G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

Landscape and Urban Planning xxx (2012) xxx–xxx

Contents lists available at SciVerse ScienceDirect

Landscape and Urban Planning

jou rnal homepage: www.elsevier.com/locate/landurbplan

Biodiversity in urban ecosystems: and macromycetes as indicators for

conservation planning in the city of Coimbra (Portugal)

Lurdes Barrico , Anabela Marisa Azul, Maria Cristina Morais, António Pereira Coutinho, Helena Freitas,

Paula Castro

Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal

a r t i c l e i n f o a b s t r a c t

Article history: Urban landscapes support a high and rich diversity often occurring as unusual or unique communities.

Received 26 May 2011

Urban green areas are a vital part of the urban landscape, providing contact with wildlife and environ-

Received in revised form 8 February 2012

mental services with additional socio-ecological benefits to the overall quality of life. The composition

Accepted 14 February 2012

and diversity of vascular plants and macromycetes were assessed in an urban green area of the city of

Available online xxx

Coimbra (central Portugal) comprising three landscape types (Oak-, Eucalyptus-, and Olive-stands), with

historical periurban agriculture and forest uses. We recorded 287 taxa of plants, including three taxa with

Keywords:

important ecological value (Quercus suber, Quercus faginea subsp. broteroi and Ruscus aculeatus) and 96

Biodiversity

taxa of macromycetes. The pattern of land use resulted in the establishment of different and soil

Urban green area

fungal communities’ composition and diversity among these landscapes. The plant richness and diversity

Vascular plants

Macromycetes indices revealed similar trends within the landscape types, with the highest values found in the Olive-

Land use stands due to the presence of herbaceous that decreased with tree cover density. Richness and diversity

Bioindicators of macromycetes were higher in Oak-stands especially the symbiotic ectomycorrhizal (ECM) fungal com-

munities. Although not significant, higher saprobic fungi richness and diversity values were found in the

Eucalyptus-stands. Given the undoubted ecological complexity of urban green areas and the value of

these ecosystems for society in terms of goods and services, it is imperative to select bioindicators that

are readily accessible and reliable to design balanced urban ecosystems by linking wildlife and biological

parameters to human well-being.

© 2012 Elsevier B.V. All rights reserved.

1. Introduction loss of biodiversity by promoting the replacement of native species

with non-native counterparts, leading to the extinction of some

Landscapes across the world have been severely affected by species and to biotic homogenization (Chapin et al., 2000; Kowarik,

human activities since the second half of the 20th century (EEA, 2011; Mckinney, 2006).

2006). A major concern involving human impact is a rise in urban- In the past decade, studies and discussions focusing on bio-

ization, associated with the rapid growth of the world’s population logical diversity have become one of the most pressing and

and the consequent transformation of rural and natural landscapes important topics for the scientific community, environmental pol-

(Keles¸ , Sivrikaya, C¸ akir, & Köse, 2008). Although urban landscapes icy makers and forestry planners (Dana, Vivas, & Mota, 2002;

occupy only approximately 4% of the earth’s surface (UN, 2008), 75% Gustafsson, Appelgren, & Nordin, 2005; Jooss, Geissler-Strobel,

of the population in developed countries lives in urban settlements Trautner, Hermann, & Kaule, 2009). Biodiversity is an important

with a corresponding 29% of the population in less developed coun- component of any ecological system that promotes functional

tries (UNFPA, 2009). In Portugal, approximately 60% of the total diversity and improves ecological stability by influencing the resis-

population inhabits urban areas (UNFPA, 2009). tance and resilience to environmental change (Chapin et al., 2000;

Urban landscapes are complex ecological systems, affected by Peterson, Allen, & Holling, 1998) and is therefore crucial to the over-

human practices that have increasingly altered biogeochemical all quality of life. In this context, urban green spaces have gradually

cycles and contributed to the deterioration of natural habitats and become recognized as important local habitats in urban systems.

In Portugal, urban gardens and green spaces have also been

identified for a long time as major contributors to the physi-

∗ cal and aesthetic quality of neighbourhoods (Loures, Santos, &

Corresponding author. Tel.: +351 239 855210; fax: +351 239 855211.

Panagopoulos, 2007). In the 1940s, city managers determined that

E-mail addresses: [email protected] (L. Barrico), [email protected]

urban growth in Coimbra (in the central region of Portugal) should

(A.M. Azul), [email protected] (M.C. Morais), [email protected] (A. Pereira Coutinho),

[email protected] (H. Freitas), [email protected] (P. Castro). follow the “garden-city” concept in which the urban area would

0169-2046/$ – see front matter © 2012 Elsevier B.V. All rights reserved.

doi:10.1016/j.landurbplan.2012.02.011

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

2 L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx

Fig. 1. Location of the study site and the three landscape types.

be bounded by a rural landscape – the green belt – containing no provide a recreational resource for local residents (Chiesura, 2004;

urban development (Santos, 1983). This green belt would serve as Van Herzele & Wiedemann, 2003), contribute towards carbon

a reservoir of clean air, as protection against the encroachment of sequestration and generate both food and habitats for other organ-

other urban centres, and as a supplier of agricultural products. This isms (Davies, Edmondson, Heinemeyer, Leake, & Gaston, 2011;

type of agriculture, within the city boundaries or in the immediate Mathieu, Freeman, & Aryal, 2007). Soil fungi play a pivotal role

surroundings, is nowadays generally defined as periurban agricul- in decomposition and nutrient cycling in terrestrial ecosystems

ture (FAO, 2007). These areas are of extreme importance due to the and influence the establishment and dynamic succession of plant

services they may provide to cities, and should be taken into con- communities (Smith & Read, 2008). Certain soil fungi establish a

sideration in any territorial development policies. The Santa Clara symbiotic relationship with roots of plants, called mycorrhizas,

Plateau (SCP) represents one example of Coimbra’s periurban agri- that is widely recognized as mediators between soil processes

culture area where no urban infrastructures were allowed until and plant community, by enhancing nutrient acquisition, drought

the 1990s. Soil management associated with agriculture and for- tolerance, and pathogen resistance of their hosts (Smith & Read,

est uses over several decades resulted in three distinct landscape 2008), whereas saprobic fungi have been shown to remobilize and

types in the SCP. This mosaic within SCP offers an excellent case translocate biomass and store mineral nutrients. Several ectomyc-

study, not only because of the historical periurban use, but also orrhizal (ECM) fungal species, predominantly basidiomycetes and

due to two potential environmental risks in the area: (i) fire, asso- some ascomycetes, likely have similar functions in nutrient cycling

ciated with the forest–urban interface, and (ii) pressures associated (Finlay, 2008). In Mediterranean Basin ecosystems all major types

with urban and commercial growth, particularly in the last tweenty of mycorrhiza can co-exist, depending on the plant community

years. Moreover, the SCP evaluation of biodiversity parameters rep- structure and the stage of ecological succession.

resents a unique example to explore biological conservation and We hypothesized that the pattern of land use in the SCP has

include collaborative reflections on urban design strategies and influenced the establishment of the floristic and macromycete com-

planning decisions. munities, resulting in different plant and soil fungal community

The value of wildlife and native biota in urban green areas composition and diversity among landscapes. In order to evaluate

is often underestimated and its socio-ecological functions have these differences, we determined the composition and diversity

not been comprehensively studied (EEA, 2010). Assessing, under- of flora and macromycetes in the three different landscape types

standing, and improving urban biodiversity is of great importance that currently characterize this green area. The study also aims

from both conservation and social point of views (Kowarik, 2011). to provide relevant information for policy makers to design bal-

Two important biological and ecological components in these anced urban ecosystems by linking biological indicators to human

systems include vegetation and soil fungi (in particular, the sym- well-being.

biotic and the decomposers). The vegetation component provides

important environmental services, such as stabilization of stream 2. Materials and methods

banks, moderation and improvement of storm water flow, and

conversion of nitrate pollution to harmless gaseous nitrogen, in 2.1. Study site

addition to contributing towards the sustainability of urban areas

and helping to recharge water tables (Chiesura, 2004; Grove, Troy, The study was conducted in the Santa Clara Plateau (SCP;

◦  ◦ 

O’Neil-Dunne, Burch, Cadenasso, & Pickett, 2006). Furthermore, 40 21 N, 8 45 W), an urban green area (54.2 ha) in the centre of

vegetation can improve climatic conditions within urban areas, Coimbra (Fig. 1). The SCP is influenced by a Mediterranean climate,

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx 3

characterized by warm, dry summers and mild, humid winters. Plant taxa were identified according to Castroviejo et al.

The average annual temperature and total annual precipitation is (1986–2010) and Franco & Afonso (1971–2003) and plant spec-

around 15 C and 900 mm, respectively (CMC, 2008). The geolog- imens from the Herbarium of University of Coimbra. English

ical formation is composed of dolomite and calcareous rock, and common names and potential uses were described according to

a soil type consisting of Podzols, associated with Eutric Cambisols Cunha, Silva, and Roque (2003), Garrido-Lestache (2001), Huxley,

(APA, 1971). The SCP stands on the left bank of the River Mon- Griffiths, and Levy (1992), Mabberley (2008) and Wink and van Vyk

dego and is surrounded by two growing urban areas: Santa Clara (2008). The invasive plant taxa were classified in accordance with

in the south and S. Martinho do Bispo in the northwest, both of Portuguese law (Ministério do Ambiente, 1999).

which put pressure on land natural resources at local and regional

levels. 2.3. Macromycete survey

Since the 1950s this area has been occupied by some scattered

urban buildings for forestry and agricultural use, similar to the situ- This study focused exclusively on the macromycete community

ation described by Pato, Tavares, and Magalhães (2008) regarding a – saprobic and ectomycorrhizal fungi – based on fruiting bodies.

small-scale hydrological basin in an area adjacent to the SCP (on the Although fruit bodies’s production is unlikely to reflect the below-

western side). However, given its role as a green support area for the ground fungal community (Lilleskov & Bruns, 2001), surveys can

city of Coimbra, the pattern of land use development in the SCP was be particularly valuable as indicators for assessing the impacts of

different from the scenario described by Pato et al. (2008), as urban different land use types on macromycete populations, as observed

settlements did not emerge. However, the trend towards replacing by Azul, Castro, Sousa, and Freitas (2009).

agricultural areas with forest and/or abandoned areas is similar to In 2008 and 2009, four plots of 20 m × 20 m were randomly

what took place in the hydrological basin. Consequently, land use selected in each landscape type. We considered a minimum dis-

fragmented the SCP into three major landscape types, designated tance of 100 m per plot to guarantee the fruiting incidence to be

in this study as Oak-stands, Olive-stands and Eucalyptus-stands. independent among the neighbouring plots. Field surveys included

The Oak-stands (11.7 ha) are dominated by the evergreen cork oak the species richness and abundance of macromycetes, following the

(Quercus suber), with many Mediterranean native taxa present. methodology used by Azul et al. (2009), and were carried out every

The Olive-stands (11.3 ha) consist of old olive plantations (Olea two weeks during the main fruiting period (October–December).

europaea) in which extensive agro-pastoral activities take place, The clumped distribution was determined by counting the fruit

with natural pastures used for grazing sheep alternating with crop bodies. The observations did not include species forming hypo-

production. The Eucalyptus-stands (10.6 ha) correspond to 40-year geous or resupinate fruit bodies.

plantations of Eucalyptus globulus commercially developed until the Macromycetes were identified according to Bon (1988),

late 1990s, in which the establishment and expansion of invasive Courtecuisse and Duhem (2005) and Gerhardt, Vila, and

plant taxa is more noticeable. The cork oak is a native species from Llimona (2000). Author citations for each taxon are abbreviated

the Mediterranean Basin and is predominantly an ectomycorrhizal according to the Index Fungorum (http://www.index-

(ECM) tree (Smith & Read, 2008). The eucalyptus is an exotic species fungorum.org/names/Names.asp, accessed January 2011). We

(introduced in Portugal in the 19th century) and forms both arbus- used quantification of the fruit bodies instead of biomass analysis

cular mycorrhizas (AM) and ECM (Chilvers, 1968; Smith & Read, to evaluate the macromycete community, as different taxa produce

2008). The olive tree, native from the Mediterranean Basin (long- different sizes of fruit bodies and biomass measurements would

ago introduced in Portugal) establishes AM (Calvente, Cano, Ferrol, have obscured abundant fruiting of smaller macromycetes.

Azcón-Aguilar, & Barea, 2004; Meddad-Hamza et al., 2010).

2.4. Data analysis

2.2. Floristic survey

The plant and macromycete diversity in each plot was estimated

The floristic survey was conducted in the spring of 2008 and using the following descriptors: (1) species richness (S) the total

2009 and comprised three different steps. The first step was car- number of taxa sampled within a plot; (2) the Shannon–Wiener



ried out in the spring of 2008 and involved a preliminary floristic diversity index (H ) which combines species richness with relative

inventory. The taxa composition was sampled randomly by walk- abundance; (3) Simpson’s diversity index (1/D) which is heavily

ing along the network of paths within the study site and also along weighted towards the most abundant taxa in the sample while



their edges, following the methodology used by Santos, Kinoshita, being less sensitive to species richness; (4) Pielou’s evenness (J )

and Rezende (2009). The site was thoroughly searched (about 80% and (5) Simpson’s evenness (E1/D) equitability indices which quan-

of the total area) until no new taxa were discovered. In step two, the tify how equal the community is numerically (Magurran, 2004). The

three major landscape types were defined, and their spatial distri- importance value (IV) was calculated for all plant taxa in each land-

bution and extent mapped using geographic information software scape type using the formula: IVi = RCi + RFi, in which RCi and RFi are

®

(ArcInfo 10) (ESRI, Redlands, CA, USA). Finally, in step three, car- the relative cover rate and relative frequency of species i, respec-

ried out in the spring of 2009, a quantitative vegetation analysis tively (Karavas, Georghiou, Arianoutsou, & Dimopoulos, 2005).

was performed, based on determining the presence and abundance This value gives an overall estimate of the dominance of a taxon

of individual taxa in the three major landscape types. Within each within the community (Curtis & McIntosh, 1951). Macromycete

landscape type, 12 plots of 5 m × 5 m with nested plots of 3 m × 3 m data analysis also included: (1) taxon abundance, estimated as the

and 2 m × 2 m used for sampling trees, shrubs and herbaceous taxa, cumulative number of fruit bodies produced by a given taxon dur-

respectively, were selected using the methodology described by ing the two consecutive fruiting seasons; (2) species frequency,

Lindgren and Sullivan (2001) and Mueller-Dombois and Ellenberg calculated as the percentage within the landscape type in which a

(1974). In each plot, the abundance of each taxon was deter- given taxon fruited at least once during the entire sampling period,

mined by a visual estimate of percentage cover. For this study, (3) fruit body fructification, defined as the total number of fruit

the tree growth-form included taxa that were either adult trees bodies counted over the study period, and (4) relative abundance,

or seedlings. The shrub growth-form included all taxa designated determined as the total number of fruit bodies of a given taxon per

as shrub or woody climbing taxa and the herbaceous growth-form total fruit bodies. Data on macromycetes was pooled within each

comprised all taxa designated as herbaceous or non-woody climb- plot and the differences between the two years of the main fruiting

ing taxa. period (2008 and 2009) were analysed.

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

4 L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx

One-way analysis of variance (ANOVA) and the Tukey test

(p ≤ 0.05) for overall comparisons were used to test for signifi-

cant differences in the species cover and indices calculated for the

different landscape types. All the data were checked for normal-

ity and homogeneity of variance, and transformed if necessary to

meet ANOVA assumptions (Zar, 1996). Statistical analyses were

performed using SPSS 17.0 software for Windows (SPSS Inc., IL, USA).

3. Results

3.1. Floristic inventory

A total of 287 taxa of vascular plants belonging to 66 fami-

lies and 200 genera were found in the study site (Appendix A).

These included 25 trees, 39 shrubs and 223 herbaceous plants.

The three dominant families, Fabaceae (38 taxa), Asteraceae and

Poaceae (34 taxa each), comprised 36% of the total genera and 37%

of the total taxa. In terms of significant biological and conservation

value, the presence of Quercus suber, a species protected under Por-

tuguese law (Ministério da Agricultura, do Desenvolvimento Rural

e das Pescas, 2001), Quercus faginea subsp. broteroi, an endemic

taxa in Portugal, and Ruscus aculeatus, included in Annex V (ani-

mal and plant species of community interest whose taking in the

wild and exploitation may be subject to management measures) of

the Habitats Directive (Directive 92/43/EEC), should be highlighted.

The presence of nine invasive species recognized by Portuguese

law (Ministério do Ambiente, 1999) should also be emphasized, of

which Acacia dealbata, Acacia melanoxylon and Ailanthus altissima

are the most common.

3.2. Richness and diversity of floristic species

The mean species richness ranged from 10.08 (Eucalyptus-

stands) to 13.33 (Olive-stands) (Fig. 2A). Significant differences

Fig. 2. Plant species richness (A) and plant species cover (B) for the three landscape

(p = 0.041) were found between landscape types, with more plant

types. Values are means ± SE. The different letters above the bars indicate significant

taxa found in the Olive-stands. When compared by growth-forms ≤

differences (p 0.05) between landscape types.

(Fig. 2A), there were significant differences in species richness

for trees and herbaceous plants (p < 0.001) and shrubs (p = 0.018)

between the different landscape types. The highest values for trees

both presented the lowest values in Oak-stands (Table 1). When

were found in Eucalyptus- and Oak-stands, while the highest values

analysed by growth-forms, only herbaceous equitability was sig-

for shrubs and herbaceous plants were found in Oak- and Olive-

nificantly lower in the Olive-stands according to the Simpson

stands, respectively.

evenness index (Table 1).

The total species cover ranged from 111% (Oak-stands) to 148%

The highest importance value corresponded to the Quercus taxa

(Eucalyptus-stands) (Fig. 2B), and did not show any significant

in Oak-stands (IV ≈ 33%, Table 2), despite these taxa also presented

differences (p = 0.142) in terms of landscapes. The mean species

a considerable value in Eucalyptus-stands (IV ≈ 12%, Table 2). Trees

cover for growth-forms was significantly different in the landscape

and shrubs jointly represented 87% of the total IV in Eucalyptus-

types for trees and herbaceous (p < 0.001) and shrubs (p = 0.002).

stands, while herbaceous plants (≈70%) were clearly dominant

The highest values corresponded to trees in Eucalyptus- and Oak-

in Olive-stands (Table 2). It is worth noting that Ruscus aculea-

stands, shrubs in Eucalyptus-stands and herbaceous plants in

tus (Annex V of the Habitats Directive) was found in both Oak-

Olive-stands.

and Eucalyptus-stands, but with a higher IV in the former. Table 2

Although the Shannon and Simpson diversity indices did

also illustrates the importance of the two invasive Acacia species

not reveal any significant differences between landscape types

(A. melanoxylon and A. dealbata) in the Eucalyptus-stands, which

(p = 0.137 and p = 0.175, respectively), Olive-stands had the high-

together represented almost 9% of the total IV.

est values (Table 1), mainly as a result of the many herbaceous taxa

present, whereas tree and shrub taxa dominated in the other two

landscapes (Tables 1 and 2). With regard to growth-forms, the two 3.3. Macromycete inventory

diversity indices showed similar tendencies among growth-forms

with the highest value found in Eucalyptus-stands for trees, Olive- Overall, 6109 fruit bodies were recorded in the three landscape

stands for herbaceous plants and Oak-stands for shrubs (Table 1). types during the two consecutive fruiting seasons (Table 3). We

Nevertheless, the Shannon diversity index was significantly differ- registered 96 taxa consisting of 36 ECM fungi and 60 saprobic

ent in terms of vegetation types for trees (p = 0.010) and herbaceous fungi (Appendix B); the genera Russula (9 taxa), Amanita (6 taxa),

plants (p = 0.015) and the Simpson diversity index was significantly Mycena (5 taxa), and Scleroderma (5 taxa) were the best repre-

different only for shrubs (p = 0.013). sented. Macromycetes of economic interest were represented by

Despite the fact that the Pielou and Simpson evenness several edible species (Appendix B) and three medicinal species

indices did not differ significantly between landscape types, Fomes fomentarius, Schizophyllum commune and Trametes versicolor.

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx 5

Table 1

±

Descriptive statistics of different diversity indices for vascular plants present in the three landscape types. Values are means SE. The different letters and (*) indicate

significant differences (p ≤ 0.05) between landscape types.

Oak-stands Olive-stands Eucalyptus-stands F p



Shannon’s diversity index (H )

Total diversity 1.42 ± 0.12 1.63 ± 0.12 1.32 ± 0.08 2.11 0.137

Growth-form

Trees 0.52 ± 0.12 ab 0.26 ± 0.10 b 0.68 ± 0.11 a 5.35 0.010*

Shrubs 0.89 ± 0.16 0.42 ± 0.16 0.72 ± 0.07 3.13 0.057

Herbaceous 0.89 ± 0.19 ab 1.32 ± 0.13 a 0.61 ± 0.16 b 4.76 0.015*

Simpson’s diversity index (1/D)

±

± ± Total diversity 3.26 0.39 4.30 0.64 3.12 0.25 1.84 0.175

Growth-form

Trees 1.67 ± 0.21 1.07 ± 0.22 1.77 ± 1.17 3.44 0.053

Shrubs 2.50 ± 0.39 a 1.32 ± 0.44 b 1.86 ± 0.14 ab 4.99 0.013*

Herbaceous 2.32 ± 0.40 3.39 ± 0.57 2.14 ± 0.56 1.69 0.200



Pielou’s evenness index (J )

Total evenness 0.57 ± 0.04 0.63 ± 0.04 0.58 ± 0.03 0.73 0.489

Growth-form

Trees 0.42 ± 0.10 0.33 ± 0.12 0.49 ± 0.06 0.67 0.518

±

±

±

Shrubs 0.57 0.09 0.37 0.11 0.63 0.08 2.06 0.143

Herbaceous 0.53 ± 0.09 0.57 ± 0.04 0.55 ± 0.12 0.06 0.944

Simpson’s evenness index (E1/D)

Total evenness 0.27 ± 0.04 0.32 ± 0.04 0.33 ± 0.03 0.93 0.404

Growth-form

Trees 0.62 ± 0.08 0.67 ± 0.12 0.46 ± 0.04 1.69 0.200

Shrubs 0.65 ± 0.07 0.46 ± 0.11 0.59 ± 0.08 1.13 0.336

±

±

Herbaceous 0.50 ± 0.08 ab 0.34 0.05 b 0.69 0.11 a 4.54 0.018*

3.4. Macromycete richness and diversity the Eucalyptus-stands was particularly evident for the saprobics

Coprinellus micaceus and Cyathus striatus, with 209 and 174 fruit

Macromycetes diversity and abundance were distinct in the bodies, respectively. These two species together accounted for 11%

three landscape types. The species richness of the macromycete of the total community.

community was statistically different (p = 0.037), with higher val- Patchiness in the ECM and saprobic fungal community was

ues found in Oak-stands, in particular, for the ECM fungi community consistently observed during the 2 years study in the Oak- and

(Tables 3 and 4). The saprobic community dominated in all land- Eucalyptus-stands. Olive-stands registered the lowest fructifica-

scape types in which, about 85% consisted of basidiomycetes. tion with about 32% of the total macromycetes taxa (across all sites)

As a macromycete group, ECM fungi include a wide range of (Table 3). The saprobic community was represented by 30 taxa. The

ascomycetes and basidiomycetes with different host specificity clumped distribution of fruit bodies was observed for Marasmius

(Molina, Massicotte, & Trappe, 1992), but in this study only basid- oreades, with 347 fruit bodies, that accounted for 30% of the total

iomycetes were recorded. fruit bodies. The species Scleroderma polyrhizum was the only ECM

Clumped distribution of fruit bodies in the Oak-stands, was par- fungi present in these stands.

ticularly noticeable for the ECM species Astraeus hygrometricus and Significant differences were noticed in the Shannon diversity

Laccaria laccata, with 212 and 101 fruit bodies, respectively, and the index for the ECM community (p = 0.000), with the highest val-

saprobic species Marasmius oreades, with 206 fruit bodies. These ues obtained in the Oak-stands (Table 4). The Simpson diversity

three species together accounted for 33% of the total fruit bodies index exposed significant differences between the three landscape

observed. types for the total macromycetes diversity (p = 0.045) and the ECM

Although not significant (p = 0.147), the Eucalyptus-stands community (p = 0.024), also with highest values registered in Oak-

showed higher fructification values (Table 4), particularly due to stands (Table 4). The Pielou and Simpson evenness indices showed

the abundance of Laccaria laccata, with 1345 fruit bodies evenly different distribution patterns between the three landscape types

distributed in the plots. Clumped distribution of fruit bodies in and communities (Table 4).

Table 2

Importance value (IV) of the taxa found in the three landscape types (only the 15 taxa with highest values are recorded).

Oak-stands Olive-stands Eucalyptus-stands

Taxon IV (%) Taxon IV (%) Taxon IV (%)

Quercus suber 24.58 Olea europaea 11.64 Eucalyptus globulus 26.09

Quercus faginea subsp. broteroi 8.19 Brachypodium distachyon 7.97 Rubus ulmifolius 10.06

Rubus ulmifolius 7.10 Dactylis glomerata 7.57 Acacia melanoxylon 7.43

Hedera maderensis subsp. iberica 6.45 Hyparrhenia hirta 5.43 Ulex europaeus subsp. latebracteatus 7.15

Laurus nobilis 4.36 Crataegus monogyna 4.59 Lonicera periclymenum 6.86

Lonicera periclymenum 3.98 Poa pratensis 3.09 Quercus suber 6.28

Rosa canina 2.87 Rhamnus alaternus 3.05 Quercus faginea subsp. broteroi 5.66

Rubia peregrina 2.81 Asparagus aphyllus 2.74 Hedera maderensis subsp. iberica 3.71

Dactylis glomerata 2.38 Avena alba 2.59 Rubia peregrina 2.54

Osyris alba 2.26 Dittrichia viscosa 2.50 Rosa canina 2.00

Geranium purpureum 2.09 Rubia peregrina 2.46 Tamus communis 1.77

Briza maxima 2.08 Origanum virens 2.41 Oxalis corniculata 1.66

Daphne gnidium 1.99 Rosa canina 1.99 Acacia dealbata 1.39

Ruscus aculeatus 1.81 Vicia sativa 1.92 Pinus pinaster 1.33

Crataegus monogyna 1.78 Rubus ulmifolius 1.83 Crataegus monogyna 1.30

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

6 L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx

Table 3

Total macromycete taxa and fruit bodies, over the two years of fruiting seasons, for the three landscape types.

Community Oak-stands Olive-stands Eucalyptus-stands

Taxa Fruit bodies Taxa Fruit bodies Taxa Fruit bodies

ECM fungi 29 697 1 22 13 1883

Saprobes 43 879 30 1149 40 1479

Total 72 1576 31 1171 53 3362

% ECM fungi in macromycetes community 40 44 3 2 25 56

4. Discussion The plant diversity and richness indices showed similar trends

among the landscape types, with variations in the overall stands

Although the total area allocated to periurban land in the depending on the dominant canopy. Although not significantly dif-

Santa Clara Plateau has remained substantially the same in recent ferent, the highest values were found in the Olive-stands, declining

decades, the patterns of agriculture and forest uses have led to as the tree canopy increased (Table 1 and Fig. 2). When analysed

important changes in the establishment and spatial dominance of by growth-forms, the Olive-stands showed the lowest and highest

plant communities. Shannon diversity index for trees and herbaceous plants, respec-

The overall results obtained from this study revealed the pres- tively (Table 1). Consistent with this result, previous studies have

ence of a considerable diversity of plants and macromycetes in the demonstrated that greater biodiversity may exist in open wood-

SCP urban green area. In total, 287 taxa of vascular plants and 96 lands than in forests with closed canopies (Pérez-Ramos, Zavala,

taxa of macromycetes were recorded, 37.5% of them ectomycor- Maranón,˜ Díaz-Villa, & Valladares, 2008; Peterson & Reich, 2008;

rhizal. The diversity of vascular plants found in the SCP represents Rad, Manthey, & Mataji, 2009), and that the ground flora in Olive-

8.7% of the total taxa found in Portugal (Crespí et al., 2011). With stands is dominated by herbaceous plants (Allen, Randall, Amable,

regard to macromycete’s communities, the diversity corresponds & Devereux, 2006). In contrast, the Eucalyptus-stands showed the

to 41% of the total taxa observed in old-growth Mediterranean for- lowest and highest Shannon diversity index for herbaceous species

est dominated by Quercus ilex (Richard, Moreau, Selosse, & Gardes, and trees, respectively (Table 1). The small number of herbaceous

2004) and 56% of the total taxa observed in managed woodlands taxa in Eucalyptus-stands was also evident in their importance val-

dominated by Quercus suber (Azul et al., 2009). ues (Table 2). Fabião et al. (2002) also found that a small number

Moreover, 21% of the vascular plants and several macromycetes of species prevailed in the understory cover in habitats dominated

taxa observed in the SCP may be of multiple potential interest by Eucalyptus sp. In fact, our results suggest that the closed canopy

(e.g. food, aromatics, medicinal, wood, plant fitness, soil protec- observed in the stands may reduce the possibility of regeneration

tion), demonstrating that we should take into account not only the of the undergrowth due to the high growth rate and competi-

biological and ecological perspectives of the landscapes but also tive advantage of Eucalyptus in terms of light, water, and nutrients

their potential products and environmental services with regard to (Carneiro et al., 2008). The presence of some invasive taxa such

future land use and urban life. as Acacia in these stands (Table 2) may also influence the growing

Table 4

±

Descriptive statistics of different diversity indices for macromycete communities present in the three landscape types. Values are means SE. The different letters and (*)

indicate significant differences (p ≤ 0.05) between landscape types.

Oak-stands Olive-stands Eucalyptus-stands F p

Mean species richness (S)

Total species 59 ± 3 a 22 ± 9 b 48 ± 4 ab 11.93 0.037*

Community

ECM 24 ± 2 a 1 ± 0 c 11 ± 3 b 39.10 0.007*

Saprobes 35 ± 1 21 ± 9 36 ± 1 2.96 0.195

Mean abundance (A)

Total abundance 788 ± 70 586 ± 138 1682 ± 489 3.88 0.147

Community

ECM 349 ± 96 11 ± 10 942 ± 266 8.35 0.059

Saprobes 439 ± 25 575 ± 128 719 ± 205 0.99 0.467



Shannon’s diversity index (H )

Total diversity 4.70 ± 0.09 3.25 ± 0.46 3.62 ± 0.08 7.51 0.068

Community

ECM 3.22 ± 0.12 a 0.00 ± 0.00 c 1.36 ± 0.02 b 538.82 0.000*

Saprobes 4.11 ± 0.01 3.20 ± 0.42 4.19 ± 0.11 4.88 0.114

Simpson’s diversity index (1/D)

Total diversity 16.26 ± 2.76 a 6.86 ± 1.56 ab 5.40 ± 0.08 b 10.34 0.045*

Community

ECM 6.40 ± 1.24 a 1.00 ± 0.00 b 1.85 ± 0.08 b 16.32 0.024*

Saprobes 11.01 ± 0.53 6.63 ± 1.36 12.99 ± 1.33 8.12 0.062



Pielou’s evenness index (J )

Total evenness 0.80 ± 0.02 a 0.76 ± 0.00 a 0.65 ± 0.00 b 29.56 0.011*

Community

ECM 0.70 ± 0.04 – 0.40 ± 0.04 22.07 0.043*

Saprobes 0.81 ± 0.01 0.76 ± 0.02 0.81 ± 0.02 4.33 0.131

Simpson’s evenness index (E1/D)

Total evenness 0.06 ± 0.01 0.15 ± 0.04 0.19 ± 0.00 8.87 0.055

Community

ECM 0.16 ± 0.03 – 0.54 ± 0.02 93.49 0.011*

Saprobes 0.09 ± 0.00 0.16 ± 0.03 0.08 ± 0.01 4.80 0.116

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx 7

conditions for herbaceous species (Marchante, Kjøller, Struwe, & The processes influencing ECM fungi ecology and succession

Freitas, 2008). Cork oak showed a high capacity for regenera- remain unclear, but the key role of host plants and land use is

tion (field observations) in this landscape, which is likely due to becoming increasingly recognized (Azul et al., 2009; Buée et al.,

increased seed sources, probably because of the progressive aban- 2010; Diédhiou et al., 2009). Saprobic fungi richness and abun-

donment of the commercial exploitation of Eucalyptus which may dance seemed to be less affected by vegetation composition.

have allowed the habitat to follow the natural succession pro- The greater abundance of saprobic fungi in the Eucalyptus-

cess. stands may be related to the accumulation of dead woody

Oak-stands showed the highest Simpson diversity index for debris and the role they play in decomposition and nutrient-

shrubs (Table 1), including some native species such as Aspara- release processes suggested by Azul et al. (2009) and Azul et al.

gus aphyllus, Myrtus communis, Ruscus aculeatus, Smilax aspera, and (2010).

Viburnum tinus, which are species characteristic of Quercus suber In conclusion, our analysis provides new insights into wildlife

forests. In these stands, Quercus suber and Quercus faginea subsp. and biological paramenters in three distinct landscapes types

broteroi showed the highest importance values (Table 2), jointly in a Mediterranean urban context, underlining four impor-

representing 32%. The flora present in Oak-stands considerably tant findings regarding land use and the specific attributes

increases the biological and conservation values of this type of of each habitat. Firstly, plant and macromycetes composi-

habitat, which should be taken into consideration in any urban tion and diversity were clearly different and dependent on

strategic planning. The biological and ecological importance asso- human intervention in recent decades. Secondly, the Oak-

ciated to Quercus suber ecosystems is widely acknowledged (Azul, stands exhibited a large number of plant and macromycetes

2011; Azul et al., 2009; Pereira & Fonseca, 2003), in addition to their native taxa with high environmental and conservation value,

socio-economic role and value to agroforestry and potential as sus- particularly ECM fungi. Thirdly, our data demonstrated that

tainable management ecosystems (INE, 2009; Pereira, Domingos, in this climate, and when subjected to some level of aban-

Vicente, & Proenc¸ a, 2009). donment, these areas revealed a high potential for regen-

Regarding macromycetes, the diversity and richness indices eration, allowing for the establishment of a natural succes-

also revealed clear differences depending on the landscape type, sion process towards a typical Quercus suber forest. Fourtly,

especially in the ECM macromycetes community (Table 4). The the plant and macromycete communities revealed to be

dominance of vegetation cover and the presence of a broad sensitive indicators of habitat quality in urban ecosystems.

host range species may influence soil fungi fruiting patterns This is of high relevance, particularly for ECM fungi, which

(Azul et al., 2009; Richard et al., 2004). In the SCP, Oak-stands are recognized as a pivotal component of soil in terrestrial

exhibited the highest ECM macromycetes’s diversity values, and ecosystems.

the species richness was 1.2 and 2.7 times higher than that of Analysing and managing urban growth is critically important

Eucalyptus- and Olive-stands, respectively. The ecological value but there is often little support for the decision-making involved

provided by the ECM fungi in this type of landscape is broadly rec- in producing management plans and appropriate measures to

ognized in the literature (Azul et al., 2009; Azul, Sousa, Agerer, meet sustainable development objectives, and frequently land use

Martín, & Freitas, 2010). The significance of ECM fungi in bal- changes do not take the natural biophysical characteristics of land-

ancing ecosystems can be highly relevant, since they can be scapes into consideration (Hietel, Waldhardt, & Otte, 2004). This

used to increase plant resistance/tolerance to abiotic stresses research topic was not covered in our survey, but the study made

(Ahonen-Jonnarth, Göransson, & Finlay, 2003; Colpaert, Wevers, by Pato et al. (2008) on an area adjacent to the Santa Clara Plateau

Krznaric, & Adriaensen, 2011; Finlay, 2008), interact with soil bac- testifies to this poor relationship.

teria (Frey-Klett, Garbaye, & Tarkka, 2007), and protect against The area of the Coimbra municipality presents physical con-

pathogenic fungi, bacteria and nematodes (Compant, Duffy, Nowak, trasts that are crucial and conditional in the natural hazard and

Clément, & Barka, 2005; Duchesne, 1994; Wehner, Antunes, in the risks involved, such as flooding, landmass movements or

Powell, Mazukatow, & Rillig, 2010), with the added advan- wildfires (Tavares, Mendes, Basto, & Cunha, 2010).

tage of improving the vegetative growth and nutrient status Urban Oak-stands are nowadays represented only by very

of the plant with which they established the symbiosis (Smith small, disperse fragments, highlighting the necessity to protect

& Read, 2008). In addition, the extraradical mycelium of ECM and manage them. Besides connecting humans to nature, these

fungi provides a direct pathway for translocation of photosyn- habitats provide additional benefits including cleaner air, resis-

thetically derived carbon to microsites in the soil and a large tance to fire and recreational areas. The preservation of natural

surface area for interaction with other microorganisms (Finlay, processes helps support a functioning city, prevent or mitigate

2008). environmental risks and improve well-being. Thus, biodiversity

The ECM fungi fructification was higher in the Eucalyptus- values and habitat conservation are important issues that should

stands (Table 3), mostly due to the species Laccaria laccata. be considered for the planning of balanced ecosystems in this

However, we believe that the regeneration capacity of the city.

cork oak found in these stands may also have contributed to

increase macromycete’s abundance. Some ECM species, such as

L. laccata and Pisolithus tinctorius, recorded in both Oak- and Acknowledgements

Eucalyptus-stands, form associations with a broader range of

host plants (Parladé, Álvarez, & Pera, 1996). Other ECM fungi Funding for this study was provided by the Project – Protocol

exhibit a much narrower host specificity, including host speci- between the City Council of Coimbra and the Faculty of Sciences and

ficity of genus–species and species–species specificity, such as Technology of the University of Coimbra (FCTUC). Lurdes Barrico

Cortinarius trivialis and Russula amoenolens with angiosperms, Lac- was supported by an individual research grant (CB/C05/2008/113)

tarius chrysorrheus with Quercus sp., and Scleroderma polyrhizum from the FCTUC. We wish to thank Arménio Matos for his help

with Mediterranean shrubs and trees in thermophilic areas. The in the field work and plant identification. We are grateful to the

Eucalyptus-stands shared seven ECM fungi with Oak-stands. The three anonymous reviewers who made valuable comments that

lower presence of ECM fungi in the Olive-stands is due to the fact have helped improving the quality of the manuscript. We also

that, contrary to what is observed for oaks or eucalypus species, wish to thank Catarina Moura for reviewing the final version of

olive trees do not form ectomycorrhizal associations. the manuscript.

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

8 L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx

Appendix A.

Vascular plant taxa recorded in the study area.

Taxon English common names Family Potential uses/impacts

Allium roseum L. var. roseum Rosy garlic Alliaceae Ornamental

Pistacia lentiscus L. Mastic, lentisco Anacardiaceae Woodwork

Daucus carota L. subsp. carota L. Wild carrot Apiaceae Edible (root)

Eryngium campestre L. Sea holly, field eryngo Apiaceae

Foeniculum vulgare Mill. Fennel Apiaceae Edible, aromatic

Smyrnium olusatrum L. Alexanders, horse parsley Apiaceae Edible (leaves)

Thapsia villosa L. Apiaceae Ornamental

Torilis arvensis (Huds.) Link Hedge parsley, field hedge parsley, Apiaceae

spreading hedge parsley

Vinca difformis Pourret Periwinkle Apocynaceae Medicinal, poisonous (monoterpene indole alcaloids)

Arisarum simorrhinum Durieu Friar’s cowl Araceae

Arisarum vulgare Targ.-Tozz. Friar’s cowl Araceae

Arum italicum Mill. Lords-and-ladies, cuckoo-pint Araceae Poisonous (aroin, calcium oxalate, cyanogenic

glucosides, saponins), irritant for the mucous

membranes

Hedera maderensis K. Koch ex A. Ivy, common-ivy Araliaceae Ornamental, poisonous (triterpene saponins,

Rutherf. subsp. iberica Mc Allister sesquiterpenes, falcarinol). Causes contact dermatitis

Aristolochia sempervirens L. Birthwort, Dutchman’s pipe Aristolochiaceae Medicinal, poisonous (aristolochic acid and related

alkaloids)

Asparagus aphyllus L. Prickly asparagus Asparagaceae

Asparagus officinalis L. Asparagus Asparagaceae Edible (young shoots)

Drimia maritima (L.) Stearn Sea onion, squill Asparagaceae Medicinal, poisonous (bufadienolides), raticide

Ruscus aculeatus L. Butcher’s broom, box holly, jew’s Asparagaceae Ornamental, poisonous (steroidal saponins)

myrtle

Asplenium adiantum-nigrum L. Black sleepenwort Aspleniaceae Ornamental

Achillea ageratum L. Sweet nancy Asteraceae Medicinal. Causes contact allergies

Andryala integrifolia L. Rabbit’s bread Asteraceae

Anthemis arvensis L. Corn chamomile, mayweed, scentless Asteraceae Weed

chamomile

Arctotheca calendula (L.) Levyns. Cape weed Asteraceae Ornamental, invasive

Bellis perennis L. Daisy Asteraceae Ornamental

Carduncellus caeruleus (L.) C. Presl Asteraceae

Carduus tenuiflorus Curtis Thistle Asteraceae

Carlina racemosa L. Carlina thistle Asteraceae

Chamaemelum nobile (L.) All. Chamomile Asteraceae

Cichorium intybus L. Chicory, succory, witloof Asteraceae Medicinal, edible

Coleostephus myconis (L.) Reichenb. fil. Chrysanthemum goblin, Asteraceae Weed

chrysanthemum gold plate, yellow

daisy

Conyza canadensis (L.) Cronq. Horseweed, mule-tail Asteraceae

Cotula australis (Spreng.) Hook.f. Brass buttons Asteraceae

Crepis vesicaria L. Beaked hawksbeard Asteraceae

Cynara humilis L. Artichoke, cardoon Asteraceae

Dittrichia viscosa (L.) W. Greuter False yellowhead, strong-smelling Asteraceae

Inula

Erigeron karvinskianus DC. Daisy, daisy fleabane, Mexican daisy Asteraceae Ornamental, invasive

fleabane

Galactites tomentosa Moench Asteraceae

Hypochaeris radicata L. Spotted cat’s ear, hairy’s cat’s ear, Asteraceae

frogbit

Lactuca serriola L. Prickly lettuce Asteraceae Poisonous (sesquiterpene lactones)

Leontodon taraxacoides (Vill.) Mérat Lesser hawkbit Asteraceae

Leontodon taraxacoides subsp. Asteraceae

longirostris Finch & P.D. Sell

Pallenis spinosa (L.) Cass. Spiny starwort Asteraceae

Phagnalon saxatile (L.) Cass. Asteraceae

Picris echioides L. Bristly ox-tongue Asteraceae

Pseudognaphalium luteo-album (L.) Jersey cudweed, kettlehole cudweed Asteraceae

Hilliard & B.L. Burtt

Pulicaria odora (L.) Reichenb. Fleabane Asteraceae

Scolymus hispanicus L. Golden thistle, Spanish oyster thistle Asteraceae

Senecio jacobaea L. Common ragwort Asteraceae Medicinal, poisonous (pyrrolizidine alkaloids)

Senecio sylvaticus L. Woodland ragwort, heath groundsel Asteraceae Medicinal, poisonous (pyrrolizidine alkaloids)

Senecio vulgaris L. Common groundsel, old man in the Asteraceae Medicinal, poisonous (pyrrolizidine alkaloids)

Spring

Sonchus asper (L.) Hill Milk thistle Asteraceae

Sonchus oleraceus L. Milk thistle Asteraceae Edible, foraging

Tolpis barbata (L.) Gaertner European umbrella milkwort, yellow Asteraceae

hawkweed

Cynoglossum creticum Miller Hond’s tong

Echium plantagineum L. Paterson’s curse, salvation Jane, lady Boraginaceae Melliferous, poisonous (pyrrolizidine alkaloids)

campbell weed

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx 9

Taxon English common names Family Potential uses/impacts

Echium tuberculatum Hoffmanns. & Boraginaceae Melliferous, poisonous (pyrrolizidine alkaloids)

Link

Myosotis ramosissima Rochel Common forget-me-not, scorpion grass Boraginaceae

Cardamine hirsuta L. Bittercress Brassicaceae

Hirschfeldia incana (L.) Lagr.-Foss. Buchanweed, mediterranean mustard, Brassicaceae Weed

shortpod mustard

Raphanus raphanistrum L. Wild radish, mediterranean radish Brassicaceae Edible

Rapistrum rugosum (L.) All. Bastard cabbage, turnip weed, wild Brassicaceae Weed

turnip

Sinapis alba L. White mustard, salad mustard Brassicaceae

Campanula rapunculus L. Rampion Campanulaceae Ornamental

Jasione montana L. Sheep’s bit Campanulaceae Ornamental

Lonicera periclymenum L. Honeysuckle, woodbine Caprifoliaceae Ornamental, poisonous (berries – cyanogenic

glucosides, saponins)

Viburnum tinus L. Laurustinus Caprifoliaceae Ornamental

Cerastium glomeratum Thuill. Mouse-ear chickweed Caryophyllaceae

Cerastium pumilum Curtis Dwarf mouse-ear, European chickweed Caryophyllaceae

Polycarpon tetraphyllum (L.) L. Four-leaved allseed, fourleaf manyseed Caryophyllaceae

Silene gallica L. Campion, catchfly Caryophyllaceae

Silene vulgaris (Moench) Garcke Campion, catchfly Caryophyllaceae

Stellaria media (L.) Vill. Chickweed Caryophyllaceae Edible

Beta vulgaris L. Beetroot Chenopodiaceae Edible

Cistus crispus L. Rock rose Cistaceae Ornamental, melliferous

Cistus monspeliensis L. Rock rose Cistaceae Ornamental, melliferous

Cistus salviifolius L. Sageleaf rockrose Cistaceae Ornamental, melliferous

Xolantha guttata (L.) Raf. European frostweed, tuberaria, spotted Cistaceae Ornamental, melliferous

rockrose

Hypericum humifusum L. Trailing St John’s Wort Clusiaceae Ornamental, poisonous (dianthrones, hyperforin),

skin-irritant

Hypericum perforatum L. St Jonh’s wort Clusiaceae Ornamental, poisonous (dianthrones, hyperforin),

skin-irritant

Tradescantia fluminensis Vell. Spider-lily, spider-wort Commelinaceae Invasive

Convolvulus althaeoides L. Hollyhock bindweed, mallow Convolvulaceae Poisonous

bindweed

Convolvulus arvensis L. Field bindweed Convolvulaceae Poisonous

Umbilicus rupestris (Salisb.) Dandy Navel wort, penny wort Crassulaceae

Cupressus lusitanica Mill. Portuguese cypress, Mexican cypress, Cupressaceae Ornamental, allergenic, poisonous (monoterpenes,

cedar of Goa sesquiterpenes)

Carex peregrina Link Sedge Cyperaceae

Carex depressa Link Sedge Cyperaceae

Carex distachya Desf. Sedge Cyperaceae

Carex divulsa Stokes Sedge, berkeley sedge, European grey Cyperaceae

sedge

Carex flacca Schreb. Sedge, blue sedge Cyperaceae

Cyperus longus L. Common galingale, sweet galingale Cyperaceae Weed

Tamus communis L. Black briony, murraim berries Dioscoreaceae Poisonous (steroid sponins, calcium oxalate raphides).

Causes dermatitis

Dipsacus fullonum L. Common teasel, Wild teasel, fuller’s Dipsacaceae

teasel, venuscup teasel

Scabiosa atropurpurea L. Mournfull widow, sweet scabious Dipsacaceae Ornamental

Arbutus unedo L. Strawberry tree Ericaceae Edible (berries)

Calluna vulgaris (L.) Hull Scotts heather Ericaceae Ornamental, melliferous

Erica arborea L. Tree heath Ericaceae Ornamental, melliferous

Erica umbellata Loefl. ex L. Dwarf spanish heath Ericaceae Ornamental, melliferous

Euphorbia characias L. Spurge, mediterranean spurge Euphorbiaceae Ornamental, poisonous

Acacia dealbata Link Silver wattle, mimosa Fabaceae Melliferous, invasive, allergenic (pollen)

Acacia longifolia (Andrews) Willd. Sydney golden wattle, sallow wattle Fabaceae Melliferous, invasive, allergenic (pollen)

Acacia melanoxylon R. Br. Blackwood Fabaceae Melliferous, invasive, allergenic (pollen)

Anthyllis vulneraria L. subsp. maura Kidney vetch Fabaceae

(Beck) Maire

Cercis siliquastrum L. Judas tree Fabaceae Ornamental

Coronilla scorpioides (L.) W.D.J. Koch Crown vetch Fabaceae Ornamental, poisonous (glycosides with cardiac

activity,)

Cytisus striatus (Hill) Rothm. Broom Fabaceae Ornamental, medicinal, melliferous, poisonous

(quinolizidine alkaloids)

Genista triacanthos Brot. Broom, woodwaxen Fabaceae Melliferous, poisonous (quinolizidine alkaloids)

Lathyrus annuus L. Vetchling Fabaceae Poisonous (non-protein amino acids)

Lathyrus aphaca L. Yellow vetchling Fabaceae Poisonous (non-protein amino acids)

Lathyrus hirsutus L. Singletary pea, caley pea, rough pea Fabaceae Poisonous (non-protein amino acids)

Lathyrus sphaericus Retz. Grass pea Fabaceae Poisonous (non-protein amino acids)

Lathyrus sylvestris L. Flat pea, narrow-leaved everlasting pea Fabaceae Poisonous (non-protein amino acids)

Lathyrus tingitanus L. Tangier pea Fabaceae Ornamental, poisonous (non-protein amino acids)

Lotus angustissimus L. Slender bird’s foot trefoil Fabaceae Poisonous (cyanogenic glycosides)

Medicago doliata Carmign. Medic, medick Fabaceae

Medicago lupulina L. Black medick, hop clover, nonsuch Fabaceae

Medicago minima (L.) L. Medic, medick Fabaceae

Medicago orbicularis (L.) Bartal. Medic, medick Fabaceae

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

10 L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx

Taxon English common names Family Potential uses/impacts

Melilotus indicus (L.) All. Indian sweet clover, sour clover, Fabaceae Poisonous (coumarins)

small-flowered melilot

Ononis reclinata L. Rest-harrow Fabaceae

Ononis viscosa L. Rest-harrow Fabaceae

Ornithopus compressus L. Yellow serradella Fabaceae

Scorpiurus muricatus L. Prickly scorpion’s-tail, many-flowered Fabaceae

Scorpiurus

Scorpiurus vermiculatus L. Single-flowered Scorpiurus Fabaceae

Spartium junceum L. Spanish broom, weaver’s broom Fabaceae Ornamental, poisonous (quinolizidine alkaloids)

Trifolium angustifolium L. Narrow-leaved clover, narrowleaf Fabaceae Foraging, melliferous

crimson clover

Trifolium arvense L. Haresfoot clover, rabbitfoot clover, Fabaceae Foraging, melliferous

stone clover

Trifolium campestre Schreb. Low hop clover, field clover, large hop Fabaceae Foraging, melliferous

clover

Trifolium dubium Sibth. Suckling clover, lesser yellow trefoil Fabaceae Foraging, valuable as nitrogen-fixing, melliferous

Trifolium repens L. White clover, Dutch clover, shamrock Fabaceae Foraging, poisonous (benzofuranocoumarins,

isoflavones)

Trifolium tomentosum L. Wooly clover Fabaceae Foraging, melliferous

Ulex europaeus L. subsp. latebracteatus Gorse, common gorse Fabaceae Melliferous, poisonous (quinolizidine alkaloids)

(Mariz) Rothm.

Ulex minor Roth Dwarf furze, dwarf gorse Fabaceae Melliferous, poisonous (quinolizidine alkaloids)

Vicia angustifolia L. Vetch, tare Fabaceae

Vicia benghalensis L. Vetch, tare Fabaceae

Vicia disperma DC. Vetch, Tare Fabaceae

Vicia sativa L. Spring vetch, tare Fabaceae Foraging, poisonous (glycosides of pyrimidines,

non-protein amino acids)

Castanea sativa Mill. Sweet chestnut, Spanish chestnut Fagaceae Edible (nuts), medicinal, ornamental, woodwork

Quercus coccifera L. Kermes oak, grain oak Fagaceae Poisonous (tanins and other polyphenols)

Quercus faginea Lam. subsp. broteroi Portuguese oak Fagaceae Woodwork, tanning, allergenic, poisonous (tanins and

(Cout.) A. Camus other polyphenols)

Quercus pyrenaica Willd. Pyrenean oak, Spanish oak Fagaceae Woodwork, tanning, allergenic (pollen), poisonous

(tanins and other polyphenols)

Quercus robur L. English oak, common oak, pedunculate Fagaceae Medicinal, woodwork, allergenic (pollen), tanning,

oak poisonous (tanins and other polyphenols)

Quercus suber L. Cork oak Fagaceae Cork production, edible (acorns), allergenic (pollen),

tanning, poisonous (tanins and other polyphenols)

Blackstonia perfoliata (L.) Hudson Yellow wort Gentianaceae

Centaurium erythraea Rafn Common centaury, European centaury Gentianaceae Poisonous (secoiridoids)

Centaurium maritimum (L.) Fritsch Yellow centaury Gentianaceae Rare, poisonous (secoiridoids)

Centaurium tenuiflorum (Hoffmanns. & Yellow star thistle, Geeldissel, golden Gentianaceae Poisonous (secoiridoids)

Link) Fritsch star thistle

Erodium cicutarium (L.) L‘Herit. Storksbill, heron’s bill Geraniaceae

Geranium columbinum L. Long stalked cranes bill Geraniaceae

Geranium dissectum L. Cranesbill, wild geranium, cut leaved Geraniaceae

geranium

Geranium lucidum L. Shining crane’s bill, shining geranium Geraniaceae

Geranium purpureum Vill. Herb Robert, robert geranium Geraniaceae

Geranium rotundifolium L. Round-leaved geranium, round-leaved Geraniaceae

crane’s bill

Pteridium aquilinum (L.) Kuhn Bracken, brake Hypolepidaceae Poisonous (ptaquiloside, thiaminase)

Gladiolus illyricus W.D.J. Kock Wild gladiolus Iridaceae Ornamental

Iris foetidissima L. Roast beef plant, stinking gladwyn Iridaceae Ornamental, poisonous (safranal)

Juncus bufonius L. Toad rush Juncaceae

Luzula campestris (L.) DC. Field wood-rush Juncaceae

Calamintha sylvatica Bromf. Common calamint Lamiaceae Aromatic, spice

Clinopodium vulgare L. Wild basil, cushion calamint Lamiaceae Ornamental

Lavandula pedunculata (Miller) Cav. French lavender Lamiaceae Ornamental, aromatic, melliferous

Melissa officinalis L. Bee balm, lemon balm Lamiaceae Medicinal, aromatic

Mentha pulegium L. Pennyroyal Lamiaceae Medicinal, aromatic

Mentha rotundifolia (L.) Huds. False apple mint, round leaved mint Lamiaceae Aromatic

Micromeria graeca (L.) Reichenb. Lamiaceae Aromatic, spice

Origanum virens Hoffmanns. & Link Lamiaceae Spice

Origanum vulgare L. Wild marjoram, oregano Lamiaceae Aromatic, spice

Prunella vulgaris L. Common selfheal Lamiaceae

Salvia verbenaca L. Vervain, wild clary Lamiaceae Ornamental, melliferous

Stachys arvensis (L.) L. Betony, hedge nettle Lamiaceae Melliferous

Stachys germanica L. Downy woundwort Lamiaceae Ornamental, melliferous

Thymus vulgaris L. Common thyme, garden thyme Lamiaceae Aromatic, spice, melliferous

Laurus nobilis L. True laurel, bay laurel, sweet bay Lauraceae Spice

Linum bienne Miller Pale flax Linaceae Poisonous (cyanogenic glucisides, podophyllotoxin,

saponins)

Linum setaceum Brot. Flax Linaceae Poisonous (cyanogenic glucisides, podophyllotoxin,

saponins)

Linum strictum L. Flax Linaceae Poisonous (cyanogenic glucisides, podophyllotoxin,

saponins)

Lavatera arborea L. Tree mallow Malvaceae Ornamental

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx 11

Taxon English common names Family Potential uses/impacts

Lavatera trimestris L. Annual mallow, English rose mallow, Malvaceae Ornamental

royal mallow

Malva sylvestris L. Tall mallow, high mallow, cheeses Malvaceae Ornamental

Eucalyptus globulus Labill. Tasmanian blue gum, blue gum Myrtaceae Medicinal, pulp production

Myrtus communis L. Myrtle Myrtaceae Ornamental

Fraxinus angustifolia Vahl Ash, narrow leaved ash Oleaceae Ornamental, medicinal

Fraxinus excelsior L. Common European ash Oleaceae Ornamental

Olea europaea L. Common olive, edible olive Oleaceae Edible (olives, olive oil), allergenic (pollen)

Olea europea L. var. sylvestris (Miller) Common olive, edible olive Oleaceae Allergenic (pollen)

Lehr.

Anacamptis pyramidalis (L.) Rich. Pyramid orchid Orchidaceae Ornamental

Serapias lingua L. Tongue orchid Orchidaceae

Oxalis corniculata L. Procumbent yellow sorrel, creeping Oxalidaceae Poisonous

oxalis

Oxalis pes-caprae L. Bermuda buttercup, English-weed Oxalidaceae Invasive, poisonous (calcium oxalate)

Fumaria capreolata L. Climbing fumitory, fumitory, white Papaveraceae

ramping fumitory

Fumaria muralis Sond. ex W.D.J. Koch Fumaria, wall fumitory Papaveraceae

Papaver dubium L. Poppy Papaveraceae

Papaver rhoeas L. Corn poppy, field poppy, flanders Papaveraceae

poppy

Phytolacca americana L. Pokeweed, skoke, garget Phytolaccaceae Poisonous (lectins, triterpene saponins)

Pinus pinaster Aiton Maritime pine Pinaceae Woodwork, edible (seeds)

Pinus pinea L. Stone pine Pinaceae Woodwork, edible (seeds)

Pittosporum undulatum Vent. Victorian box, cheesewood Pittosporaceae Ornamental, invasive

Plantago afra L. Flea wort Plantaginaceae Allergenic (pollen)

Plantago lanceolata L. English plantain, ribwort, buckhorn Plantaginaceae Allergenic (pollen)

Plantago serraria L. Plantain Plantaginaceae Allergenic (pollen)

Agrostis curtisii Kerguélen Bristle bent Poaceae Allergenic (pollen)

Aira praecox L. Early hair grass Poaceae

Arrhenatherum elatius (L.) P. Beauv. False oat-grass, tall oat-grass, tall Poaceae

meadow oat

Arundo donax L. Giant reed Poaceae Ornamental

Avena alba L. Oat Poaceae

Brachypodium distachyon (L.) Beauv. False brome, purple false brome, stiff Poaceae

brome

Brachypodium phoenicoides (L.) Roemer Thinleaf false brome Poaceae

& Schultes

Briza maxima L. Great quaking grass Poaceae Ornamental

Briza media L. Common quaking grass, didder Poaceae Ornamental

Briza minor L. Lesser quaking grass Poaceae Ornamental

Bromus diandrus Roth Brome, chess Poaceae

Bromus hordeaceus L. Brome, chess Poaceae

Bromus rigidus Roth Brome, chess Poaceae

Cynodon dactylon (L.) Pers. Bermuda grass, bahama grass, kweek Poaceae

Cynosurus echinatus L. Rough dog’s tail grass Poaceae

Dactylis glomerata L. Cocksfoot, orchard grass Poaceae Allergenic (pollen)

Dactylis glomerata L. subsp. hispanica Cocksfoot, orchard grass Poaceae Allergenic (pollen)

(Roth) Nyman

Gastridium ventricosum (Gouan) Nit grass Poaceae

Schintz & Tell.

Hordeum murinum L. Barley Poaceae

Hordeum secalinum Schreber Barley Poaceae

Hyparrhenia hirta (L.) Stapf Thatching grass, coolatai grass Poaceae

Lolium rigidum Gaudin Ryegrass, darnel Poaceae Allergenic (pollen)

Melica uniflora Retz. Wood melic Poaceae

Periballia involucrata (Cav.) Janka Poaceae

Phalaris aquatica L. Toowomba canary grass, harding grass Poaceae

Phalaris arundinacea L. Reed canary grass, gardener’s garter Poaceae

Phleum pratense L. Timothy grass Poaceae Allergenic (pollen)

Piptatherum miliaceum (L.) Cosson Smilo grass Poaceae

Poa annua L. Annual bluegrass, annual meadow Poaceae Allergenic (pollen)

grass

Poa pratensis L. Kentucky blue grass, June grass Poaceae Allergenic (pollen)

Poa trivialis L. Meadowgrass, blue grass Poaceae Allergenic (pollen)

Polypogon viridis (Gouan) Breistr. Beardless rabbitsfoot grass Poaceae

Pseudarrhenatherum longifolium Poaceae

(Thore) Rouy

Vulpia muralis (Kunth) Nees Poaceae

Polygonum aviculare L. Knotweed, smartweed Polygonaceae Allergenic (pollen)

Rumex acetosa L. Garden sorrel, sour dock Polygonaceae Poisonous (anthraquinones, tanins, oxalates),

allergenic (pollen)

Rumex bucephalophorus L. Dock, sorrel Polygonaceae Poisonous (anthraquinones, tanins, oxalates),

allergenic (pollen)

Rumex conglomeratus Murray Dock, sorrel Polygonaceae Poisonous (anthraquinones, tanins, oxalates),

allergenic (pollen)

Rumex crispus L. Curled dock Polygonaceae Poisonous (anthraquinones, tanins, oxalates),

allergenic (pollen)

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

12 L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx

Taxon English common names Family Potential uses/impacts

Polypodium vulgare L. Common polypody, adder’s fern, wall Polypodiaceae Ornamental

fern

Anagallis arvensis L. Scarlet pimpernel, shepperd’s clock Primulaceae Ornamental, poisonous (cucurbitacins, oxalates,

triterpene saponins)

Anagallis monelli L. Blue pimpernel Primulaceae Ornamental

Clematis campaniflora Brot. Virgin’s bower, leather flower Ranunculaceae Ornamental

Ranunculus bulbosus L. subsp. aleae Buttercup, crowfoot Ranunculaceae Poisonous (protoanemonin)

(Willk.) Rouy & Foucaud

Ranunculus muricatus L. Buttercup, crowfoot Ranunculaceae Poisonous (protoanemonin)

Ranunculus parviflorus L. Buttercup, crowfoot Ranunculaceae Poisonous (protoanemonin)

Reseda luteola L. Mignonette Resedaceae

Reseda media Lag. Mignonette Resedaceae

Frangula alnus Mill. Alder buckthorn Rhamnaceae Medicinal, poisonous (anthracene glycosides,

anthranol derivatives, dianthrones)

Rhamnus alaternus L. Buckthorn Rhamnaceae Medicinal, woodwork, tanning

Agrimonia eupatoria L. Agrimony Rosaceae Medicinal

Aphanes arvensis L. Parsley piert, parsley breakstone Rosaceae

Crataegus monogyna Jacq. English hawthorn Rosaceae Ornamental, medicinal

Cydonia oblonga Mill. Quince, Portuguese quince Rosaceae Edible, medicinal

Eriobotrya japonica (Thunb.) Lindl. Loquat, Japanese plum Rosaceae Edible (berries)

Geum urbanum L. Avens, chocolate root, benedicte Rosaceae

Potentilla reptans L. Cinquefoil, five fingers Rosaceae

Prunus avium L. Bird cherry, Sweet cherry, gean Rosaceae Edible (drupes), ornamental

Prunus cerasifera cv. atropurpurea H. Cherry plum Rosaceae Edible (drupes), ornamental

Jaeger

Prunus cerasifera Ehrh. Cherry plum, myrobalan Rosaceae Edible (drupes), ornamental

Prunus spinosa L. Sloe, blackthorne Rosaceae Edible (drupes)

Pyrus communis L. Common pear Rosaceae Edible (pomes)

Rosa canina L. Dog rose, dog brier Rosaceae

Rubus ulmifolius Schott. Brumble Rosaceae Edible (aggregate fruit)

Sanguisorba minor Scop. Burnet, garden burnet Rosaceae Medicinal

Galium murale (L.) All. Tiny bedstraw, small goosegrass, Rubiaceae

yellow wall bedstraw

Rubia peregrina L. Wild madder, levant madder Rubiaceae

Sherardia arvensis L. Field madder, spurwort Rubiaceae

Citrus reticulata Blanco Mandarine orange, tangerine, Rutaceae Edible (hesperidium)

lementine, satsuma

Citrus sinensis (L.) Osbeck Orange, sweet orange Rutaceae Edible (hesperidium)

Osyris alba L. Osyris Santalaceae Tanning

Digitalis purpurea L. Purple foxglove Scrophulariaceae Medicinal, poisonous (cardenolides)

Kickxia spuria (L.) Dumort. Roundleaf cancerwort, roundleaf Scrophulariaceae

fluellen

Misopates orontium (L.) Raf. Weasel’s Snout Scrophulariaceae

Scrophularia grandiflora DC. Figwort Scrophulariaceae Poisonous (active principle unknown)

Verbascum sinuatum L. Wavyleaf mullein, scalop-leaved Scrophulariaceae

mullein

Verbascum virgatum Stokes Twiggy mullein Scrophulariaceae Ornamental

Veronica arvensis L. Speedwell, bird’s eye Scrophulariaceae

Ailanthus altissima (Miller) Swingle Tree of heaven Simaroubaceae Invasive

Smilax aspera L. Common smilax, prickly ivy, rough Smilacaceae Medicinal

smilax, salsaparilla

Solanum sublobatum Willd. ex Roem. & Black nightshade, poisonberry Solanaceae Poisonous (steroidal glyco-alkaloids)

Schult.

Daphne gnidium L. Flax-leaved daphne, spurge-flax Thymelaeaceae Poisonous (phorbol esters, coumarin glycosides), skin

irritant

Ulmus minor Mill. Eurpean fiel elm, smooth-leaved elm Ulmaceae Woodwork, medicinal, allergenic (pollen)

Parietaria judaica L. Pellitory of the wall Urticaceae Allergenic

Urtica dioica L. Stinging nettle Urticaceae Edible, medicinal, skin irritant

Centranthus calcitrapae (L.) Dufr. Annual valerian, pink valerian, Urticaceae

cut-leaved valerian

Verbena officinalis L. Common verbena Valerianaceae Medicinal

Vitis vinifera L. Common grape vine Verbenaceae Edible (grapes, wine)

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx 13

Appendix B.

Macromycete taxa recorded in the study area.

Taxon Family Host range Edibility

Agaricus arvensis Schaeff. Agaricaceae Saprobe Edible

Agaricus campestris L. Agaricaceae Saprobe Edible

Agaricus xanthodermus Genev. Agaricaceae Saprobe Not edible, poisonous

Bovista plumbea Pers. Agaricaceae Saprobe Edible at young stage

Coprinus comatus (O.F. Müll.) Pers. Agaricaceae Saprobe Edible

Coprinus plicatilis (Curtis) Fr. Agaricaceae Saprobe Not edible

Cyathus striatus (Huds.) Willg. Agaricaceae Saprobe Not edible

Lepiota clypeolaria (Bull.) P. Kumm. Agaricaceae Saprobe Not edible, poisonous

Lycoperdon perlatum Pers. Agaricaceae Saprobe Edible at young stage

Macrolepiota procera (Scop.) Singer Agaricaceae Saprobe Edible, excellent

Rickenella fibula (Bull.) Raithelh Agaricomycetes Saprobe Not edible

Amanita citrina (Schaeff.) Pers. Amanitaceae ECMF/Broad HR Not edible

Amanita muscaria (L.) Lam. Amanitaceae ECMF/Broad HR Not edible, poisonous

Amanita pantherina (DC.) Krombh. Amanitaceae ECMF/Broad HR Not edible, poisonous

Amanita phalloides (Vaill. ex Fr.) Link Amanitaceae ECMF/Broad HR Not edible, mortal

Amanita rubescens Pers. Amanitaceae ECMF/Broad HR Edible

Amanita vaginata (Bull.) Lam. Amanitaceae ECMF/Broad HR Edible

Boletus chrysenteron Bull. Boletaceae ECMF/Broad HR Edible

Boletus subtomentosus L. Boletaceae ECMF/Broad HR Edible

Cantharellus lutescens Fr. Cantharellaceae ECMF/Broad HR Edible, excellent

Cortinarius trivialis J.E. Lange Cortinariaceae ECMF/Angiosperms Not edible

Calocera cornea (Batsch) Fr. Dacrymycetaceae Saprobe Not edible

Astraeus hygrometricus (Pers.) Morgan Diplocystidiaceae ECMF/Broad HR Not edible

Bisporella citrina (Batsch) Korf & S.E. Carp. Diplocystidiaceae Saprobe Not edible

Ramaria formosa (Pers.) Quél. Gomphaceae Saprobe Not edible, purgative

Ramaria stricta (Pers.) Quél. Gomphaceae ECMF/Broad HR Edible, low value

Chroogomphus rutilus (Schaeff.) O. K. Mill. Gomphidiaceae ECMF/Broad HR Edible

Hydnum repandum L. Hydnaceae ECMF/Broad HR Edible

Laccaria laccata (Scop.) Cooke Hydnangiaceae ECMF/Broad HR Edible

Hygrocybe conica (Scop.) P. Kum. Hygrophoraceae Saprobe Not edible

Inonotus radiatus (Sowerby) P. Karst. Hymenochaetaceae Saprobe Not edible

Crepidotus variabilis (Pers.) P. Kumm. Inocybaceae Saprobe

Inocybe sp1 Inocybaceae ECMF/Broad HR

Marasmius oreades (Bolton) Fr. Marasmiaceae Saprobe Edible

Micromphale foetidum (Snowerby) Singer Marasmiaceae Saprobe Not edible

Omphalotus illudens (Schwein.) Bresinsky & Besl Marasmiaceae Saprobe Not edible, poisonous

Rhodocollybia butyracea (Bull.) Lennox Marasmiaceae Saprobe Edible, low value

Abortiporus biennis (Bull.) Singer Meruliaceae Saprobe

Mycena epipterygia (Pers.) P. Kumm. Mycenaceae Saprobe Not edible

Mycena galopus (Pers.) P. Kumm. Mycenaceae Saprobe

Mycena pura (Pers.) P. Kumm. Mycenaceae Saprobe Not recommended, hallucinogenic

properties

Mycena rorida (Fr.) Quél. Mycenaceae Saprobe Not edible

Mycena seynesii Quél. Mycenaceae Saprobe

Nectria cinnabarina (Tode) Fr. Nectriaceae Saprobe Not edible

Pulcherricium caeruleum (Lam.) Parmasto Phanerochaetaceae Saprobe Not edible

Armillaria mellea (Vahl) P. Kumm. Physalacriaceae Saprobe Edible at young stage

Fomes fomentarius (L.) J.J. Kickx Polyporaceae Saprobe Not edible, medicinal

Trametes hirsuta (Wulfen) Pilát Polyporaceae Saprobe Not edible

Trametes versicolor (L.) Lloyd Polyporaceae Saprobe Not edible, medicinal

Trichaptum abietinum (Dicks.) Ryvarden Polyporaceae Saprobe Not edible

Coprinellus micaceus (Bull.) Vilgalys, Hopple & Jacq. Johnson Psathyrellaceae Saprobe

Coprinopsis atramentaria (Bull.) Redhead, Vilgalys & Moncalvo Psathyrellaceae Saprobe Not edible, poisonous when consumed

with alcohol

Coprinopsis picacea (Bull.) Redhead, Vilgalys & Moncalvo Psathyrellaceae Saprobe

Psathyrella velutina (Pers.) Singer Psathyrellaceae Saprobe Not edible

Aleuria aurantia (Pers.) Fuckel Pyronemataceae Saprobe Edible

Humaria hemisphaerica (F.H. Wigg.) Fuckel Pyronemataceae Saprobe

Otidea cochleata (Huds.) Fuckel Pyronemataceae Saprobe

Scutellinia scutellata (L.) Lambotte Pyronemataceae Saprobe

Lactarius chrysorrheus Fr. Russulaceae ECMF/Quercus sp Edible

Lactarius deliciosus (L.) Gray Russulaceae ECMF/Broad HR Edible, excellent

Russula amoenolens Romagn. Russulaceae ECMF/Angiosperms

Russula cyanoxantha (Schaeff.) Fr. Russulaceae ECMF/Broad HR Edible

Russula delica Fr. Russulaceae ECMF/Broad HR Edible, low value

Russula nigricans (Bull.) Fr. Russulaceae ECMF/Broad HR Edible at young stage

Russula sp1 Russulaceae ECMF

Russula sp2 Russulaceae ECMF

Russula sp3 Russulaceae ECMF

Russula virescens (Schaeff.) Fr. Russulaceae ECMF/Broad HR Edible

Russula xerampelina (Schaeff.) Fr. Russulaceae ECMF/Broad HR

Sarcoscypha coccinea (Jacq.) Sacc. Sarcoscyphaceae Saprobe

Schizophyllum commune Fr. Schizophyllaceae Saprobe Not edible, medicinal

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

14 L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx

Taxon Family Host range Edibility

Pisolithus tinctorius (Mont.) E. Fisch. Sclerodermataceae ECMF/Broad HR Edible at young stage

Scleroderma areolatum Ehrenb. Sclerodermataceae ECMF/Broad HR

Scleroderma bovista Fr. Sclerodermataceae ECMF/Broad HR

Scleroderma citrinum Pers. Sclerodermataceae ECMF/Broad HR

Scleroderma polyrhizum (J.F. Gmel.) Pers. Sclerodermataceae ECMF/Thermophilic

Scleroderma verrucosum (Bull.) Pers. Sclerodermataceae ECMF/Broad HR

Stereum hirsutum (Wild.) Pers. Stereaceae Saprobe Not edible

Stereum reflexulum D.A. Reid Stereaceae Saprobe Not edible

Gymnopilus junonius (Fr.) P.D. Orton Strophariaceae Saprobe Not edible

Gymnopilus penetrans (Fr.) Murrill Strophariaceae Saprobe Not edible

Hypholoma fasciculare (Huds.) P. Kumm. Strophariaceae Saprobe Not edible, poisonous

Stropharia aurantiaca (Cooke) M. Imai Strophariaceae Saprobe Not edible

Tremella foliacea Pers. Tremellaceae Saprobe

Tremella mesenterica Retz. Tremellaceae Saprobe

Clitocybe costata Kühner & Romagn. Tricholomataceae Saprobe Edible

Clitocybe gibba (Pers.) P. Kumm. Tricholomataceae Saprobe Edible

Clitocybe odora (Bull.) P. Kumm. Tricholomataceae Saprobe Edible

Lepista nuda (Bull.) Cooke Tricholomataceae Saprobe Edible

Lepista sordida (Fr.) Singer Tricholomataceae Saprobe

Melanoleuca melaleuca (Pers.) Murrill Tricholomataceae Saprobe Edible

Tricholoma fracticum (Britzelm.) Kreisel Tricholomataceae ECMF/Broad HR Edible only after cooked, low value

Tricholoma sulphureum (Bull.) P. Kumm. Tricholomataceae ECMF/Broad HR Not edible, poisonous

Tricholoma portentosum (Fr.) Quél. Tricholomataceae ECMF/Broad HR Edible

Lycogala epidendrum (J.C. Buxb. ex L.) Fr. Tubiferaceae Saprobe Not edible

Xylaria hypoxylon (L.) Grev. Xylariaceae Saprobe Not edible

Colpaert, J. V., Wevers, J. H. L., Krznaric, E., & Adriaensen, K. (2011). How metal-

References

tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal

pollution. Annals of Forest Science, 68(1), 17–24.

Ahonen-Jonnarth, U., Göransson, A., & Finlay, R. D. (2003). Growth and nutrient Compant, S., Duffy, B., Nowak, J., Clément, C., & Barka, E. A. (2005). Use of plant

uptake of ectomycorrhizal Pinus sylvestris seedlings in a natural substrate treated growth-promoting bacteria for biocontrol of plant diseases: Principles, mecha-

with elevated Al concentrations. Tree Physiology, 23(3), 157–167. nisms of action, and future prospects. Applied and Environmental Microbiology,

Allen, H. D., Randall, R. E., Amable, G. S., & Devereux, B. J. (2006). The impact of 71(9), 4951–4959.

changing olive cultivation practices on the ground flora of olive groves in the Courtecuisse, R., & Duhem, B. (2005). (Guide to fungi of the Iberian Peninsula, Europe

Messara and Psiloritis regions, Crete, Greece. Land Degradation and Development, and North Africa) Guía de los Hongos de la Península Ibérica, Europa y Norte de

17(3), 249–273. África. Barcelona: Omega. [in Spanish].

APA – Agência Portuguesa do Ambiente. (1971). (Soil map – Atlas of the digital Crespí, A. M. L., Pereira Coutinho, A., Aguiar, C., Neto, C., Pinto-Gomes, C., Espírito

environment) Carta dos Solos – Atlas do Ambiente Digital. Ministério do Ambiente, Santo, D., et al. (2011). In M. M. Sequeira, D. Espírito-Santo, C. Aguiar, J. Capelo,

do Ordenamento do Território e do Desenvolvimento Regional. [in Portuguese]. & J. Honrado (Eds.), Checklist da Flora de Portugal (Continental, Ac¸ ores e Madeira)

http://www.iambiente.pt/atlas/est/index.jsp?zona=continente&grupo=&tema= (Checklist of the flora of Portugal (continental, azores and madeira)). Lisboa:

ctipossolo [accessed February 2011] Associac¸ ão Lusitana de Fitossociologia (Alfa) [in Portuguese].

Azul, A. M. (2011). Diálogos e modos de actuac¸ ão colectiva com vista à sustentabil- Cunha, A. P., Silva, A. P., & Roque, O. R. (2003). (Plants and plant products in phy-

idade do sobreiro em Portugal [Dialogues and modes of collective action for totherapy) Plantas e Produtos Vegetais em Fitoterapia. Lisboa: Fundac¸ ão Calouste

sustainability of the cork oak in Portugal]. e-cadernos CES, 10, 70–90 [in Por- Gulbenkian. [in Portuguese].

tuguese]. Curtis, J. T., & McIntosh, R. P. (1951). An upland forest continuum in the prairie-forest

Azul, A. M., Castro, P., Sousa, J. P., & Freitas, H. (2009). Diversity and fruiting pat- border region of Wisconsin. Ecology, 32(3), 476–496.

terns of ectomycorrhizal and saprobic fungi as indicators of land-use severity in Dana, E. D., Vivas, S., & Mota, J. F. (2002). Urban vegetation of Almería City—A contri-

managed woodlands dominated by Quercus suber–a case study from southern bution to urban ecology in Spain. Landscape and Urban Planning, 59(4), 203–216.

Portugal. Canadian Journal of Forest Research, 39(12), 2404–2417. Davies, Z. G., Edmondson, J. L., Heinemeyer, A., Leake, J. R., & Gaston, K. J. (2011).

Azul, A. M., Sousa, J. P., Agerer, R., Martín, M. P., & Freitas, H. (2010). Land use practices Mapping an urban ecosystem service: Quantifying above-ground carbon storage

and ectomycorrhizal fungal communities from oak woodlands dominated by at a city-wide scale. Journal of Applied Ecology, 48(5), 1125–1134.

Quercus suber L. considering drought scenarios. Mycorrhiza, 20(2), 73–88. Diédhiou, A. G., Dupouey, J. L., Buée, M., Dambrine, E., Laüt, L., & Garbaye, J. (2009).

Bon, M. (1988). (Field guide to fungi of Europe) Guía de Campo de los Hongos de Europa. Response of ectomycorrhizal communities to past Roman occupation in an oak

Barcelona: Omega. [in Spanish]. forest. Soil Biology and Biochemistry, 41(10), 2206–2213.

Buée, M., Maurice, J.-P., Zeller, B., Andrianariso, S., Ranger, J., Courtecuisse, R., et al. Directive 92/43/EEC. (1992). Council Directive 92/43/EEC of 21 May 1992 on the

(2010). Influence of tree species on richness and diversity of epigeous fungal conservation of natural habitats and of wild fauna and flora. Official Journal of

communities in a French temperate forest stand. Fungal Ecology, 4(1), 22–31. the European Communities, L206, 7.

Calvente, R., Cano, C., Ferrol, N., Azcón-Aguilar, C., & Barea, J. M. (2004). Analysing Duchesne, L. C. (1994). Role of ectomycorrhizal fungi in biocontrol. In F. L. Pfleger,

natural diversity of arbuscular mycorrhizal fungi in olive tree (Olea europaea & R. G. Linderman (Eds.), Mycorrhizae and plant health. St. Paul, USA: American

L.) plantations and assessment of the effectiveness of native fungal isolates as Phytopatholical Society Press, pp. 27–45.

inoculants for commercial cultivars of olive plantlets. Applied Soil Ecology, 26(1), EEA (European Environment Agency). (2006). Urban sprawl in Europe—The ignored

11–19. challenge, Report N. 10. Copenhagen: EEA., 56 pp.

Carneiro, M., Fabião, A., Martins, M. C., Fabião, A., da Silva, M. A., Hilário, L., et al. EEA (European Environment Agency). (2010). 10 messages for 2010: Urban ecosys-

(2008). Effects of harrowing and fertilisation on understory vegetation and tim- tems. Copenhagen: EEA., 11 pp.

ber production of a Eucalyptus globulus Labill. plantation in Central Portugal. Fabião, A., Martins, M. C., Cerveira, C., Santos, C., Lousã, M., Madeira, M., et al. (2002).

Forest Ecology and Management, 255(3–4), 591–597. Influence of soil and organic residue management on biomass and biodiversity

Castroviejo, S., et al. (Eds.). (1986–2010). Flora Iberica. Plantas Vasculares de la Penín- of understory vegetation in a Eucalyptus globulus Labill. plantation. Forest Ecology

sula Ibérica e Islas Baleares (Iberian flora. Vascular plants of the Iberian Peninsula and Management, 171(1–2), 87–100.

and Balearic Islands). Madrid: Real Jardín Botánico [in Spanish]. FAO (Food, Agriculture Organization of the United Nations). (2007). The urban pro-

Chapin, F. S., III, Zavaleta, E. S., Eviner, V. T., Naylor, R. L., Vitousek, P. M., Reynolds, ducer’s resource book. A practical guide for working with low income urban and

H. L., et al. (2000). Consequences of changing biodiversity. Nature, 405(6783), peri-urban producers organizations. Rome: FAO., 137 pp.

234–242. Finlay, R. D. (2008). Ecological aspects of mycorrhizal symbiosis: With special

Chiesura, A. (2004). The role of urban parks for the sustainable city. Landscape and emphasis on the functional diversity of interactions involving the extraradical

Urban Planning, 68(1), 129–138. mycelium. Journal of Experimental Botany, 59(5), 1115–1126.

Chilvers, G. A. (1968). Some distinctive types of eucalypt mycorrhiza. Australian Franco, J. A., & Afonso, M. R. (1971–2003). (New flora of Portugal (continent and

Journal of Botany, 16(1), 49–70. azores)) Nova Flora de Portugal (Continente e Ac¸ ores). Lisboa: Sociedade Astória.

CMC (Câmara Municipal de Coimbra). (2008). (Municipal master plan of [in Portuguese].

Coimbra—Review: Characterization studies) Plano Director Municipal de Frey-Klett, P., Garbaye, J., & Tarkka, M. (2007). The mycorrhiza helper bacteria revis-

Coimbra—revisão: estudos de caracterizac¸ ão. Coimbra: Direcc¸ ão Municipal ited. New Phytologist, 176(1), 22–36.

de Administrac¸ ão do Território, Departamento de Planeamento, Divisão de Garrido-Lestache, J. S. (2001). Polinosis en Madrid. In M. Gutiérrez, C. Sáenz, E.

Ordenamento e Estratégia., 95 pp. [in Portuguese]. Aránguez, & J. Ordónez (Eds.), Polen Atmosférico en la Comunidad de Madrid

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011

G Model

LAND-2183; No. of Pages 15 ARTICLE IN PRESS

L. Barrico et al. / Landscape and Urban Planning xxx (2012) xxx–xxx 15

(Atmospheric pollen in the Madrid community. Documentos Técnicos de Salud M. F. Allen (Ed.), Mycorrhizal functioning: An integrated plant–fungal process (pp.

Pública n 70). Dirección General de Salud Pública. Consejería de Sanidad. Comu- 357–423). New York: Chapman & Hall.

nidad de Madrid, pp. 27–35 [in Spanish]. Mueller-Dombois, D., & Ellenberg, H. (1974). Aims and methods of vegetation ecology.

Gerhardt, E., Vila, J., & Llimona, X. (2000). (Mushrooms of Spain and Europe) Hongos New York: John Wiley & Sons.

de Espa˜na y de Europa. Barcelona: Omega. [in Spanish]. Pato, R. L., Tavares, A. O., & Magalhães, M. C. (2008). Developments in land use in

Grove, J. M., Troy, A. R., O’Neil-Dunne, J. P. M., Burch, W. R., Jr., Cadenasso, M. L., & a periurban area of central Portugal: The importance of biophysical parame-

Pickett, S. T. A. (2006). Characterization of households and its implications for ters. In Geo-environment and landscape evolution III. WIT transactions on built

the vegetation of urban ecosystems. Ecosystems, 9(4), 578–597. environment, vol. 100. UK: The New Forest., pp. 109–117.

Gustafsson, L., Appelgren, L., & Nordin, A. (2005). Biodiversity value of potential Parladé, J., Álvarez, I. F., & Pera, J. (1996). Ability of native ectomycorrhizal fungi from

forest fertilisation stands, as assessed by red-listed and ‘signal’ bryophytes and northern Spain to colonize Douglas-fir and other introduced conifers. Mycor-

lichens. Silva Fennica, 39(2), 191–200. rhiza, 6(1), 51–55.

Hietel, E., Waldhardt, R., & Otte, A. (2004). Analysing land-cover changes in relation to Pereira, H. M., Domingos, T., Vicente, L., & Proenc¸ a, V. (Eds.). (2009). Ecos-

environmental variables in Hesse, Germany. Landscape Ecology, 19(5), 473–489. sistemas e Bem-Estar Humano: Avaliac¸ ão para Portugal do Millennium

Huxley, A., Griffiths, M., & Levy, M. (1992). The new royal horticultural society dictio- Ecosystem Assessment (Ecosystems and human well-being: Assessment for

nary of gardening. London and Basingstoke: The Macmillan Press Limited. portugal millennium ecosystem assessment). Lisboa, Portugal: Escolar Editora

Index Fungorum. http://www.index-fungorum.org/names/Names.asp [accessed [in Portuguese].

January 2011]. Pereira, P. M., & Fonseca, M. P. (2003). Nature vs. nurture: The making

INE (Instituto Nacional de Estatística). (2009). (Agricultural statistics—2008) Estatís- of the montado ecosystem. Conservation Ecology, 7(3), 7 [online]. URL:.

ticas Agrícolas—2008. Lisboa: Instituto Nacional de Estatística. [in Portuguese] http://www.consecol.org/vol7/iss3/art7

Jooss, R., Geissler-Strobel, S., Trautner, J., Hermann, G., & Kaule, G. (2009). ‘Con- Pérez-Ramos, I. M., Zavala, M. A., Maranón,˜ T., Díaz-Villa, M. D., & Valladares, F.

servation responsibilities’ of municipalities for target species: Prioritizing (2008). Dynamics of understorey herbaceous plant diversity following shrub

conservation by assigning responsibilities to municipalities in Baden- clearing of cork oak forests: A five-year study. Forest Ecology and Management,

Wuerttemberg, Germany. Landscape and Urban Planning, 93(3–4), 218–228. 255(8–9), 3242–3253.

Karavas, N., Georghiou, K., Arianoutsou, M., & Dimopoulos, D. (2005). Vegetation and Peterson, G., Allen, C. R., & Holling, C. S. (1998). Ecological resilience, biodiversity,

sand characteristics influencing nesting activity of Caretta caretta on Sekania and scale. Ecosystems, 1(1), 6–18.

beach. Biological Conservation, 121(2), 177–188. Peterson, D. W., & Reich, P. B. (2008). Fire frequency and tree canopy structure influ-

Keles¸ , S., Sivrikaya, F., C¸ akir, G., & Köse, S. (2008). Urbanization and forest cover ence plant species diversity in a forest-grassland ecotone. Plant Ecology, 194(1),

change in regional directorate of Trabzon forestry from 1975 to 2000 using 5–16.

landsat data. Environmental Monitoring and Assessment, 140(1–3), 1–14. Rad, J. E., Manthey, M., & Mataji, A. (2009). Comparison of plant species diversity

Kowarik, I. (2011). Novel urban ecosystems, biodiversity, and conservation. Environ- with different plant communities in deciduous forests. International Journal of

mental Pollution, 159(8–9), 1974–1983. Environmental Science and Technology, 6(3), 389–394.

Lilleskov, E. A., & Bruns, T. D. (2001). Nitrogen and ectomycorrhizal fungal commu- Richard, F., Moreau, P.-A., Selosse, M.-A., & Gardes, M. (2004). Diversity and fruiting

nities: What we know, what we need to know. New Phytologist, 149(2), 154–158. patterns of ectomycorrhizal and saprobic fungi in an old-growth Mediter-

Lindgren, P. M. F., & Sullivan, T. P. (2001). Influence of alternative vegetation manage- ranean forest dominated by Quercus ilex L. Canadian Journal of Botany, 82(12),

ment treatments on conifer plantation attributes: Abundance, species diversity, 1711–1729.

and structural diversity. Forest Ecology and Management, 142(1–3), 163–182. Santos, L. (1983). (Urbanization plans for the Coimbra city) Planos de urbanizac¸ ão para

Loures, L., Santos, R., & Panagopoulos, T. (2007). Urban parks and sustainable city a cidade de Coimbra. Coimbra: Museu Nacional de Machado de Castro., 95 pp. [in

planning—The case of Portimão, Portugal. WSEAS Transactions on Environment Portuguese].

and Development, 3(10), 171–180. Santos, K., Kinoshita, L. S., & Rezende, A. A. (2009). Species composition of climbers in

Mabberley, D. J. (2008). Mabberley’s plant – Book: A portable dictionary of plants, their seasonal semideciduous forest fragments of Southeastern Brazil. Biota Neotrop-

classification and uses. Cambridge: Cambridge University Press. ica, 9(4), 175–188.

Magurran, A. E. (2004). Measuring biological diversity. Malden: Blackwell. Smith, S. E., & Read, D. J. (2008). Mycorrhizal symbiosis (third ed.). London: Academic

Marchante, E., Kjøller, A., Struwe, S., & Freitas, H. (2008). Short- and long-term Press.

impacts of Acacia longifolia invasion on the belowground processes of a Mediter- Tavares, A. O., Mendes, J. M., Basto, E., & Cunha, L. (2010). Risk perception, extreme

ranean coastal dune ecosystem. Applied Soil Ecology, 40(2), 210–217. events and institutional trust: A local survey in Portugal. In R. Bris,ˇ C. G. Soares,

Mathieu, R., Freeman, C., & Aryal, J. (2007). Mapping private gardens in urban areas & S. Martorell (Eds.), Reliability, risk and safety: Theory and applications. London:

using object-oriented techniques and very high-resolution satellite imagery. Taylor & Francis Group, pp. 1245–1252.

Landscape and Urban Planning, 81(3), 179–192. UN (United Nations). (2008). World urbanization prospects: The 2007 revision.

Mckinney, M. L. (2006). Urbanization as a major cause of biotic homogenization. ESA/P/WP/205. New York: Department of Economic and Social Affairs, Population

Biological Conservation, 127(3), 247–260. Division., 230 pp.

Meddad-Hamza, A., Beddiar, A., Gollotte, A., Lemoine, M. C., Kuszala, C., & Gianinazzi, UNFPA (United Nations Population Fund). (2009). State of world population 2009.

S. (2010). Arbuscular mycorrhizal fungi improve the growth of olive trees and Facing a changing world: Women, population and climate. New York: UNFPA., 94

their resistance to transplantation stress. African Journal of Biotechnology, 9(8), pp.

1159–1167. Van Herzele, A., & Wiedemann, T. (2003). A monitoring tool for the provision of acces-

Ministério da Agricultura, do Desenvolvimento Rural e das Pescas. (2001). Decreto- sible and attractive urban green spaces. Landscape and Urban Planning, 63(2),

◦ ◦

Lei n. 169/2001, de 25 de Maio de 2001 [Decree-Law n. 169/2001 of 25 May 109–126.

2001]. Diário da República - I Série - A, 121, 3053–3059 [in Portuguese]. Wehner, J., Antunes, P. M., Powell, J. R., Mazukatow, J., & Rillig, M. C. (2010). Plant

Ministério do Ambiente. (1999). Decreto-Lei n. 565/99, de 21 de Dezembro de 1999 pathogen protection by arbuscular mycorrhizas: A role for fungal diversity?

[Decree-Law n. 565/99 of 21 December 1999]. Diário da República - I Série - A, Pedobiologia, 53(3), 197–201.

295, 9100–9114 [in Portuguese]. Wink, M., & van Vyk, B.-E. (2008). Mind-altering and poisonous plants of the world.

Molina, R., Massicotte, H., & Trappe, J. (1992). Specificity phenomena in mycorrhizal Portland, London: Timber Press.

symbioses: Community-ecological consequences and practical implications. In Zar, J. H. (1996). Biostatistical analysis. London: Prentice Hall International.

Please cite this article in press as: Barrico, L., et al. Biodiversity in urban ecosystems: Plants and macromycetes as indicators for conservation

planning in the city of Coimbra (Portugal). Landscape Urban Plan. (2012), doi:10.1016/j.landurbplan.2012.02.011