels and
underground buildings are typical sites for estab-
lishing roof greening. The main benets of green
roofs include air and water ltering, thermal
buffering, storage and protective properties. They
give rise to a variety of urban evironmental services
like energy savings (Niachou et al. 2001), sound
insulation, life extension of roof membranes, water
retention (Bengtsson et al. 2005; Van Woert et al.
2005), mitigation of urban heat and solar radiation
(Kralli et al. 1996; Theodosiou 2003), and improve-
ment of air quality (Liesecke and Borgwardt 1997).
Furthermore, green roofs may be part of a larger
system of wildlife corridors in urban and suburban
areas, including park areas, gardens and grave-
yards, offering an environment for plants, birds and
invertebrates (Kim 2004). With this in mind, green
roofs may function as stepping stone habitats
connecting isolated habitat pockets with each
other to promote urban biodiversity (Kim 2004).
Finally, green roofs even have aesthetic value and
may serve as recreational islands in conurbations.
Roof greening has a long history from its
beginning in ancient times as roof gardens using
pure soil to todays technically well-developed and
diverse greening systems in urban areas throughout
the world. Osmundson (1999) presents a detailed
overview on the historical background. The great
stepped pyramid towers of ancient Mesopotamia,
built more than a millennium B.C., are commonly
assumed to be the beginning. The Hanging Gardens
of Babylon, whether they really existed or not,
seem to be the most famous example. Historical
roof gardening was primarily established for aes-
thetic reasons. At the end of the 19th and the
beginning of the 20th century, rooftops in major
cities of the US like New York City were gardened to
overcome the increasing land costs of the inner
city. In some countries with extreme climates, the
traditional style of architecture benets from the
insulation value of so-called sod roofs covered with
soil and growing grasses. In Norway, for instance,
sod roofs serve to retain building heat while in
Tanzania they keep buildings cool.
In the late 19th century, a German builder in
Berlin used vulcanised cement for the rst time as a
non-soil-derived growing medium for roof greening.
Nowadays, green roofs are characterised by a
stratied and mainly articial substrate (overviews
in Osmundson 1999; Peck and Kuhn 2004). In
principle, basic green roof construction consists of
two membranes, the rst a waterproong and the
second a root-proong membrane. These are
followed by another protective layer, a drainage
layer and a lter fabric. Finally, the growing
medium is spread out onto this technical substruc-
ture and is sometimes topped with a mulch layer.
Two green roof systems can be distinguished:
extensive and intensive roof greening (Osmundson
1999; Peck and Kuhn 2004). Intensive greening
applies to entire gardens with shrubs and small
trees like those found at ground level. It usually
involves a thick layer of growing medium of more
than 20 cm, and often 60 cm, which allows for the
development of a more complex and diverse
ecosystem. In contrast, extensive roof greening is
based on a thin layer of growing medium, generally
612 cm thick, and is restricted to a very limited
choice of herbaceous plants, mainly succulent,
alpine or drought resistant, and grasses. On the
other hand, extensive greening is less expensive
and time consuming to install and requires minimal
ARTICLE IN PRESS
S. Schrader, M. Boning 348
technical and horticultural maintenance later
on. Sedum species are the most common plants
used for extensive roof greening because of their
ability to withstand harsh environmental conditions
(e.g., extended drought periods) (Van Woert et al.
2005).
Normally, the substrate is colonised accidentally
by invertebrates depending on the exposure and
depth of substrate layers, as well as the distance to
the closest green areas (Frund 1996; Joger and
Vowinkel 1992; Klausnitzer 1992). In an urban
environment, invertebrates spread and settle ac-
tively by ying, or passively by air transport (e.g.,
ballooning of small spiders). Collembolans are
typical pioneer microarthropods in the primary
succession of virgin anthropogenic substrates like
those of newly reclaimed mining areas (Dunger
1989). They are introduced to these areas by
air transport during the pioneer period (Dunger
1989). It is likely that similar mechanisms are also
responsible for the spreading of pioneers in urban
areas.
In contrast to above ground invertebrates like
spiders and ground beetles, urban biodiversity of
below ground invertebrates has been neglected
(Klausnitzer 1992). Particular studies on below
ground invertebrates colonising green roofs are
absolutely rare (Frund 1996). On roofs with
extensive greening, Joger and Vowinkel (1992)
mainly identied synanthropic and thermophilic
collembolan species. Buttschardt (2001) studied
the soil fauna of six roofs (47 years old) of the
extensive greening type. He found collembolans
to be predominant over mites, ants and larvae
of diptera and beetles. All these different arthro-
pod groups become permanently established
in the growing media once they are settled in
(Buttschardt 2001).
We hypothesised that soil formation occurs in the
growing medium of extensive roof greening, and
that the successive development in the growing
medium promotes urban biodiversity and counters
habitat loss. For this purpose, we selected 10
representative green roofs of two different age
classes within the inner urban area of Hanover
(Germany): 812 years after installation (old roofs)
and 34 years after installation (young roofs). We
focussed on collembolans because they are known
as pioneers in colonising heavily disturbed land-
scapes like recultivation areas (Dunger 1989).
Furthermore, collembolans obviously promote soil
forming processes by catalysing microbial activity
and decomposition processes (overview in Hopkin
1997). The results are discussed in the context of
urban soils and the development of soil in extreme
environments.
Materials and methods
Roofs and growing media
Ten at green roofs were sampled within the
inner urban area of Hanover (52122
0
N; 9144
0
E; 55 m
above sea level) in Lower Saxony, Germany. The
city of Hanover, including outskirts, comprises an
area of about 200 km
2
currently providing space for
516,000 inhabitants. The local climate is charac-
terised by a mean annual air temperature of 8.7 1C
and an average of 661 mm of precipitation per year.
The year of construction and greening installa-
tion determined the choice of roofs for sampling.
They were divided into two different age classes
(Table 1). The rst age class comprised roofs
constructed between 1998 and 1999, referred to
from here on as young roofs. The second age
class, old roofs, was constructed between 1990
and 1994. The distance between roof and ground
level was 36 m except for two cases (10 and 30 m).
An extensive roof greening system was established
on top of all roofs in the year of their construction.
The mineral part of the substrate (growing
medium) consisted of expanded clay pellets (old
roofs) and expanded shale pellets (young roofs)
with a texture ranging from 2 to 10 mm for both.
While these pellet types differ in terms of their
technical development and production processes,
they have the same properties when installed on
roofs (manufacturers instructions, unpubl.). On
average, the substrate layers were about 8 cm
thick. Apart from one roof (25 m
2
), the areas of
sampled roofs were between 125 and 600 m
2
. Table
1 gives more detailed roof characteristics.
During the sampling season, the roofs were
exposed to sunlight for 8 (72) h per day. The
vegetation coverage of the roof surfaces ranged
from 75% to 95% represented by the sedo-scler-
anthetea plant community with dominating Sedum
species (Crassulaceae; mainly Sedum acre, Sedum
sexangulare and Sedum album), Trifolium species
(Fabaceae; mainly Trifolium arvense and Trifolium
repens) and grasses like Agrostis capillaris. As
compared to young roofs, old roofs were increas-
ingly colonised by species of Caryophyllaceae,
Geraniaceae and Asteraceae.
Sampling and sample processing
Undisturbed soil samples were taken randomly
from the upper 4 cm using a corer (5.6 cm dia-
meter). Sampling occurred biweekly on three dates
between June and July 2002. One set of soil cores
(n 8 per roof at each date) was extracted for
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Collembolans on green roofs in an urban area 349
microarthropods according to the high gradient
method of MacFadyen (1961). The extraction lasted
10 days, starting at 20 1C with a daily increase of
5 1C up to 45 1C from day 6 onwards. The collembo-
lans were separated from all other material and
stored in ethanol (96%) until they were identied
according to the keys of Gisin (1960), Zimdars and
Dunger (1994), Bretfeld (1999), Potapow (2001) and
Thibaud et al. (2004). A second set of soil cores
were sampled to measure several soil properties.
Substrate moisture (n 5 per roof at each date)
was estimated gravimetrically by drying 20 g soil for
24 h at 105 1C. Furthermore, substrate pH (n 5
per roof at each date) was measured in 0.01 M CaCl
2
(soil/solution ratio of 1:2.5). Organic carbon (C
org
)
and total nitrogen (N
t
) contents (n 5 per roof at
each date) were determined using the macro-
element analyser LECO CHN-1000 (LECO, Kirch-
heim, Germany) with 20 mg of oven-dried (105 1C)
and pre-ground substrate. Finally, dehydrogenase
activity was measured twice on each sampling
date on every roof using the triphenyltetrazolium
chloride (TTC) method as described by Malkomes
(1993).
Data processing
The KolmogorovSmirnov test conrmed that all
data were normally distributed. For this reason, the
Student T-test was used to compare treatment
effects. Biodiversity was analysed using Shannon
Weaver diversity index and evenness. The relative
dominance structure of collembolan species was
determined following the classication system
of Engelmann (1978). According to this system,
species comprising more than 10% of the total
density are classied as dominant. A TWINSPAN
analysis (two-way-indicator-species-analysis) after
Hill (1979) was done to check species typical for
roof greening successive development. Further-
more, an agglomerative hierarchical clustering
was conducted according to Ward (1963) using
selected data sets to group roofs. Multivariate
statistics employing two-group discriminant func-
tion analysis were applied to determine which roof
characteristics separated age classes.
Results
Table 2 presents the data of the selected abiotic
properties of the growing media and the collembo-
lan densities from all ten roofs. In the following
section, we refer to some remarkable data shown in
Table 2 complemented by the overall means for the
young and the old green roofs.
Selected properties of the growing media
The mean pH values of the ve young roofs varied
between 6.4 (Y4) and 6.7 (Y3) resulting in an
average pH of 6.5. A lower mean pH of 5.8 varying
from 5.4 (O5) to 6.5 (O4) was measured in
the growing media of the ve old roofs. The pH
difference between both age classes was signicant
at P 0.007.
C
org
content was highly variable in general and
highest in the older roofs. The mean C
org
contents
lay between 1.1% (Y4) and 3.4% (Y1) for young roofs
in contrast to old roofs characterised by mean
ARTICLE IN PRESS
Table 1. Detailed characterisation of sampled young (Y) and old (O) green roofs
Yound roofs Y1 Y2 Y3 Y4 Y5
Year of construction 1999 1998 1998 1999 1998/1999
Growing medium ES 210 mm ES 210 mm ES 210 mm ES 210 mm ES 210 mm
Layer thickness (cm) 8 8 8 8 8
Roof height (m) 6 3 30 3 3
Roof area (m
2
) 750 600 500 125 125
Veg. coverage (%) 90 75 75 95 95
Old roofs O1 O2 O3 O4 O5
Year of construction 1994 1992 1994 1992 1990
Growing medium EC 210 mm ES 210 mm Mineral/Mulch EC 210 mm EC 210 mm
Layer thickness (cm) 4+4 8 9 4+6 6
Roof height (m) 3 5 10 3 6
Roof area (m
2
) 25 280 600 500 600
Veg. coverage (%) 95 80 95 95 85
ES expanded shale pellets; EC expanded clay pellets.
S. Schrader, M. Boning 350
contents from 1.6% (O2) to 8.4% (O5). Pooling
the data for each age class resulted in a signicant
difference (P 0.044) between the means of
1.8% C
org
on young and 4.6% on old roofs. The
mean N
t
content of 0.34% on old roofs exceeded
that of young roofs with 0.24% N
t
(P 0.061). The
average C:N ratio did not differ signicantly
between young and old roofs with 20.8 and 19.8,
respectively.
Very variable and extremely high dehydrogenase
activities were measured in the growing media. The
lowest mean value was measured in the substrate
of a young roof (Y2) at 451 mg TPF g
1
d
1
and the
highest mean value on an old roof (O4) reaching
4530 mg TPF g
1
d
1
. On average, the dehydrogen-
ase activity on young roofs was 1892 mg TPF g
1
d
1
,
and 2874 mg TPF g
1
d
1
on old roofs, but this
difference was not signicant.
The discriminant analysis determined the data
sets of pH values, C
org
contents and dehydrogenase
activities to contribute the most to group member-
ship (age classes). For those variables, the highest
standardised discriminant coefcients were calcu-
lated as 0.67 (pH), 0.57 (C
org
) and 0.72 (deydro-
genase activity). The Wilks Lambda statistic for
the canonical discriminant function revealed
the group centroids to be signicantly different
(Po0.001) indicating the suitability of the function
to discriminate the age classes. In total, 90% of
all cases were classied correctly into both age
classes. However, two old roofs (O1; O3) were
grouped into the class of young roofs.
A hierarchical cluster analysis, using pH, C
org
contents and dehydrogenase activities, also sepa-
rated the growing media into the two clusters
young roofs and old roofs (Fig. 1). The
dendrogram (Fig. 1) shows the similarity among
the ve young roofs which form a cluster of minimal
distances. By contrast, the roofs within the old
roof cluster show partly wider differences. Roofs
O1 and O3 are clustered adjacently with the lowest
distances followed by roofs O2, O4 and O5 with
increasing distances indicating increasing dissim-
ilarities (Fig. 1).
ARTICLE IN PRESS
Figure 1. Dendrogram obtained by hierarchical cluster-
ing pH, C
org
content and dehydrogenase activity in
growing substrate of extensive green roofs in a city.
The year of roof construction is given in brackets.
Y young green roof; O old green roof.
Table 2. Arithmetic means (SD) of abiotic properties and collembolan density, and biodiversity indices in growing
substrates of extensive green roofs in urban Hanover
Yound roofs Y1 Y2 Y3 Y4 Y5
pH 6.49 (0.18) 6.51 (0.21) 6.76 (0.13) 6.23 (0.44) 6.52 (0.19)
C
org
(%) 3.4 (1.4) 1.2 (0.6) 2.0 (2.3) 1.1 (0.6) 1.4 (0.4)
N
t
(%) 0.22 (0.03) 0.16 (0.06) 0.26 (0.13) 0.35 (0.22) 0.24 (0.01)
DHA (mg TPF g
1
d
1
) 2032 (962) 451 (75) 1382 (876) 2697 (32) 2898 (27)
Soil water content (%) 28.6 (27.8) 15.5 (15.2) 21.4 (19.89) 22.8 (21.5) 24.8 (23.4)
Collembola (10
3
ind. m
2
) 87.5 (11.7) 22.9 (8.6) 41.1 (22.9) 68.6 (11.9) 55.2 (4.0)
ShannonWeaver 1.16 0.81 0.75 0.92 0.78
Evenness 0.42 0.31 0.25 0.33 0.26
Old roofs O1 O2 O3 O4 O5
pH 5.76 (0.30) 5.77 (0.24) 5.91 (0.20) 6.47 (0.16) 5.33 (0.53)
C
org
(%) 4.2 (1.6) 1.6 (0.9) 4.0 (1.8) 4.5 (2.1) 8.4 (2.5)
N
t
(%) 0.25 (0.11) 0.34 (0.20) 0.32 (0.16) 0.48 (0.12) 0.30 (0.02)
DHA (mg TPF g
1
d
1
) 1991 (171) 3938 (2059) 1983 (1632) 4530 (1316) 1928 (842)
Soil water content (%) 18.8 (17.7) 19.0 (17.9) 26.6 (25.7) 25.9 (23.4) 23.9 (23.2)
Collembola (10
3
ind. m
2
) 76.4 (12.1) 67.0 (24.1) 19.8 (12.9) 41.3 (23.2) 80.2 (46.1)
ShannonWeaver 0.87 1.03 0.81 0.77 1.70
Evenness 0.32 0.40 0.26 0.26 0.61
The standard deviations of the means are given in brackets. Y young green roofs; O old green roofs; DHA dehydrogenase
activity.
Collembolans on green roofs in an urban area 351
Small differences and high variability were found
for the water contents of the substrates. The mean
water contents of the young roofs varied between
15.5% (Y2) and 28.6% (Y1), resulting in an overall
mean of 22.6%. In the case of old roofs, mean water
contents ranged from 18.8% (O1) to 26.6% (O3) with
a mean of 22.8%. The mean difference between
young and old roofs was not signicant (P 0.916).
Collembolans
Total collembolan abundance differed widely
among roofs ranging from 20,000 (O3) to 88,000
(Y1) individuals m
2
. Over all, mean differences
between the two age classes were not signicant
(P 0.864) with 55,000 and 57,000 individuals m
2
in the growing media of young and old roofs,
respectively.
In total, 30 species were identied (Appendix).
The number of species was similar between roof
age classes with 26 and 24 species on young and old
roofs, respectively. However, on old roof no. O5,
the Shannon Weaver index (1.70) and evenness
(0.61) were highest compared to young roof Y3, for
which the lowest Shannon Weaver index (0.75) and
evenness (0.25) were calculated. On average,
differences between both roof classes were insig-
nicant with a mean Shannon Weaver index of 0.88
and 1.04, and an evenness of 0.31 and 0.37 for
young and old green roofs, respectively.
Differences between both roof classes became
more obvious at the species level. We concentrated
on the 10 dominant species on roofs in at least one
age class. Their relative distribution and absolute
density is presented in Fig. 2. Species like Hypogas-
trura sahlbergi, Lepidocyrtus lignorum and Thalas-
saphorura encarpata were more abundant on young
roofs compared to old roofs. In fact, only 0.1% of all
H. sahlbergi individuals found were extracted from
samples of old roofs. In contrast, species like
Folsomides parvulus, Lepidocyrtus cyaneus, Cryp-
topygus thermophilus, Cryptopygus bipunctatus
and Mesaphorura krausbaueri preferred the sub-
strates of old roofs. Nearly 99% of all M. kraus-
baueri individuals were identied from old roof
samples. Finally, species like Isotoma viridis and
Parisotoma notabilis were abundant on all roofs
(42000 and 48000 individuals m
2
on average,
respectively) with similar mean densities in the
growing media of both age classes.
TWINSPAN analysis divided the growing media
into two groups: Y1, Y2, Y3, Y5 and O3 representing
one group with mostly young roofs and O1, O2, O4,
O5 and Y4 the other group with mostly old roofs.
T. encarpata and Brachystomella parvula were
identied as indicator species for this division.
A second division further separated the groups. The
rst group consisted of the young roofs Y1, Y2 and
Y5 while the second group included one young (Y3)
and one old roof (O3). This division was indicated
by Entomobrya marginata. Furthermore, TWINSPAN
identied Friesea mirabilis that divided old roofs
O1, O4 and O5 into one group and Y4 and O2 into
another group.
Discussion
The mean collembolan densities varied widely
from 20,000 to 88,000 individuals m
2
, which are
within the range reported for urban soils at the
ground level (Fountain and Hopkin 2004). Studying
extensive roof greenings (47 years old) in urban
Karlsruhe (Germany), Buttschardt (2001) counted
collembolan densities between 13,000 and
73,000 individuals m
2
. Furthermore, he found col-
lembolans predominating over all other microar-
thropods (Buttschardt 2001). Dunger (1989)
reported a similar result from mine recultivation
areas within the rst decade of soil reclamation. In
comparison to other soil systems characterised by
signicant human impact, such as arable land and
mine recultivation sites, the total collembolan
abundances in the present study were high.
A possible reason for this result may be the absence
of earthworms in extensive growing media. On
green roofs, earthworms are only common in
intensive growing media and establish themselves
in media depths of at least 12 cm (Steiner and
Schrader 2002), which was not the case in the
present study. Dunger et al. (2004) emphasised the
ecologically dominating impact of initial earth-
worm activity on collembolans in reclaimed mining
areas.
The total number of species found in the green
roofs was 30, which is comparable to the 38 species
identied by Fountain and Hopkin (2004) in urban
soils at the ground level. Among the dominant
species of the present study, H. sahlbergi,
L. lignorum and T. encarpata colonised the
young roofs but were less abundant or nearly
absent on old roofs. Other dominant species
like P. notabilis, C. thermophilus and L. cyaneus
can be classied as cosmopolitan pioneers (Dunger
et al. 2004) that are also common in urban
soils (Fountain and Hopkin 2004). According to
Klausnitzer (1992), urban habitats are often colo-
nised by xerophilic and thermophilic species. In the
present study, this ecological classication com-
prises four dominant species, namely, F. parvulus,
ARTICLE IN PRESS
S. Schrader, M. Boning 352
L. cyaneus, C. thermophilus and C. bipunctatus.
The indicator species B. parvula, E. marginata
and F. mirabilis, that divided roofs into different
groups according to the TWINSPAN analysis, are also
common in urban soils (Fountain and Hopkin 2004),
and even on greened roofs under extreme climatic
conditions (Joger and Vowinkel 1992). Summarising
the results on collembolan species diversity, ubi-
quists colonised green roofs rst, specialists domi-
nated the communities later on. Dunger et al.
(2004) demonstrated primary succession of collem-
bolan communities in mine sites passing through
bottlenecks with lower niche diversity after the
rst decade of development. It is questionable if
ARTICLE IN PRESS
Figure 2. Distribution of the most frequent collembolan species in growing substrates of extensive green roofs in a city.
The relative quotas of the species from young and old roofs are given including their densities (individuals m
2
). 100% in
one pie chart summarises all individuals of one species collected from all 10 roofs.
Collembolans on green roofs in an urban area 353
such successive patterns also take place in matur-
ing green roofs. Future studies should consider this
question.
In extensive roof greening concepts, Sedum
species and other species of the sedo-scleranthetea
plant community have been the most commonly
used plants. They provide and maintain the best
conditions for soil biota in this harsh environment
as was shown by Buttschardt (2001) and conrmed
by our results. These plants withstand extended
drought periods best in greening substrates thicker
than 6 cm (Van Woert et al. 2005) as in our study.
They are heat and cold tolerant and have a high
growth index in order to provide quick coverage of
the roofs (Monterusso et al. 2005), which protects
soil biota like collembolans in their habitat.
Furthermore, these plants promote moisture re-
tention very well in the growing media (Van Woert
et al. 2005).
According to the results of Scharenbroch et al.
(2005), time is an important developmental
factor for distinguishing soils in urban environ-
ments. They sampled urban sites up to 3, around 10
and greater than 50 years old and demonstrated
reductions in bulk density, increases in microbial
biomass and activity, and increases in organic
matter with increasing age. These results match
ours with respect to soil forming processes. In our
case, we found acidication, increasing contents of
C
org
and N
t
, and increasing dehydrogenase activity
with time. Scharenbroch et al. (2005) concluded
from their results that the impact of initial
disturbance decreases rapidly with time and that
simultaneously, increasing synergistic processes
improve physical, biological and chemical soil
properties.
We could demonstrate from cluster analysis
on the substrate properties that young roofs
seemed to be more similar to each other compared
to old roofs, which are characterised by increasing
dissimilarities with increasing time from initial
disturbance (i.e., construction and greening instal-
lation). Old roof no. O5, the oldest roof studied
here, was most distant from the other roofs in
the cluster analysis (Fig. 1), and had the highest
biodiversity. We conclude that soil development is
most advanced on roof O5. In most cases, the
roofs could be grouped according to their growing
media properties into young and old roofs.
However, the results for old roof O3 were not
consistent with this trend. According to discrimi-
nant analysis, this roof was classied with the
young roofs. When the TWINSPAN analysis was
applied to the collembolan species, roof O3, next
to roof O1, was the youngest among the old
roofs. Roof O1 was also grouped with the young
roofs according to discriminant analysis and clus-
tered close to roof O3 (Fig. 1). However, roof O3 is
the only one which is covered by a 9 cm thick
layer of a mineral and mulch mixture (Table 1),
which would presumably increase the rate of
soil formation. Probably other factors, which
were not considered here, might account for our
observations.
Our results showed that extensive roof greening
provides conditions for successive developments of
soil biota (in this case, Collembola) and soil-
forming processes which clearly contribute to
urban biodiversity and compensate, at least in
part, for conventional asphalt roofs. Although roof
greening does not replace nature, a dense network
of green roofs in conurbations may promote urban
ecological services and should be part of sustain-
able urbanisation concepts (Kim 2004; Platt 2004).
With respect to German legislation, von Haaren and
Reich (2006) summarised implementation possibi-
lities and different planning approaches to con-
serve biodiversity in habitat networks. We propose
that green roofs, in light of our results, may provide
a partial solution. Wong et al. (2003) conducted an
economic case study to compute and compare
different types of costs between conventional at
roofs, and intensive and extensive green roofs.
They clearly demonstrated that life cycle costs
including energy costs of extensive green roofs
are the lowest despite the higher initial costs of
installation.
Especially in megacities (human population of
greater than 10 million inhabitants), where envir-
onmental problems are most striking, many urban
ecological measures are underway as in New York
City (Alfsen-Norodom et al. 2004), Seoul (Kim 2004)
and Mexico City (Molina and Molina 2004). In this
context, Kim (2004) proposed a sustainable urba-
nisation concept for Seoul where green roofs play a
key role as stepping stone habitats within an
urban green area cluster. This cluster should be
part of an urban biosphere reserve with a green
belt surrounding the city and green corridors
passing through the city (Kim 2004). Green roofs
can revalue an urban environment even under
severe space constraints and intense population
pressures.
Conclusions
The maturing development of the growing media
of green roofs reects soil-forming processes in-
dicated by acidication and increasing contents of
C
org
and N
t
. Collembolan abundance and number of
ARTICLE IN PRESS
S. Schrader, M. Boning 354
species develop slowly. But the species diversity is
highly dynamic over time, undergoing successive
development comparable to that occurring in
extreme environments. It can be assumed that at
least soil mesofaunal successive developments in the
growing media of roof greenings and newly re-
claimed mining areas are quite similar. Keeping in
mind that such comparisons are always limited,
some basic similarities are evident: (1) virgin
anthropogenic substrate; (2) initial soil-forming
processes during substrate maturation; (3) increas-
ing organic matter and increasing biological activity.
How such initially articial and developing
substrates, like those of maturing green roofs,
may be integrated into common soil classication
systems remains to be debated. Nevertheless, our
study shows the properties of these substrates
developing towards a soil-like state to provide a
living habitat for soil organisms and a growing
medium for plants. We conclude that soil-forming
processes occur which improve niche occupancy of
collembolans and ultimately promote urban biodi-
versity and urban ecology.
Despite their benecial properties and ecological
value for urban landscapes, green roofs should
never be considered a justication for destroying
natural or semi-natural habitats on the outskirts of
cities and beyond. Roof greening revalues cities but
does not replace nature.
Acknowledgements
We wish to thank the owners and holders of all
buildings, whose green roofs we studied, for their
permission and patience. Furthermore, we ob-
tained valuable advice from the companies Optima
Nord (Tornesch), which produced the substrates,
and Janisch Garten- und Landschaftsbau (Hanover),
which installed all the green roofs we studied.
David Russell provided valuable help with the
identication of collembolan species in some
doubtful cases. Finally, we would like to thank
two anonymous reviewers for their helpful com-
ments.
Appendix
Collembolan species recorded in the present
study
PODUROMORPHA
Brachystomella parvula (Scha ffer, 1896)
Friesea mirabilis (Tullberg, 1871)
Thalassaphorura encarpata (Denis, 1931)
Mesaphorura krausbaueri s.l. (Borner, 1901)
Hypogastrura assimilis (Krausbauer, 1898)
Hypogastrura sahlbergi (Reuter, 1895)
ENTOMOBRYOMORPHA
Cryptopygus bipunctatus (Axelson, 1903)
Cryptopygus thermophilus (Axelson, 1900)
Folsomia inoculata (Stach, 1947)
Folsomia similis (Bagnall, 1939)
Folsomides parvulus (Stach, 1922)
Parisotoma notabilis (Scha ffer, 1896)
Isotoma viridis (Bourlet, 1893)
Vertagopus westerlundi (Reuter, 1898)
Isotomodes productus (Axelson, 1906)
Isotomurus palustris (Muller, 1760)
Entomobrya marginata (Tullberg, 1871)
Entomobrya multifasciata (Tullberg, 1871)
Lepidocyrtus lignorum (Fabricius, 1781)
Lepidocyrtus cyaneus (Tullberg, 1871)
Pseudosinella octopunctata (Borner, 1901)
Coecobrya caeca (Schott, 1896)
NEELIPLEONA
Megalothorax minimus (Willem, 1900)
SYMPHYPLEONA
Sminthurides malmgreni (Tullberg, 1876)
Sphaeridia pumilis (Krausbauer, 1898)
Stenacidia violacea (Reuter, 1878)
Sminthurinus aureus (Lubbock, 1862)
Sminthurinus elegans (Fitch, 1862)
Sminthurinus trinotatus (Axelson, 1805)
Bourletiella hortensis (Fitch, 1863)
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