Urban Forestry & Urban Greening 56 (2020) 126875

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Urban Forestry & Urban Greening

journal homepage: www.elsevier.com/locate/ufug

The effects of growth form on the impact of companion planting of

nectar-producing plant species with Sedum album for extensive green roofs
Tatsuya Matsuoka a, *, 1, Kazuaki Tsuchiya a, Susumu Yamada b, Jeremy Lundholm c,
Toshiya Okuro a
a
Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku, Tokyo, 113-8657, Japan
b
Faculty of Agriculture, Tokyo University of Agriculture1737, Funako, Atsugi-shi, Kanagawa, 243-0034, Japan
c
Biology Department, Saint Mary’s University, 923 Robie St., Halifax, NS, B3H 3C3, Canada

A R T I C L E I N F O A B S T R A C T

Handling Editor: Wendy Chen Pollinators provide crucial urban ecosystem services. Introducing nectar-producing species on green roofs is one
method to support pollinator populations. However, novel cultivation methods may be required to improve plant
Keywords: health with minimal irrigation on extensive green roofs, which are severely restricted in soil thickness. Although
Extensive green roof companion planting with CAM plants such as Sedum has been reported to improve the performance of neigh­
Companion planting
boring plants, the growth form of the beneficiary species seems important in determining the effectiveness of the
Species mixture
technique. In this study, eleven species of nectar-producing plants were classified into two growth forms: carpet
Growth forms
Nectar-producing plants species (Phyla canescens, Trifolium repens, Thymus serpyllum and Thymus longicaulis), non-carpet species (Calam­
Competition intha nepeta, Lavandula officinalis, Lavandula stoechas, Melissa officinalis, Mimosa pudica, Rosmarinus officinalis
‘Erectus’, Rosmarinus officinalis ‘Prostratus’), and were planted together with Sedum album in a greenhouse or on
a rooftop space. There were no net positive effects in the impacts of companion planting with S. album on plant
biomass both in carpet and non-carpet species. However, companion planting with S. album had net positive
effects on leaf health in L. stoechas, M. officinalis, M. pudica, and R. officinalis ‘Prostratus’, classified as non-carpet
species. In contrast, there were no positive effects on carpet species, planted together with S. album. These results
suggest that complementary growth forms could be one of the factors to determine effective planting combi­
nations to improve plant health conditions on extensive green roofs. Additionally, the increase in soil water
content by suppressing evapotranspiration when water is limiting can be effective in improving leaf health
conditions of neighbors in companion planting with S. album. While past studies have shown positive benefits of
companion planting with CAM species, this experiment suggests the possibility that not all growth forms may
benefit from facilitation by Sedum.

1. Introduction particular, plant-pollinator networks are considered essential for sup­

Ecosystem services, which bring about a variety of benefits to
humans directly and indirectly, have attracted a great deal of attention
in urban areas (Millennium Ecosystem Assessment 2005, Cardinale
et al., 2015). Pollinators in urban areas have important roles in
ecosystem services such as regulating services (pollination), provision­
ing services (honey production) and cultural services (opportunities for
environmental education) (Baldock et al., 2015; Yamada et al., 2011). In
porting biodiversity (Klein et al., 2007). However, urbanization has
often caused reduction of insect populations by alteration of nesting and
food resources and other ecological changes (Jones and Leather, 2012).
Hence, researchers have sought to support urban pollinators by creating
artificial habitats such as green roofs planted with nectar-producing
plants (Colla et al., 2009; MacIvor, 2016).
In general, green roofs are classified as ‘extensive’ or ‘intensive’.
Extensive green roofs are characterized by shallower substrate depth

Abbreviations: CAM, Crassulacean acid metabolism; ET, Evapotranspiration.

* Corresponding author.
E-mail addresses: quiche1124@gmail.com (T. Matsuoka), tcy@live.jp (K. Tsuchiya), sy206447@nodai.ac.jp (S. Yamada), Jeremy.lundholm@smu.ca
(J. Lundholm), aokuro@mail.ecc.u-tokyo.ac.jp (T. Okuro).
1
Current affiliation: Institute of Technology, Shimizu Corporation, 3-4-17 Etchujima, Koto-ku, Tokyo 135-8530.

https://doi.org/10.1016/j.ufug.2020.126875
Received 9 January 2020; Received in revised form 12 September 2020; Accepted 7 October 2020
Available online 13 October 2020
1618-8667/© 2020 Elsevier GmbH. All rights reserved.
T. Matsuoka et al.
and reduced needs for watering, while intensive green roofs require
more than 20 cm substrate depth and have high water demand
(Oberndorfer et al., 2007). Due to the weight and cost limitation for the
building, extensive green roofs have been more commonly introduced
because of low maintenance requirements and greater ecological sus­
tainability (Cook-Patton and Bauerle, 2012; Castleton et al., 2010).
However, the number of nectar-producing species that can survive
without irrigation on extensive green roofs is limited (MacIvor and
Lundholm, 2011; Nagase and Dunnett, 2010).
Diverse plant mixtures can result in improved survival under drought
conditions compared with monocultures (Mulder et al., 2001), and CAM
(Crassulacean acid metabolism) species have been considered to
improve the health condition for neighboring non-succulent plants on
extensive green roofs (Nagase and Dunnett, 2010). It has been suggested
that companion planting with Sedum species can substitute for frequent
watering on green roofs in terms of the health condition of the plants
(Ahmed et al., 2017). Some Sedum species have creeping stems and form
wide mats, thus reduction of soil temperature due to a mulching effect
was suggested as one of the factors to explain positive effects on other
species (Butler and Orians, 2011). On the other hand, soil water content
and other factors were also suggested as important factors in driving the
health condition of plants on extensive green roofs (Butler and Orians,
2009; Young et al., 2017). CAM plants, including Sedum species, tolerate
drought-prone substrates typical of extensive green roofs, and this is
due, in part, to CAM photosynthesis. Transpiration of CAM plants is
generally less than other C3 plants because stomata are closed in daytime
through CAM photosynthesis (Black and Osmond, 2003). Therefore,
when Sedum species are planted on green roofs, ET (evapotranspiration)
can be suppressed due to CAM photosynthesis and a mulching effect,
and this may lead to higher substrate water content (Lundholm et al.,
2010).
Thus far, companion planting with Sedum species in green roofs had
positive effects on the health condition of Agastache “Black Adder” and
some perennial culinary herbs (Butler and Orians, 2011; Ahmed et al.,
2017). However, in some other species, companion planting with CAM
plants had no effects on the healthy biomass of neighboring plants
(Nagase and Dunnett, 2010). On the contrary, total biomass and di­
versity levels of some annual plants interacted negatively with Sedum
species when planted together (Vasl et al., 2017). In general, coexisting
plant species share resources (e. g. soil water content, nutrients), and
positive or negative interactions often occur (Connell, 1983; Schoener,
1983). In some cases, facilitation effects or competition for space in
plant communities also affect plant size and distribution of individuals
(Schwinning and Weiner, 1998), and these interactions can occur
concurrently (Callaway and Walker, 1997). Diverse species mixtures on
extensive green roofs can also positively affect canopy density and
ecosystem functioning (Lundholm, 2015), with certain combinations of
life-forms (e. g. tall forbs, grasses and succulents) being especially useful
(Lundholm et al., 2010). However, it must be noted that not all species
combinations show positive inter-specific interactions in green roof
systems (Lundholm et al., 2010; Heim and Lundholm, 2014), and plant
traits are important in determining the degree of competition for re­
sources and space (Tilman, 1994). Although some studies have reported
on the effective combinations of growth forms to improve ecosystem
functioning with positive interactions like niche complementarity and
facilitation (Roscher et al., 2008; Lundholm, 2015; Young et al., 2017;
Vasl et al., 2017), there is still much to be learned about how companion
planting of Sedum species with other plant species might improve health
condition and ecological functions on green roofs and in other urban
settings.
Our study investigates how plants with different growth forms might
perform on green roofs, specifically 1) how does nectar plant growth
form affect companion planting success relative to monoculture
planting?, and 2) Do rates of ET and moisture content help explain
growth outcomes? In order to address these questions, we evaluated
eleven species of nectar-producing plants, classified into carpet or non-
2
Urban Forestry & Urban Greening 56 (2020) 126875
carpet growth forms. To test the effects of inter-specific interactions due
to companion planting with Sedum species in different growth forms, we
cultivated each nectar-producing species with and without Sedum album
in a greenhouse or on a rooftop space. The greenhouse experiment al­
lows us to control rainfall and remove effects of extreme wind and
irradiation on plant growth. The rooftop experiments can evaluate the
effects of growth forms of the plants on the plant growth in companion
planting under realistic environmental conditions, allowing us to
determine whether the greenhouse results are reproducible on actual
green roofs. We hypothesized that S. album will positively affect the
health conditions of non-carpet species, since there would be little
competition for space, and negative or neutral effects on carpet species.
2. Materials and methods
2.1. Experiment 1: cultivation experiment in a greenhouse
2.1.1. Study site and green roof system
Experiments were performed from July to September in 2017. Plant
cultivation and all experiments were conducted in a greenhouse
(35◦ 44′ N, 139◦ 32′ W). The plants were exposed to natural conditions in
terms of light intensity, humidity and air-temperature. The average air-
temperature ranged from 20.2 ◦ C to 30.3 ◦ C in a greenhouse which was
opened at the sides so that humidity was the same as outside. For plant
cultivation, we used a plastic module with dimensions of 40 cm × 30 cm
(Green vegetable planter 40, Richell co., Toyama, Japan), and filled with
10 cm depth of commercial soil for green roofs (RS-8, Up-land ltd.,
Tokyo, Japan) which had a saturated weight of 0.89 t/m3, a dry weight
of 0.45 t/m3, a maximum water capacity 400 L/m3, a water permeability
of 1.2 × 10− 4, a pH of 6.4, and included more than 50 % organic matter
consisted of coco peat, black peat and peat moss. We covered the bottom
of the modules, which had free draining bases, with nylon mesh (2 mm
pore size) to prevent soil runoff.
2.1.2. Plant growth
We cultivated eight species of perennial plants classified into two
growth forms, carpet (Phyla canescens, Trifolium repens and Thymus ser­
pyllum) and non-carpet (Calamintha nepeta, Lavandula officinalis, Mimosa
pudica, Rosmarinus officinalis ‘Erectus’ and Rosmarinus officinalis ‘Pros­
tratus’)(additional details in Table 1). All these species were cited as
excellent nectar sources in Japan (Japan Beekeeping Association, 2017;
Sasaki, 2010). The seeds of T. repens (Kaneko Seeds ltd., Gunma, Japan)
and M. pudica (Ingu co., Tokyo, Japan) were sown in 128 plug trays (FP
co., Hiroshima, Japan) on May 2. C. nepeta, L. officinalis, P. canescens, R.
officinalis ‘Erectus’, R. officinalis ‘Prostratus’ T. serpyllum were grown
from seedlings (Green Rocket co., Ibaragi, Japan), and 4 individuals
were planted per module on May 10.
We used Sedum album as companion CAM plants. S. album is char­
acterized by small and circular succulent leaves, and a mat-like growth
form (Starry et al., 2014). Rooted cuttings of S. album were prepared
from commercial seedlings (Green Rocket co., Ibaragi, Japan) on May
29. They were transferred to the modules after 3 days of rooting period
on plastic trays in a greenhouse. All plants were transferred to the
modules for the experiments on June 26.
We set two combinations for nectar-producing plants, as shown in
Fig. 1A. A minimum of 7 cm spacing was provided between individuals
at the beginning of the experiments (Lundholm et al., 2010; Heim and
Lundholm, 2014). There were four replicates for each combination, and
the total number of modules was 64. To avoid spatial effects in the
greenhouse, all modules were randomly positioned and rotated every
four days.
Before the beginning of the experiments, all seedlings were fully
watered every other day (Nagase and Dunnett, 2010). During the
experimental period, from July 12 to September 10, 1200 mL of water
(equivalent to 10 mm of rain event) was added to all modules once every
12 days (Lundholm et al., 2010), which is enough drying time to achieve
T. Matsuoka et al. Urban Forestry & Urban Greening 56 (2020) 126875

Table 1
The effects of species type of nectar-producing plants (i. e. Carpet and Non-carpet) on the impact of companion planting with S. album in Experiment 1. Mean value of
dry shoot weight of nectar-producing plants were standardized in each species by following formula: [(Original value – Mean value)/The standard deviation]. Mean
values of health score, soil water content, water loss and dry weight of Sedums were analyzed by Kruskal-Wallis test, post hoc Steel-Dwass test in each treatments (n =
4).
Measurements 　 Carpet Non-Carpet

　 Monoculture With S. album Monoculture With S. album

Standardized values of dry shoot weight of nectar-producing plants (g) 0.21 ± 1.02 − 0.22 ± 0.87 0.34 ± 1.00 − 0.34 ± 0.78
Health score 2.83 ± 0.83 a 2.33 ± 0.98 a 3.00 ± 1.17 ab 3.90 ± 0.91 b
August 4.27 ± 3.48 ab 4.62 ± 2.17 b 2.78 ± 3.40 a 5.02 ± 4.08 b
Soil water content (100×m3/m3)
September 3.81 ± 1.45 ab 3.61 ± 1.47 ab 2.69 ± 1.17 a 4.86 ± 1.97 b
August 0.22 ± 0.04 ab 0.23 ± 0.03 ab 0.25 ± 0.04 a 0.20 ± 0.05 b
Water loss (kg/48 h)
September 0.28 ± 0.07 0.27 ± 0.06 0.27 ± 0.07 0.27 ± 0.06
Dry weight of Sedums (g) 5.28 ± 1.76 a 11.72 ± 2.65 b

2010). We derived a health score using five levels; 5, all leaves were
healthy; 4, less than 30 % of the leaves were wilted or stressed; 3, 30%–
70% of the leaves were wilted or stressed; 2, more than 70 % of the
leaves were wilted or stressed; 1, dead.
Soil water content of the substrate were measured using a HH2
Moisture Meter (Delta-T Devices Ltd, Cambridge, UK) with Wet-2 sensor
(Delta-T Devices Ltd, Cambridge, UK) which was calibrated to the sub­
strate we used. We inserted the sensor vertically to 50 mm depth from
the soil surface. Average soil water content of growth media were
calculated from the measured values of 4 points around the central
individual.
Water loss was estimated by weight changes after watering. Weight
changes from modules after watering should be attributable to ET since
we used an electronic force balance (M2F-8KA, Shiro. Co., Osaka, Japan)
to quantify ET. We weighed each module 15 min after watering with
1200 mL, which is comparable to a 10 mm rain event, and then weighed
them again after 48 h (Lundholm et al., 2010). We added water over a
20-second interval to the surface of the modules.
All plants were harvested on September 15, and they were dried at 70
◦
C for 7 days, and then their dry weights were measured (Nagase and
Dunnett, 2010).

2.2. Experiment 2: Cultivation experiment on a rooftop space

2.2.1. Study site and green roof system

Experiments were performed from May to July in 2017. Plant
cultivation and all experiments were conducted on a rooftop space
(35◦ 74′ N, 139◦ 84′ W). The average air-temperature ranged from 16.3 ◦ C
to 28.9 ◦ C. For plant cultivation, we used a plastic module with di­
mensions of 50 cm × 40 cm (Green vegetable planter 50, Richell co.,
Toyama, Japan), and filled with 10 cm of substrates which are same as
that in Experiment 1.

2.2.2. Plant growth

Fig. 1. A. Plant configurations in Experiment 1.
B. Plant configurations in Experiment 2.
CAM induction in S. album (Matsuoka et al., 2019), and the plants were
not watered outside of the ET experiments.
2.1.3. Measurements
Health score and soil water content of nectar plants were measured
every month one day before watering, July 23, August 16 and
September 9. Additionally, we measured ET every month with watering,
July 24, August 17 and September 10.
Health score was measured to evaluate the health condition of
nectar-producing plants (Monterusso et al., 2005; Nagase and Dunnett,
We cultivated three species of nectar-producing plant classified into
two growth forms: carpet (Thymus longicaulis), non-carpet (Lavandula
stoechas, Melissa officinalis). The detailed species type of these plants
were listed in Table 5. All were cited as excellent nectar sources in Japan
(Japan Beekeeping Association, 2017; Sasaki, 2010). They were grown
from seedlings (Green Rocket co., Ibaragi, Japan), and were planted in
the modules on March 29. Due to limited rooftop space for experiments,
we used only three species.
Different nectar-producing plant species were selected in Experiment
1 and Experiment 2, and this is due to the earlier growing periods in
Experiment 2 (May to July). Plant species used in Experiment 1 have later
flowering periods compared to the species used in Experiment 2 (Herrera,
1993; Eriksson, 1998; Chwil, 2009; Kimbrough and Swift, 2009; Cam­
polo et al., 2015), and thus we could conduct the experiments before the
reproductive phase which might induce wilting during the experimental
periods.
We set two combinations for nectar-producing plants, as shown in

3
T. Matsuoka et al. Urban Forestry & Urban Greening 56 (2020) 126875

Fig. 1B. A minimum of 7 cm spacing was provided between individuals

at the beginning of the experiments (Lundholm et al., 2010; Heim and
Lundholm, 2014). There were four replicates for each combination, and
the total number of modules was 24. Combination patterns of plants in
Experiment 2 differed from that in Experiment 1, and this is due to the
limited space in the greenhouse. In Experiment 2, we used larger modules
for plant cultivation to avoid overturning by strong winds on the
rooftop. We used three nectar-producing plants on the roof, instead of
one, due to concerns about achieving enough cover of the substrate
during the growing season (from May to July in 2017). In Experiment 1,
we planted one individual nectar-producing plant in each module to
avoid intra-specific competition, and aimed to reveal the detailed effects
of growth forms of plants on the impacts of companion planting.
Before the beginning of the experiments, all seedlings were fully
watered every other day (Nagase and Dunnett, 2010). During the
experimental period, from May 2 to July 16, the plants were not watered
outside of the water loss experiments (June 3 and July 15).

2.2.3. Measurements
Health score and soil water content of nectar plants were measured
every month one day before watering, June 3 and July 15 as in Experi­
ment 1.
All plants were harvested on July 17, and they were dried at 70 ◦ C for Fig. 2. The relationship between health score of nectar-producing plants and
soil water content in Experiment 1. The fitted line is y = 36.1 x + 1.7 (R2 = 0.37,
7 days, and then their dry weights were measured (Nagase and Dunnett,
d.f. = 1,14, F = 8.282, p < 0.05).
2010).

significant differences in dry shoot weights of nectar-producing plants

2.3. Statistical analysis
between treatments with and without S. album either (Table 2). In non-
carpet species, dry shoot weights of L. officinalis, R. officinalis ‘Erectus’
All collected data were analyzed statistically to determine significant
and R. officinalis ‘Prostratus’ were significantly higher than C. nepeta and
differences between planting treatments using Rstudio (3.4.2). To
M. pudica when they were planted together with S. album. Additionally,
evaluate the effects of species type of nectar-producing plants (i. e.
there were no significant differences between carpet species (i. e.
Carpet and Non-carpet) on the impact of companion planting with
P. canescens, T. repens and T. serphyllum) and M. pudica and R. officinalis
S. album, we performed Kruskal-Wallis tests and post-hoc Steel-Dwass
‘Prostratus’ (Fig. 3).
tests for all comparisons. Additionally, to evaluate the effects of com­
However, health scores of M. pudica and R. officinalis ‘Prostratus’,
panion planting with S. album for each species, we performed Wilcoxon
classified as non-carpet species, were significantly higher when they
rank sum tests for health score, and performed Student’s t-tests for soil
were planted together with S. album than in monoculture in September.
water content, water loss and dry shoot weight between monoculture
Water loss was significantly reduced when they were planted together
(nectar plants only) and mixture (companion planting with S. album)
with S. album in August (Table 3). Moreover, soil water contents in non-
treatments. Moreover, to evaluate the differences between plant species,
carpet plant treatments were significantly higher in the modules with
we performed one-way ANOVA, post hoc Tukey’s HSD test for dry shoot
S. album than in monoculture in August (Table 4). In other non-carpet
weight of nectar-producing plants and S. album. Different letters and
species (e. g. C. nepeta, L. officinalis, R. officinalis ‘Erectus’), soil water
asterixes show that the p-value was less than 0.05 between combina­
contents were relatively increased by companion planting with S. album
tions. Moreover, we performed linear regression by the least-squares
method to clarify the relationship between health score and soil water
content in Experiment 1.
Table 2
Mean dry shoot weight of nectar-producing plants, planted together with
3. Results S. album in Experiment 1. Wilcoxon rank sum tests were performed between
monoculture (nectar plants only) and mixture (companion planting with
3.1. Experiment 1: cultivation experiment in a greenhouse S. album) treatments (n = 4).
Plant species Mean value of dry shoot weight (g) Growth
There were no significant differences in dry shoot weight between form
monoculture (nectar plants only) and mixture (companion planting with 1 individual With p-
S. album) treatments in both carpet and non-carpet species. Health score S. album value
and soil water content in non-carpet species were significantly higher Phyla canescens 14.88 ± 11.28 ± 0.23 Carpet
when they were planted together with S. album than in monoculture. 5.19 1.76
Additionally, water loss in non-carpet species was also suppressed by Trifolium repens 8.70 ± 1.22 8.13 ± 0.76 0.69 Carpet
Mimosa pudica 6.78 ± 1.03 5.68 ± 2.17 0.34 Non-
companion planting with S. album. In contrast, there were no significant Carpet
differences in health score, soil water content and water loss between Thymus serpyllum 11.75 ± 12.28 ± 0.69 Carpet
monoculture and mixture treatments in carpet species. Furthermore, dry 2.44 4.54
weights of S. album that were planted together with carpet species were Calamintha nepeta 6.58 ± 3.36 4.75 ± 3.86 0.69 Non-
Carpet
significantly lower than with non-carpet species (Table 1).
Lavandula officinalis 14.13 ± 12.65 ± 0.31 Non-
In terms of the relationship between the health condition of nectar- 1.38 0.99 Carpet
producing plants and soil water content, there was a moderate posi­ Rosmarinus officinalis 16.83 ± 15.30 ± 1.00 Non-
tive correlation between health score and soil water content in ’Erectus’ 5.31 1.43 Carpet
September (R2 = 0.37, d.f. = 1,14, F = 8.282, p < 0.05) (Fig. 2). Rosmarinus officinalis 20.08 ± 15.45 ± 0.69 Non-
8.49 2.55 Carpet
When the results were analyzed by plant species, there were no
’Prostratus’

4
T. Matsuoka et al. Urban Forestry & Urban Greening 56 (2020) 126875

during the experimental period (Table 3). Additionally, there were no

significant differences in water loss between treatments with and
without S. album in carpet plants during the experimental period either.
Soil water contents of P. canescens and T. repens were not increased by
companion planting with S. album during the experimental period. In
T. serpyllum, soil water content was significantly higher in the modules
with S. album than in the no neighbors treatment in August (Table 1).
Furthermore, dry weights of S. album that were planted together with
carpet species (e. g. P. canescens, T. repens and T. serpyllum) were
significantly lower than with non-carpet species (e. g. C. nepeta,
M. pudica L. officinalis, R. officinalis ‘Erectus’ and R. officinalis ‘Prostra­
tus’) (Fig. 4). Pictures of the nectar-producing plants with and without
neighboring S. album are attached in Appendix 1 to Appendix 8.

3.2. Experiment 2: Cultivation experiment on a rooftop

We cultivated three nectar-producing species on a rooftop space and

examined whether the effects of companion planting with S. album
depend on the species type of neighbors. The effects of companion
Fig. 3. Mean dry shoot weight of nectar-producing plants (Phyla canescens, planting with S. album on dry weight of nectar-producing plants were
Trifolium repens and Thymus serpyllum, Calamintha nepeta, Lavandula officinalis, not altered by species type in the rooftop trial (Table 6), and similar
Mimosa pudica, Rosmarinus officinalis ‘Erectus’ and Rosmarinus officinalis ‘Pros­ results were obtained when they were analyzed by species (Table 7).
tratus’), planted together with S. album in Experiment 1. Bars with different Health score and soil water content in non-carpet species were signifi­
letters incidate means that are significantly different (p < 0.05) from each other cantly higher when they were planted together with S. album than in
(one-way ANOVA, post hoc Tukey’s HSD test).
monoculture. Furthermore, dry weights of S. album that were planted
together with carpet species were significantly lower than with non-
Table 3
carpet species (Table 6).
The description of nectar-plant species and the effects of companion planting Dry shoot weight was higher in non-carpet species than that in
with S. album on the health condition of neighboring nectar-producing plants in T. longicaulis, a carpet species (Fig. 5), and dry weights of S. album that
Experiment 1. Wilcoxon rank sum tests were performed between monoculture were planted together with T. longicaulis were significantly lower than
(nectar plants only) and mixture (companion planting with S. album) treatments with non-carpet species (Fig. 6). In T. longicaulis, there were no signifi­
(n = 4). cant differences in health condition and soil water content between
Plant species Heath condition in September Growth treatments with and without neighboring S. album (Tables 8 and 9 ). In
form contrast, health scores and soil water contents in M. officinalis and
1 With p- L. stoechas, non-carpet species, were improved by companion planting
individual S. album value
with S. album in June (Tables 8 and 9). Pictures of the nectar-producing
Phyla canescens 2.25 ± 0.96 2.00 ± 0.82 0.91 Carpet plants with and without neighboring S. album are attached in Appendix
Trifolium repens 3.50 ± 0.58 3.25 ± 0.50 1.00 Carpet 9 to Appendix 11.
Mimosa pudica 3.75 ± 0.50 5.00 ± 0.00 < 0.05 Non-Carpet
Thymus serpyllum 2.75 ± 0.50 1.75 ± 0.96 0.26 Carpet
Calamintha nepeta 1.50 ± 0.58 2.50 ± 0.58 0.17 Non-Carpet 4. Discussion
Lavandula officinalis 3.50 ± 0.58 3.75 ± 0.50 1.00 Non-Carpet
Rosmarinus officinalis 4.00 ± 0.82 4.25 ± 0.50 1.00 Non-Carpet 4.1. Influence of growth form
’Erectus’
Rosmarinus officinalis 2.25 ± 0.96 4.00 ± 0.00 < 0.05 Non-Carpet
’Prostratus’ Judging from our results, growth form of nectar plants (carpet vs
non-carpet) had only a minor influence on the impact of the companion
planting with S. album. The results indicated that dry weight of nectar-
(Table 4), though there were no significant differences in health score producing plants, common measure of plant performance, was not
between the treatments with and without S. album (Table 3). improved by companion planting with S. album in both carpet and non-
In contrast, health score of carpet species (e. g. P. canescens, T. repens carpet species (Tables 1 and 6). Therefore, it could be suggested that
and T. serpyllum) was not improved by companion planting with S. album positive effects of companion planting on overall performance of nectar

Table 4
The effects of companion planting with S. album on soil water content of nectar-producing plants in Experiment 1. Student t-tests were performed between monoculture
(nectar plants only) and mixture (companion planting with S. album) treatments (n = 4).
Plant species Mean value of soil water content (100×m3/m3) Growth form

August September

1 individual With S. album p-value 　 With S. album p-value

1 individual

Phyla canescens 2.36 ± 0.11 2.54 ± 0.44 0.45 2.56 ± 0.66 2.49 ± 1.03 0.90 Carpet
Trifolium repens 8.83 ± 1.52 7.34 ± 0.74 0.13 5.49 ± 0.81 5.30 ± 0.65 0.73 Carpet
Mimosa pudica 9.29 ± 0.45 12.51 ± 1.46 < 0.05 4.35 ± 1.01 8.17 ± 1.11 < 0.05 Non-Carpet
Thymus serpyllum 1.64 ± 0.45 3.97 ± 0.62 < 0.05 3.37 ± 0.73 3.04 ± 0.75 0.55 Carpet
Calamintha nepeta 1.96 ± 0.80 4.45 ± 0.64 < 0.05 2.69 ± 0.32 4.21 ± 1.43 0.08 Non-Carpet
Lavandula officinalis 0.64 ± 0.37 1.78 ± 0.37 < 0.05 2.75 ± 0.45 4.30 ± 1.21 0.05 Non-Carpet
Rosmarinus officinalis ’Erectus’ 0.94 ± 0.35 2.01 ± 0.24 < 0.05 2.53 ± 0.40 3.48 ± 0.97 0.12 Non-Carpet
Rosmarinus officinalis ’Prostratus’ 1.10 ± 0.67 4.39 ± 1.05 < 0.05 1.12 ± 0.48 4.16 ± 0.49 < 0.05 Non-Carpet

5
T. Matsuoka et al. Urban Forestry & Urban Greening 56 (2020) 126875

Table 5
The effects of companion planting with S. album on water loss of nectar-producing plants in Experiment 1. Student t-tests were performed between monoculture (nectar
plants only) and mixture (companion planting with S. album) treatments (n = 4).
Plant species Mean value of water loss (kg/48 h) Growth form

August September

1 individual With S. album p-value 　 With S. album p-value

1 individual

Phyla canescens 0.24 ± 0.03 0.22 ± 0.02 0.25 0.21 ± 0.06 0.29 ± 0.05 0.09 Carpet
Trifolium repens 0.24 ± 0.01 0.24 ± 0.04 0.90 0.33 ± 0.02 0.32 ± 0.02 0.43 Carpet
Mimosa pudica 0.28 ± 0.03 0.22 ± 0.02 < 0.05 0.35 ± 0.04 0.38 ± 0.04 0.38 Non-Carpet
Thymus serpyllum 0.18 ± 0.04 0.22 ± 0..02 0.11 0.29 ± 0.06 0.20 ± 0.02 0.11 Carpet
Calamintha nepeta 0.22 ± 0.01 0.17 ± 0.06 0.16 0.21 ± 0.03 0.22 ± 0.03 0.56 Non-Carpet
Lavandula officinalis 0.23 ± 0.01 0.21 ± 0.05 0.48 0.25 ± 0.04 0.22 ± 0.01 0.20 Non-Carpet
Rosmarinus officinalis ’Erectus’ 0.28 ± 0.05 0.23 ± 0.06 0.27 0.29 ± 0.06 0.26 ± 0.04 0.56 Non-Carpet
Rosmarinus officinalis ’Prostratus’ 0.26 ± 0.02 0.16 ± 0.01 < 0.05 0.23 ± 0.06 0.29 ± 0.04 0.19 Non-Carpet

Table 7
Mean dry shoot weight of nectar-producing plants, planted together with
S. album in Experiment 2. Wilcoxon rank sum tests were performed between
monoculture (nectar plants only) and mixture (companion planting with
S. album) treatments (n = 4).
Plant species Mean value of dry shoot weight (g) Growth form

1 individual With S. album p-value

Thymus longicaulis 14.50 ± 2.27 12.50 ± 3.06 0.43 Carpet

Lavandula stoechas 24.44 ± 3.07 23.40 ± 3.03 0.74 Non-Carpet
Melissa officinalis 24.58 ± 4.38 28.83 ± 5.83 0.46 Non-Carpet

Fig. 4. Mean dry weights of neighboring S. album, planted together with

nectar-producing plants, per module after experimental periods in Experiment 1.
Bars with different letters indicate means that are significantly different (p <
0.05) from each other (one-way ANOVA, post hoc Tukey’s HSD test).

Table 6
The effects of species type of nectar-producing plants (i. e. Carpet and Non-
carpet) on the impact of companion planting with S. album in Experiment 2.
Fig. 5. Mean dry shoot weight of nectar-producing plants(Thymus longicaulis,
Mean value of dry shoot weight of nectar-producing plants were standardized in
Lavandula stoechas, Melissa officinalis), planted together with S. album in
each species by following formula: [(Original value – mean value)/The standard
Experiment 2. The values with different letters indicate means that are signifi­
deviation]. Mean values of health score, soil water content and dry weight of
cantly different (p < 0.05) from each other (one-way ANOVA, post hoc Tukey’s
Sedums were analyzed by Kruskal-Wallis test, post hoc Steel-Dwass test in each
HSD test).
treatments (n = 4).
Measurements Carpet Non-Carpet
plants cannot be induced, regardless of their growth forms. However,
　

　 Monoculture With Monoculture With the results also indicated that health score of nectar-producing plants
S. album S. album
showed obvious differences between growth forms in response to com­
Standardized values of 0.37 ± 0.84 − 0.37 ± − 0.11 ± 0.11 ± panion planting with S. album. Previous studies revealed that although
dry shoot weight of 1.13 0.94 1.04 companion planting with Sedum species had no net positive effects on
nectar-producing
plants (g)
plant biomass of neighbors, soil water content was increased (Vasl et al.,
Health score 4.00 ± 0.00 4.00 ± 3.00 ± 0.00 4.13 ± 2017) and health conditions of neighboring plants were relatively
a 0.00 a b 0.35 a improved compared with monocultures (Young et al., 2017). These
Soil water
June 10.56 ± 2.20
10.84 ±
9.09 ± 2.48
11.62 ± studies suggested a potential of companion planting with Sedum for
content 1.90 3.47
improving green roof performance, and the current study supports these
(100×m3/ 18.76 ± 0.88 18.64 ± 14.66 ± 2.02 20.38 ±
m3)
July
a 2.04 ab b 2.40 a results. Therefore, while nectar plant biomass was not improved by
7.63 ± 13.39 ± companion planting with S. album, there were positive effects on soil
Dry weight of Sedums (g)
0.53 a 1.17 b water and health scores but only with non-carpet species.
　Our results also indicated that companion planting with S. album
had no net negative effects on dry shoot weight of non-carpet species,

6
T. Matsuoka et al. Urban Forestry & Urban Greening 56 (2020) 126875

S. album is a creeping plant and spreads widely, thus evaporation from

Fig. 6. Mean dry weights of neighboring S. album, planted together with
nectar-producing plants, per module after experimental periods in Experiment 2.
The values with different letters indicate means that are significantly different
(p < 0.05) from each other (one-way ANOVA, post hoc Tukey’s HSD test).
Table 8
The effects of companion planting with S. album on the health condition of
neighboring nectar-producing plants in Experiment 2. Wilcoxon rank sum tests
were performed between monoculture (nectar plants only) and mixture (com­
panion planting with S. album) treatments (n = 4).
Plant species Heath condition in September Growth form
1 individual With S. album p-value
Thymus longicaulis 4.00 ± 0.00 4.00 ± 0.00 1.00 Carpet
Lavandula stoechas 3.00 ± 0.00 4.25 ± 0.43 < 0.05 Non-Carpet
Melissa officinalis 3.00 ± 0.00 4.00 ± 0.00 < 0.05 Non-Carpet
and soil water contents were higher when they were planted together
with S. album (Tables 1 and 6). Particularly, the positive effects of
companion planting with S. album on health score were observed in
M. pudica and R. officinalis ‘Prostratus’ in greenhouse experiments
(Fig. 2) and in M. officinalis and L. stoechas in rooftop experiments
(Fig. 5). These species grow upright during initial stages of their growth,
and then grow horizontally, but do not show carpet-like growth.
Although R. officinalis ‘Prostratus’ behaves as a carpet species in the mid
to long term, its creeping stems spread above S. album and did not
contact the soil surface, and thus we defined it as a non-carpet species. In
these cases, there would be no direct spatial competition with S. album,
which forms carpet-like stands. Thus, the results could suggest the
importance of growth forms in determining the effects of companion
planting with S. album, and the combination of such non-carpet species
and S. album could induce positive companion planting effects.
Complementary growth forms would also affect soil water content in
companion planting with Sedums. The effectiveness of companion
planting with Sedum under water deficit conditions was also revealed in
previous studies (Butler and Orians, 2011; Ahmed et al., 2017). In the
present study, we found that water loss was suppressed in greenhouse
experiments, in spite of the healthy condition of the leaves (Table 1).
the modules would be decreased by mulching effects of neighboring
S. album. Additionally, transpiration of S. album should be suppressed by
CAM photosynthesis under drought conditions (Starry et al., 2014;
Matsuoka et al., 2019). Judging from these characteristics of S. album,
companion planting with S. album might decrease both evaporation and
transpiration in August. In this case, evaporation from the modules
could be suppressed by the increase of plant cover in the modules with
M. pudica, R. officinalis ‘Prostratus’, M. officinalis and L. stoechas that
have some horizontal growth. Additionally, the results indicated a
positive correlation between the health conditions of nectar-producing
plants and soil water content (Fig. 2). Therefore, we suggest that the
health conditions of these non-carpet species planted with S. album were
improved by the increase in soil water content, driven by the suppres­
sion of water loss under drought conditions. It is also possible that hy­
draulic redistribution via the roots of S. album might have promoted
passive water transport which is dependent on water potential of growth
media (Richards and Caldwell, 1987; Leffler et al., 2005), and helped
increase available soil water for neighbors.
In contrast, there is a possibility that the combination of carpet
species and S. album can induce net negative effects on the growth of
Sedums. Our results indicated that dry weights of S. album, planted
together with carpet species, were significantly lower than those planted
with non-carpet species, suggesting that there was an observable effect
of inter-specific competition in the modules. Additionally, our results
indicated that health scores of carpet species were not affected by
companion planting with S. album (Figs. 2 and 5), and soil water content
and water loss were not affected either, except for the case with
T. serpyllum in August (Tables 1 and 6). In previous reports, negative
interactions occurred in some plant communities and interaction in­
tensity was dependent on growth form (Grover, 1997; Brooker, 2006).
The growth form of carpet species was similar to that of S. album, and
there could be interspecific competition for space. Thus, positive effects
of companion planting would not be induced in prostrate carpet species
due to direct competition with S. album. Similar effects have been re­
ported for facilitation studies using mosses and vascular plants on green
roofs: companion planting with species with similar growth forms led to
net negative effects (competition) whereas mosses could facilitate sur­
vival of vascular species that did not share aboveground space with the
mosses (Heim et al., 2014). In T. serpyllum, soil water content was
increased by companion planting with S. album in July, though there
were no significant differences in the heath score (Fig. 2, Table 3). In
general, T. serpyllum grows slower than other herb species, and there
might have been no spatial competition with S. album until the initial
stages of the experimental periods. In September, however, T. serpyllum
wilted as did other prostrate carpet species when they were planted
together with S. album, and these results might be due to the deficit of
soil water content due to the growth of T. serpyllum.
4.2. The other factors to affect the impact of companion planting with
S. album
Our results indicated that health score of several non-carpet species
(C. nepeta, L. officinalis and R. officinalis ‘Erectus’) were not improved

Table 9
The effects of companion planting with S. album on soil water content of nectar-producing plants in Experiment 2. Student t-tests were performed between monoculture
(nectar plants only) and mixture (companion planting with S. album) treatments (n = 4).
Plant species Mean value of soil water content (100×m3/m3) Growth form

June July

1 individual With S. album p-value 1 individual With S. album p-value

Thymus longicaulis 10.56 ± 2.20 10.84 ± 1.90 0.92 18.76 ± 0.88 18.64 ± 2.04 0.85 Carpet
Lavandula stoechas 6.92 ± 1.02 10.07 ± 4.63 < 0.05 13.98 ± 2.07 20.29 ± 2.37 < 0.05 Non-Carpet
Melissa officinalis 11.27 ± 0.86 13.16 ± 0.43 < 0.05 15.35 ± 1.58 20.46 ± 2.44 < 0.05 Non-Carpet

7
T. Matsuoka et al.
significantly by companion planting with S. album (Fig. 2), and the de­
gree of the improvement in soil water content by companion planting
with S. album were lower than that in other non-carpet species (Table 1).
Despite this, there were no significant differences in dry weights of
neighboring S. album in all non-carpet species (Fig. 4), suggesting that
there might be no detectable net effect of inter-specific competition in
the modules. However, these results also indicate a possibility that the
growth of S. album was not sufficient to induce positive effects on
neighbors. C. nepeta, L. officinalis and R. officinalis ‘Erectus’ grow only
upright and do not show horizontal growth, suggesting that the plant
cover rate might be less than other non-carpet species in early stages of
the experiments (Tuttolomondo et al., 2017). Additionally, R. officinalis
‘Erectus’ and R. officinalis ‘Prostratus’ showed different responses to
companion planting with S. album (Fig. 1), though they are varieties of
the same species. Thus, these results may also indicated the importance
of the amount of plant cover to induce positive effects of companion
planting on the health condition of nectar-producing plants. Ahmed
et al. revealed that positive effects of companion planting with Sedum on
plant species with erect stems were observed only in relatively mature
stages of community development (e. g. 14-week-old herbs) (Ahmed
et al., 2017). Thus, health score of C. nepeta, L. officinalis and R. officinalis
‘Erectus’ planted together with S. album may be improved in a long term
experiment. However, further studies should examine the detailed re­
lationships between companion planting and timing of experimental
drought periods. Related to the planting timing of experimental periods,
we used different nectar-producing species in Experiment 1 and Experi­
ment 2. However, there were no plant species which finished repro­
ductive phase, and thus the decrease in health score during the
experimental periods would be due to the drought treatment in this
study. Nevertheless, further investigations can reveal the relationship
between the effects of companion planting and phenological traits.
Moreover, it must be noted that plant size and combination patterns
would also affect the health conditions of nectar-producing plants. In
M. pudica, which was planted together with S. album, the health con­
dition was higher and dry shoot weight was lower than that in
R. officinalis ‘Prostratus’ (Figs. 2 and 3). Larger plant species tend to have
higher water requirements due to their ET (Beeson, 2006), and the de­
gree of drought stress might not be so severe due to the small plant size
of M. pudica in this experiment. Nevertheless, health score of neigh­
boring carpet species (e. g. P. canescens, T. repens and T. serpyllum) and
larger non-carpet species (e. g. L. officinalis, R. officinalis ‘Erectus’) were
not improved significantly by companion planting with S. album, in spite
of their large plant size (Figs. 2 and 3). Therefore, we suggest that plant
size of nectar-producing plants could be one of the factors to affect their
performance in companion planting. Additionally, we used three
nectar-producing plants on the roof, instead of one to achieve enough
cover of the substrate in Experiment 2. The comparison between single
individuals in Experiment 1 and lower density of conspecifics in Experi­
ment 2 would be a harsh trial to evaluate detailed ability for S. album to
facilitate plant growth as the nectar plants are growing in a low density
setting. Therefore, further research is necessary to complement the ef­
fects of combination patterns on the impact of companion planting with
S. album.
5. Conclusion
Growth form had a minor effect on the impact of companion planting
with Sedum. Companion planting with S. album had no net positive ef­
fects on dry shoot weight of nectar-producing plants in both carpet and
non-carpet species. However, our results indicated that there were no
net negative effects of competition between non-carpet species and
Sedum species, so spatially complementary growth forms could be
important for selecting effective combinations to improve plant health
conditions on green roofs. Additionally, the increase in soil water con­
tent due to the suppression of water loss might be one of the factors
involved in the positive effects of companion planting on the health
8
Urban Forestry & Urban Greening 56 (2020) 126875
condition of neighbors. Therefore, there is a possibility that growth form
could be one of the factors determining the impact of companion
planting with Sedums. Further research is necessary to confirm repro­
ducibility in terms of grouping effective or non-effective growth forms
on companion planting with CAM plants, and other factors of inter-
specific interactions such as competition for soil nutrients and light.
Funding information
This work was carried out by Support Program for Urban Studies by
the Obayashi Foundation. (References: https://www.obayashifoundat
ion.org/english/urbanstudies/).
CRediT authorship contribution statement
Tatsuya Matsuoka: Conceptualization, Methodology, Investigation,
Writing - original draft, Funding acquisition. Kazuaki Tsuchiya:
Methodology, Formal analysis, Writing - review & editing. Susumu
Yamada: Methodology, Resources, Writing - review & editing. Jeremy
Lundholm: Software, Formal analysis, Writing - review & editing.
Toshiya Okuro: Methodology, Resources, Writing - review & editing,
Supervision, Project administration.
Declaration of Competing Interest
The authors declare no conflicts of interest associated with this
manuscript.
Acknowledgements
We are especially grateful to Mr. Yusei Ishikawa and Mr. Shinji Kudo
for various supports for this research at the Institute for Sustainable
Agro-ecosystem Services of the University of Tokyo. We would also like
to express my great thanks to Mr. Junki Mugita, Mr. Kosuke Hara, Mr.
Jun Yoshikawa, Ms. Sakura Sawano, Ms. Sakine Shinohara, Ms. Haruka
Ikematsu, Ms. Risa Hotoda, Mr. Ryuri Koyama, Mr. Kazuto Sakai, Ms.
Rena Honta, Ms. Riko Fujita and the staffs in Kyoiku Plaza Hirai for
constant supports for the experiments in this research.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.ufug.2020.126875.
References
Ahmed, S., Buckley, S., Stratton, A.E., Asefaha, F., Butler, C., Reynolds, M., Orians, C.,
2017. Sedum groundcover variably enhances performance and phenolic
concentrations of perennial culinary herbs in an urban edible green roof. Agroecol.
Sustain. Food Syst. 41 (5), 487–504.
Baldock, K.C., Goddard, M.A., Hicks, D.M., Kunin, W.E., Mitschunas, N., Osgathorpe, L.
M., Potts, S.G., Robertson, K.M., Scott, A.V., Stone, G.N., Vaughan, I.P., Memmott, J.,
2015. Where is the UK’s pollinator biodiversity? The importance of urban areas for
flower-visiting insects. Proc. R. Soc. B 282 (1803).
Beeson, Jr.R.C.(, 2006. Relationship of plant growth and actual evapotranspiration to
irrigation frequency based on management allowed deficits for container nursery
stock. J. Am. Soc. Hortic. Sci. 131 (1), 140–148.
Black, C.C., Osmond, C.B., 2003. Crassulacean acid metabolism photosynthesis: ‘working
the night shift’. Photosyn. Res. 76, 329–341.
Brooker, R.W., 2006. Plant-plant interactions and environmental change. New Phytol.
171, 271–284.
Butler, C., Orians, C.M., 2009. Sedum facilitates the growth of neighboring plants on a
green roof under water limited conditions. In: Proc. 7th Intl. Green Roof Conf.
Greening Rooftops for Sustainable Communities, 7, pp. 1–14.
Butler, C., Orians, C.M., 2011. Sedum cools soil and can improve neighboring plant
performance during water deficit on a green roof. Ecol. Eng. 37, 1796–1803.
Callaway, R.M., Walker, L.R., 1997. Competition and facilitation: a synthetic approach to
interactions in plant communities. Ecology 78 (7), 1958–1965.
Campolo, O., Zappala, L., Malacrino, A., Laudani, F., Palmeri, V., 2015. Bees visiting
flowers of Thymus longicaulis (Lamiaceae). Off. J. Soc. Bot. Ital. 150 (6),
1182–1188.
T. Matsuoka et al.
Cardinale, B.J., Duffy, J.E., Gonzalez, A., Hooper, D.U., Perrings, C., Venail, P.,
Narwani, A., Mace, G.M., Tilman, D., Wardle, D.A., Kinzig, A.P., Daily, G.C.,
Loreau, M., Grace, J.B., Larigauderie, A., Srivastava, D.S., Naeem, S., 2015.
Biodiversity loss and its impact on humanity. Nature 486, 59–67.
Castleton, H.F., Stovin, V., Beck, S.B.M., Davison, J.B., 2010. Green roofs; building
energy savings and the potential for retrofit. Energy Build. 42 (10), 1582–1591.
Chwil, M., 2009. Flowering biology and nectary structure of Melissa officinalis L. Acta
Agrobot. 62 (2), 23–30.
Colla, S.R., Willis, E., Packer, L., 2009. Can green roofs provide habitat for urban bees
(Hymenoptera: Apidae)? Cities Environ. 2 (1), 4.
Connell, J.H., 1983. On the prevalence and relative importance of interspecific
competition: evidence from field experiments. Am. Nat. 122, 661–696.
Cook-Patton, S.C., Bauerle, T.L., 2012. Potential benefits of plant diversity on vegetated
roofs: a literature review. J. Environ. Manage. 106, 85–92.
Eriksson, A., 1998. Regional distribution of Thymus serpyllum: management history and
dispersal limitation. Ecography 21 (1), 35–43.
Grover, J.P., 1997. Resource Competition. Chapman & Hall, London.
Heim, A., Lundholm, J., 2014. Species interactions in green roof vegetation suggest
complementary planting mixtures. Landsc. Urban Plan. 130, 125–133.
Heim, A., Lundholm, J., Philip, L., 2014. The impact of mosses on the growth of
neighboring vascular plants, substrate temperature, and evapotranspiration on an
extensive green roof. Urban Ecosyst. 17, 1119–1133.
Herrera, J., 1993. Blooming times of individual inflorescences and plants as determinants
of flower and fruit predation in Lavandula stoechas (Lamiaceae). Acta Oecol. 14 (6),
867–874.
Japan Beekeeping Association, 2017. Japanese Major Nectar Source. http://www.beekee
ping.or.jp/nectarsources/.
Jones, E.L., Leather, S.R., 2012. Invertebrates in urban areas: a review. Eur. J. Entomol.
109, 463–478.
Kimbrough, K.A., Swift, C.E., 2009. Growing Lavender in Colorado. Colorado State
University Extension, p. 245. Fact Sheet No.7.
Klein, A.M., Vassiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S., Kremen, C.,
Tscharntke, T., 2007. Importance of pollinators in changing landscapes for world
crops. Proc. R. Soc. B 274, 303–313.
Leffler, A.J., Peek, M.S., Ryel, R.J., Ivans, C.Y., Caldwell, M.M., 2005. Hydraulic
redistribution through the root systems of senesced plants. Ecology 86, 633–642.
Lundholm, T.J., 2015. Green roof plant species diversity improves ecosystem
multifunctionality. J. Appl. Ecol. 52, 726–734.
Lundholm, J., MacIvor, J.S., MacDougall, Z., Ranalli, M., 2010. Plant species and
functional group combinations affect green roof ecosystem functions. PLoS One 5
(3), e9677.
MacIvor, J.S., 2016. Building height matters: nesting activity of bees and wasps on
vegetated roofs. Isr. J. Ecol. Evol. 62 (1–2), 88–96.
Urban Forestry & Urban Greening 56 (2020) 126875
MacIvor, J.S., Lundholm, J., 2011. Performance evaluation of native plants suited to
extensive green roof conditions in a maritime climate. Ecol. Eng. 37, 407–417.
Matsuoka, T., Tsuchiya, K., Yamada, S., Lundholm, J., Okuro, T., 2019. Value of Sedum
species As Companion Plants for Nectar-producing Plants Depends on Leaf
Characteristics of the Sedum. Urban Forestry and Urban Greening 39:
35–44Millennium Ecosystem Assessment. (2005) Ecosystems and Human Well-
being. Island Press, Washington, DC.
Monterusso, M.A., Rowe, D.B., Rugh, C.L., 2005. Establishment and persistence of Sedum
spp. And native taxa for green roof applications. HortScience 40 (2), 391–0396.
Mulder, C.P.H., Uliassi, D.D., Doak, D.F., 2001. Physical stress and diversity-productivity
relationships: the role of positive interactions. PNAS 98 (12), 6704–6708.
Nagase, A., Dunnett, N., 2010. Drought tolerance in different vegetation types for
extensive green roofs effects of watering and diversity. Landsc. Urban Plan. 97,
318–327.
Oberndorfer, E., Lundholm, J., Bass, B., Coffman, R.R., Doshi, H., Dunnett, N., Gaffin, S.,
Köhler, M., Liu, K.K.Y., Rowe, B., 2007. Green roofs as urban ecosystems: ecological
structures, functions, and services. BioScience 57 (10), 823–833.
Richards, J.H., Caldwell, M.M., 1987. Hydraulic lift: substantial nocturnal water
transport between soil layers by Artemisia tridentate roots. Oecologia 73, 486–489.
Roscher, C., Thein, S., Schmid, B., Scherer-Lorenzen, M., 2008. Complementary nitrogen
use among potentially dominant species in a biodiversity experiment varies between
two years. J. Ecol. 96 (3), 477–488.
Sasaki, M., 2010. Bee’s eye view of flowering plants: nectar- and pollen-source plants and
related honeybee products. Kaiyusha.
Schoener, T.W., 1983. Field experiments on interspecific competition. Am. Nat. 122,
240–285.
Schwinning, S., Weiner, J., 1998. Mechanisms determining the degree of size asymmetry
in competition among plants. Oecologia 113, 447–455.
Starry, O., Lea-Cox, J.D., Kim, J., van Iersel, M.W., 2014. Photosynthesis and water use
by two Sedum species in green roof substrate. Environ. Exp. Bot. 107, 105–112.
Tilman, D., 1994. Competition and biodiversity in spatially structured habitats. Ecology
75 (1), 2–16.
Tuttolomondo, T., La Bella, S., Leto, C., Gennaro, M.C., Calvo, R., D’Asaro, F., 2017.
Biotechnical characteristics of root systems in erect and prostrate habit Rosmarinus
officinalis L. Accessions grown in a Mediterranean climate. Chem. Eng. Trans. 58,
769–774.
Vasl, A., Shalom, H., Kadas, G.J., Blaustein, L., 2017. Sedum-Annual plant interactions on
green roofs: facilitation, competition and exclusion. Ecol. Eng. 108, 318–329.
Yamada, Y., Sone, Y., Furuya, K., 2011. A study on honeybee projects as an activity to
create chances to experience and enhance understanding of nature in an urban area.
J. Jpn. Inst. Landsc. Archit. 74 (5), 585–590.
Young, T.M., Cameron, D.D., Phoenix, G.K., 2017. Increasing green roof plant drought
tolerance through substrate modification and the use of water retention gels. Urban
Water J. 14 (6), 551–560.