Arch. Biol. Sei., Belgrade, 61 (2), 307-315, 2009
DOI:10.2298/ABS0901307S
flora of the city of podgorica, montenegro - chorologic structure and comparison with the floras of rome, patras, and salonika
DANIJELA STESEVIC1, S. JOVANOVIC2, and S. SCEPANOVIC1
'Faculty of Science, University of Montenegro, 20000 Podgorica, Montenegro institute of Botany and Jevremovac Botanical Garden, Faculty of Biology, University of Belgrade, 11000 Belgrade, Serbia
Abstract — Research on the geographical structure of the flora of Podgorica revealed that 85.9% of the species are native, while 14.1% are non-native. This ratio is typical of Mediterranean settlements, where even the most urbanized region reflects the overall character of the surrounding flora. In terms of chorologic groups, the three largest are: eury-Mediterranean (18.2%), cosmopolitan (12.6%), and steno-Mediterranean (8.3%). The percentage of endemic and suben-demic plants is also significant (6.8%). Within the group of aliens, species of Asian origin prevail. Comparative analysis of the chorologic spectra of Podgorica, Rome, Patras, and Salonika revealed some similarities.
Key words: Urban flora, chorologic structure, Podgorica, Rome, Patras, Salonika, Montenegro
UDC 581.9(497.16)
INTRODUCTION
In comparison to natural environments, cities represent a relatively young habitat type. Their floras consist of a combination of both native and non-native (alien) components. Plants from surrounding natural ecosystems that can adapt to newly human-created environments are native, while species originating from geographically distant areas and introduced intentionally or unintentionally by man generally belong to the alien flora. In the geobotanical literature, all plants that become part of the flora through the direct or indirect impact of man are defined as anthropophytes. The first classification of anthropophytes was given by Thellung (1922). He distinguished two main categories based on the origin of species: apophytes, or elements of the native flora; and anthropo-chores, or elements of some alien flora. According to Schroeder (1969), anthropochores can be classified on the basis of three criteria: i) by their degree of naturalization (idiochorophytes, agriophytes, epecophytes, ephemerophytes, and argasiophytes); ii) by the time of immigration (idiochorophytes,
archaeophytes, and neophytes); and iii) and by the manner in which man supported their immigration (idiochorophytes, acolutophytes, xenophytes, and ergasiophytes). On the other hand, Trinajstic (1975) combined three criteria (chronological, anthropological, and ecological) and distinguished four main categories: archaeophytes, paleophytes, neophytes, and neotophytes. Each of these categories are then divided into four subcategories: ergasiophytes, ergasiophygophytes, epekophytes, and ephemerophytes. Further, Trinajstic (1975) distinguished a unique category of helenopalophytes from the Adriatic Coast of Yugoslavia.
It is often very difficult to determine the exact date of introduction of a species. Archaeophytes are particularly difficult to distinguish from original species, since original and secondary areas of distribution continuously overlap. The differentiation of such taxa is further complicated by the time that has elapsed since the original introduction. Indeed, it is not always clear whether a species is native or introduced (Sykora and Westhoff, 1997).
Besides the aforementioned categories, the
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Fig. 1. Geographical locations of Patras, Podgorica, Rome, and Salonika.
urban flora also includes anekophytes or obligate weeds (Scholz, 1991). These plants have coexisted with humans since prehistoric time, which has resulted in a high level of uncertainty regarding their native ranges. This group includes: Bromus hordeaceus, Capsella bursa-pastoris, Chenopodium album, Cynodon dactylion, Hordeum leporinum, Poa annua, Senecio vulgaris, and Stellaria media (Sukopp and Scholz, 1997).
The two main objectives of this paper were: i) to present the general chorologic spectrum of the flora of Podgorica; and ii) to compare the chorologic spectra of Podgorica, Rome, Patras, and Salonika, with special reference to structure of the alien flora.
In addition, we wanted to demonstrate the importance of the native component of the flora and the inherent need to protect it by preserving remnants of both natural and seminatural habitats. Just as importantly, we call attention to alien plants and the threat they bring to diversity of the native flora.
Some general information about the selected cities is given in Table 1, while their geographical locations are shown on Fig. 1.
MATERIALS AND METHODS
The flora within the city of Podgorica currently consists of 1227 taxa (Stesevic and Jovanovic, 2008), four of which are excluded from our analysis: Fraxinus excelsior, Asphodelus albus, and Myricaria germanica (uncertain data taken from the literature); and the hybrid taxon Carex acuta x elata.
The nomenclature follows Tutin et al. (1964-1980, 1993), in some cases Greuter et al. (1984-1989).
The chorologic elements are mainly defined according to Pignatti (1982). For species which are missing, we follow Tutin et al. (1964-1980, 1993), Gajic (1980), Greuter et al. (1984-1989), and Silic (1990). Table 2 outlines the chorologic spectrum of the flora of Podgorica with abbreviations as defined by Pignatti (1982).
Pignatti's classification system was chosen instead of the more generally accepted one of Stevanovic (1992) owing to compatibility with
Table 1. General information about the cities of Patras, Podgorica, Rome, and Salonika: area, number of inhabitants, climate type, average annual temperature, and average annual rainfall.
City
Area (km2)
No. of citizens
Climate type
Average annual temperature (°C)
Annual average rainfall (mm)
Patras
Podgorica
Rome Salonika
55
86
300 61
170,000
137,000
2,900,000 1,000,000
Typical Mediterranean
Moderate Mediterranean
Moderate Mediterranean
Typical Mediterranean
17.8
15.5
15.1 15.7
667.5
1625.3
839 447.7
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the chorologic data reported for the other three selected (sub)Mediterranean settlements: Rome (Celesti-Grapow, 1995); Patras (Chronopoulos and Christodoulakis, 1996, 2000); and Salonika (Krigas and Kokkini, 2004, 2005).
We use the term alien (sensu Richardson et al., 2000) to embrace the following related terms: naturalized, invasive, casual ephemeral, introductioned, occasional escaped plants, and cultivation relics.
In a few cases, it was necessary to harmonize the data according to Pysek et al. (2002) due to inconsistent information about the origin of some alien taxa.
Because of the lack of information about time of introduction, structure of the alien flora is given only in respect to its origin. If a species distribution covered more than one continent, it was considered as a representative of each of them.
Similarity between the alien floras of Podgorica, Rome, Salonika, and Patras is expressed by Sorensen's index of similarity:
Q/S = [2 j/(a + b)] x 100
j - number of species common to both floras,
a - total number of species of the first of two floras to be compared,
b - total number of species of the second flora. Abbreviations:
(I) - element of native (indigenous) flora
(A) - element of alien flora and
(C) - cosmopolitan element.
The general information about the compared cities presented in Table 1 was gathered from the following sources: Podgorica (Stesevic and Jovanovic, 2008); Rome (Celesti-Grapow, 1995); Patras (Chronopoulos and Christodoulakis, 1996); and Salonika (Krigas and Kokkini, 2004, 2005; Hellenic National Meteorological Service: www.hnms.gr).
RESULTS AND DISCUSSION
Table 2 presents the chorologic spectrum of the flora of the urban area of Podgorica. It can be seen that 85.9% of the flora are indigenous species (I),
Table 2. Chorologic spectrum of the flora of the urban area of Podgorica (classification following Pignatti, 1982).
Chorologic type/group	No. of sp.	%	Chorologic type/group	No of sp.	%
Native flora	1051	85.9%	VII OROF. S. EURO	10	0.8
I ENDEMIC	83	6.8	Vila OrofS. Euro	5	0.4
la Endemic	53	4.3	Vllb Orof. SE. Euro	4	0.3
lb Subendemic	30	2.5	VIIc Orof. SE. Euro-Cauc	1	0.1
II STENOMED	101	8.3	VIII BOR	64	5.2
III EURYMED	233	18.2	Villa Circumbor	33	2.6
IV MED-MONT	21	1.7	VHIb Euro-Sib	31	2.5
V EURAS S. L.	323	26.5	VIIIc Circum Arct.-Alpin	1	0.1
Va Paleotemp	62	5.1	IX WIDE DISTRIBUTION	370	30.3
Vb Euras	95	7.7	IXa Pantrop	1	0.1
Vc S. Euro-S. Sib	57	4.7	IXb Med-Tur	31	2.5
Vd Euro-Cauc	49	4	IXc Paleosubtrop	3	0.2
Ve Europ	18	1.5	IXd Cosm	154	12.6
Vf C. Euro	12	1	IXe Aliens	172	14.1
Vg S. Euro	30	2.5			
VI ATL	27	2.2			
Via W. Euro	6	0.5			
VIb Med-Atl	21	1.7	TOTAL	1223	100
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Fig. 2. Structure of the alien flora of Podgorica with respect to origin. If a species distribution covers more than one continent, it is considered as a representative of each of them.
while only 14.1% are alien species (A). Similar ratios between these two components were also presented for the floras of Rome: (I) = 84.7%, (A) = 15.3% (Celesti-Grapow, 1995), Patras: (I)= 87.6%, (A)= 12.4% (Chronopoulos & Christodoulakis, 1996 & 2000) and Thessaloniki (I)= 85.5%, (A)= 14.5%, (Krigas & Kokkini, 2004, 2005). Investigating the flora and vegetation of different Mediterranean settlements, Celesti-Grapow (1998) showed that even the most urbanized regions reflected the flora of their immediate surroundings and were rich in native species, while participation of aliens was low. Additionally, the role of apophytes was emphasized. In contrast to the Mediterranean, it has been found that Central European cities have a more uniform
flora with a higher abundance of aliens, which comprise 20-60% (average 35-40%) (Brandes, 1989; Pysek, 1998).
As for chorologic types, the widely distributed (IX: 30.3%) and Eurasian (V: 26.5%) types are prevalent, while among chorologic groups, the eury-Mediterranean (18.2%), cosmopolitan (12.6%), and steno-Mediterranean (8.3%) groups are (sub)dominant. The percentage of endemic and subendemic taxa is also significant (6.8%). The most abundant endemic taxa (4.3%) are Dinaric and Dinaric-Balkan elements of South European mountainous distribution (Genista sericea, Satureja montana illyrica, Micromeria parviflora, Asperula
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Structure of aienflora
%
■ EUROPA □ ASIA Q AFRICA SAMN HAIvD SAIvE
E3 AUSTRALIA
Roma Pattas Podgorica TtessalontM
Fig. 3. Structure of the alien floras of Rome, Patras, Podgorica, and Salonika.
Table 3. Structure of the alien flora of Podgorica with respect to origin. If a species distribution covers more than one continent, it is considered as a representative of each of them.
Continent	No. of species	%
Europe	39	22.7
Asia	75	43.6
Africa	11	6.4
North America (AMN)	40	23.3
Central America (AMC)	14	8.1
South America (AMS)	24	14.0
Australia	1	0.6
Table 4. Values of the Sorensen similarity index for the alien flora of Podgorica compared to those of Rome, Patras, and Salonika.
Cities_Sorensen's Q/S index_Value (%)
Podgorica-Rome                                           2 x 97 * 100/(172 + 196) 52.7 Podgorica-Salonika                                        2 x 75 * 100/(172 + 147) 47 Podgorica-Patras_2 x 48 * 100/(172 + 93)_32.2
scutellaris, etc.), as well as Illyrian (Adriatic) and Illyrian-Balkan elements of Mediterranean distribution {Chaerophyllum coloratum, Crocus dalmaticus, Hyacinthella dalmatica, Dianthus ciliatus dalmaticus, Hieracium waldsteinii, Rhamnus orbicularis, etc.). Subendemics (2.5%) were mainly presented by Balkan-Apennine taxa (Peucedanum coriaceum, Onosma echinoides, Bupleurum veronense, Matthiola fruticulosa, etc.). Because endemic and subendemic
taxa are set aside as a separate chorologic group, participation of the Mediterranean mountainous and South European orophytic groups is considerably reduced (med-mont = 1.7% and orof. s. euro = 0.8%).
Due to the abundance of natural and seminatu-ral habitats within the city of Podgorica, numerous endemic and subendemic taxa are recorded in the central zone. However, rapid urbanization and
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insufficient preservation of remaining fragments of natural habitat put serious pressure on the native flora.
The majority of endemic and subendemic species are recorded from areas near the courses of the rivers Moraca and Cijevna, which are well known as floristically rich and diverse (Bulic, 1993, 1998, 2008; Bulic et al., 2008). Part of this floristic diversity is included in the flora of the city of Podgorica.
Compared with the share of endemics in the floras of Rome (0.8%), Patras (3.2%), and Salonika (8.1%), the value of 6.8% obtained for Podgorica is relatively high (Fig. 2).
Common features of the chorologic spectra of the four cities are:
1. Prevalence of elements with wide geographic distribution and approximately the same ratio of cosmpolitan (C) and alien (A) components: in Rome, (C) = 11.3%, (A) = 15.3%; in Patras, (C) = 12.8%, (A) = 12.4%; in Salonika, (C) = 12.8%, (A) = 14.5%; and in Podgorica, (C) = 12.6%, (A) = 14.1%.
2. High participation of the Mediterranean element in the broad sense (stenomed, eurimed, med-mont, and med-tur): Patras (54%), Rome (44%), Salonika (39.7%), and Podgorica (30.7%).
With respect to participation of the Eurasian element in the broad sense, Podgorica surpasses the other cities by 26.5%. Within this chorologic type, the Eurasian (7.7%) and paleotemporal (5.1%) groups dominate. The South European-South Siberian group (which includes the Pontic element and the majority of its subelements) contributes 4.7% and the European-Caucasian group 4%.
In the boreal chorologic type (5.2%), the cir-cumboreal and Euro-Siberian groups show about the same percentage (2.6 and 2.5%, respectively).
Atlantic elements participate in the spectrum with 2.2%.
The contribution of alien taxa to the chorologic spectrum of Podgorica is 14.1%, which can be considered a relatively low value. Saarisalo-Taubert
(1963) pointed out the relationship between age of a settlement and structure of its flora. Following this, we consider the main reason for the small number of aliens to be an artifact of the old age of Podgorica. According to Sukopp et al. (1979), Sukopp andW-erner (1983), Pyšek (1989a), and Kowarik (1990), development of a transportation system and intensive trade open better options for the introduction and spread of new species and contribute to their increasing numbers. We maintain that poorly developed trade and transportation networks are a possible second reason for the low numbers of aliens.
Other studies have demonstrated a positive correlation between the number of alien taxa and settlement size (Pyšek, 1989b, 1998; Pyšek and Pyšek, 1991; etc.). Our comparative analysis supports this assumption. Rome (300 km2), the largest city in our study, is characterized by the highest contribution (15.3%), while Patras, the smallest city (55 km2), has the lowest share of aliens (12.4%).
Table 3 shows structure of the alien flora in the urban area of Podgorica.
Among alien plants in the urban area of Podgorica, species of Asian and North American distribution are prevalent. In addition, the majority of taxa are considered to be escaped from cultivation. In many countries, deliberate introduction of plant species is considered to be the main road of introduction (Groves, 1998; Reinhard and White, 2001; Mack, 2003). New trends in horticulture contribute a lot. Almost as a rule biological characteristics that make species attractive for breeding contribute to their successful expansion. According to Kowarik (2003), the naturalization rate of deliberately introduced species is considerably higher than the rate of accidentally introduced ones.
For example, Broussonetia papyrifera, an ornamental species found within the city of Podgorica, has spread rapidly due to vegetative reproduction and has started to outcompete Ailanthus altissima. Recently, pampas grass (Cortaderia selloana), a species on the EPPO list of invasive alien plant species (http://www.eppo.org/QUARANTINE/ias_ plants.htm), has been used in landscaping of city
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lawns and parks. Consequently, we expect this species to join the list of other alien species escaped from cultivation within Podgorica.
The comparative spectra of the alien floras of Rome, Patras, Podgorica, and Salonika are given in Fig. 3.
With the exception of Patras, where South American taxa dominate, a common feature of the alien floras of the compared cities is the prevalence of taxa having Asian origin. The majority of these taxa were introduced as ornamentals. In all spectra, species of Australian origin have very low participation or are completely missing (Patras, Salonika).
Values of the Sorensen index show the greatest similarity between the alien floras of Podgorica and Rome (52.7%, see Table 4). In view of the similarity in taxonomie structure of these two floras (Steševič and Jovanovič, 2008) and similar climatic conditions, such a result was expected.
Observing the trends in floristic composition over the past two centuries, many authors noted an obvious decrease in the number of native species. According to Sukopp (1973), during the period from 1850 to 1950, some European cities faced extinction rates between 4 and 16%. The example of Warsaw (Sudnik-Wojcikovska, 1987) shows that over a period of 150 years, 15% of native species became extinct, while for Zurich the rate for the last 160 years was only 5.7% (Landolt, 2001). For the Czech industrial city of Plzeň, the decrease of native species was 11.5% over the past 120 years (Chocholouškova and Pyšek, 2003).
One of the most drastic examples of general floristic loss is the case of Turnhout, Belgium, where nearly 25% of the flora became extinct between 1888 and 1990 (Van der Veken et al., 2004).
The loss of native flora due to spreading of alien species is a phenomenon known as biotic homog-enization (McKinney and Lockwood, 1999, 2006; Olden et al., 2004; La Sorte and McKinney, 2006).
The aforementioned unplanned rapid urbanization causes on the one hand a loss of native species
and on the other creates space for expansion of already established and newly introduced alien species. We expect that the effects of biotic homogeni-zation will be evident soon.
Acknowledgments — The authors would like to thank Leonardo Rosati for generous assistance in classification of some questionable chorologic elements; Anton Drescher and Danka Petrovic for valuable comments; and Marta J. Coleman for improving our English. This study was funded by the Ministry of Science and Education, Podgorica, Montenegro (project code PMN 72).
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'IIpupodHO-MameMamuHKU (fianymnem, YHU6ep3umem IjpHe Tope, 20000 rioflropiiija, LI,pHa Ibpa 2MHcmumym 3a öomamitcy u Bomammtca 6avuma "Jeepemoean,", Buonoiutcu (fianymnem, YHU6ep3umem y Eeozpady,
11000 Beorpafl, Cpönja
XopojioniKH cneicrap IIo,aropHne paniHjiaH>eH je Ha IX apean ranoßa, c thm uito HarHBHOJ kom-noHeHTH (J)jiope npHna^a 85.9 %, a ajioxTOHOJ 14.1 %. PejiaTHBHO HH3aK yaeo ajioxTOHe KOMnoHeHTe jecTe reHepajiHa ofljiHKa Me^HTepaHCKHx HaceoÖH-Ha HHJ h, naK h Hajyp6aHH30BaHHJ h cerMeHTH y Be jih-koj Mepn OACJiHKaBajy KapaKTep (Jmope OKpyaceita.
nocMarpaHO Ha HHBoy apean ranoBa y xopojio-uiKOM cneicrpy ^OMHHHpajy Bpcre iimpoKor pacno-CTpaH>eH>a (IX: 30.3 %) h eBpoa3HJCKor (V: 26.5 %). y norjie^y apean rpyna Kao AOMHHaHrae ce ncrany eypHMe^HTepaHCKa (18.2 %), KOCMonojiHTCKa (12.6 %) h creHOMcaHTepaHCKa rpyna (8.3 %). IToceöaH nenar cneicrpy (Jmope ,aajy enaeMHHHH h cyöenae-
mhhhh TaKCOHH (6.8 %).
y OKBHpy eBpoa3HJCKor apean rana 6pojeM BpcTa ce H3^Bajajy eBpoa3HJCKa rpyna y yaceM cmh-cjiy (7.7 %) h najieoTeMnopajiHa (5.1 %). BopeajiHH apean ran je 3acTynji>eH ca 5.2 %, y OKBHpy Kojer ce Hcrany nnpicyMOopeajiHa (2.6 %) h eypocHÖnp-CKa rpyna (2.5 %). ÄTjiaHTCKH eneMeHT je 3acry-njbeH ca 2.2 %.
yoeo a^BeHraBHe KOMnoHeHTe y (JrnopH IToa-ropnue H3HOCH 14.1 %, uito ce Moace CMaTpara 3a
pejiaraBHO Many Bpe^HOCT. 06jauiH>aBaMO je MajiOM CTapoinhy HaceoÖHHe, Kao h p,o He^aBHO jioine pa3-
BHJeHOM TpaHCnOpTHOM h TprOBHHCKOM MpeacoM.
y cneKTpy anoxTOHe (Jmope IIo,aropHne Kao ^OMHHaHTe cy npncyrae BpcTe a3HJCKor h ceBepHoa-MepHHKor nopeKjia, a HaJBehn 6poj BpcTa ce CMaTpa 3a "oflöerjie H3 KynraBauHJe".
ynoperjyjyhH cneKTpe chnopaIIo,aropHne, PnMa, IlaTpaca h CojiyHa vohhjih cmo hh3 cjihhhocth: AOMHHauHJy ejieMeHara nmpoKor pacnpocrpaibe-h>a h npHÖJiiüKaH yaeo KOCMonojiHTCKe h anoxro-He (Jmope; bhcok yaeo McanrepaHCKor eneMeirra (cTeHOMe^HTepaHCKor, eypHMcaHrepaHCKor, Me^h-TepaHCKO-MOHTaHor h Me,aHTepaHCKO-TypaHCKor); flOMHHai(HJy a3HJCKor ejieMeHTa y CTpyKTypn ajiox-TOHe (Jmope Kao h HaJMaity 3acTynji>eHOcra hjih norayHO o^cycTBO aycTpajinjcKor ejieMeHTa.
C oÖ3HpoM Ha Harjiy h HenjiaHCKy yp6aHH3auH-jy, Koja c je^ne crpaHe y3poKyje ryönraK HaraBHe KOMnoHeHTe (Jmope, a ca ,apyre nmpeibe Beh nocTO-jehnx h nojaBy hobhx ajioxTOHHx BpcTa, oneKyjeMO A,a he Tpena öhothhkc xoMoreffißauHJe 6hth vcko-po eBHTieHTaH h Ha noflpynjy rkmropHne.