Sarajlić, N., Jogan, N.: Alien flora of the city of Sarajevo (Bosnia and Herzegovina). Biologica Nyssana, 8 (2). BIOLOGICA NYSSANA 8 (2)  December 2017: 129-136 Sarajlić, N., Jogan, N.  Alien flora of the city of Sarajevo… 129 Original Article Received: 09 November 2017 Revised: 24 December 2017 Accepted: 25 December 2017 Alien flora of the city of Sarajevo (Bosnia and Herzegovina) Nermina Sarajlić1, Nejc Jogan2 1Ornithological Society „Naše ptice“, Semira Frašte 6, 71000 Sarajevo, Bosnia and Herzegovina 2University of Ljubljana, Biotechnical Faculty, Department of Biology, Večna pot 111, 1000 Ljubljana, Slovenia * E-mail: nermina_sarajlic@yahoo.com Abstract: Sarajlić, N., Jogan, N.: Alien flora of the city of Sarajevo (Bosnia and Herzegovina). Biologica Nyssana, 8 (2). December, 2017: 129-136. This paper presents the inventory and brief analysis of 82 alien vascular plant taxa of the urban and suburban area of the city of Sarajevo. The checklist is based on field work that has been carried out from summer 2015 to autumn 2017. Each taxon is given with information concerning its life-form, time and mode of introduction, geographic origin and previously reported occurrence in the area. Most alien plants were the members of the Asteraceae (incl. Cichoriaceae), therophytes, neophytes, originated from North and South America and deliberately introduced. The values of indicators of anthropogenic changes showed the considerable anthropogenic influence on the total flora. Key words: Alien plants, urban flora, Sarajevo Apstrakt: Sarajlić, N., Jogan, N.: Alohtona flora grada Sarajeva (Bosna i Hercegovina). Biologica Nyssana, 8 (2), Decembar, 2017: 129-136. U radu je dat spisak i kratka analiza 82 alohtona taksona vaskularnih biljaka zabeleženih u urbanom i suburbanom delu grada Sarajeva od leta 2015. do jeseni 2017. godine. Za svaki takson navedeni su podaci o životnoj formi, vremenu i načinu introdukcije, poreklu i najraniji objavljeni podatak o njegovom prisustvu na istraživanom području. Izračunati su indikatori antropogene promene flore. Najbrojnije alohtone vrste zabeležene tokom ovog istraživanja su pripadnici porodice Asteraceae (uključujući Cichoriaceae), terofite, neofite poreklom iz Severne i Južne Amerike, koje su u Evropu unesene namerno. Vrednosti indeksa antropogene promene pokazuju značajan antropogeni uticaj na ukupnu floru grada Sarajeva. Ključne reči: Alohtone biljke, urbana flora, Sarajevo 8 (2) • December 2017: 129-136 DOI: 10.5281/zenodo.1135953 BIOLOGICA NYSSANA 8 (2)  December 2017: 129-136 Sarajlić, N., Jogan, N.  Alien flora of the city of Sarajevo… 130 Introduction Urban habitats are generally characterized by high levels of disturbance, high fertility and heterogeneity of habitats, suitable for development of numerous plant species, including many alien plants. Alien (exotic, adventive, introduced, allochthonous, non- indigenous, non-native) plants are those whose presence in a certain area is due to intentional or accidental introduction as a result of human activities (P y š e k , 1995; R i c h a r d s o n et al., 2000; P y š e k et al., 2004). According to their spreading ecology in a certain territory, alien plants can be divided in three groups: casual, naturalized and invasive. According to the time when they were introduced into Europe, alien plants can be classified as archaeophytes (introduced before the year 1500) and neophytes (introduced after the year 1500) (P y š e k , 1995, K o w a r i k , 1995; P y š e k et al., 2002; P r e s t o n et al., 2004; L a S o r t e et al., 2007). Some of them were introduced deliberately, as ornamental, edible or medicinal plants, and others came to Europe accidentally, without the deliberate actions of humans. The city of Sarajevo was founded in the 15th century, but expanded, mostly towards the west, only during the post-World War II era. Intense exchange of goods since ancient times and further urbanization, construction of roads and railway enabled the introduction of new plants, some of which slowly become naturalized part of the flora. Literature on alien flora of the city of Sarajevo is scarce, and the presence of some alien plants is either mentioned in general floristic studies (K o m š a , 1928; P a v l o v i ć , 1987; T o m o v i ć -H a d ž i a v d i ć & Š o l j a n , 2006), or studies focused on particular species (S l a v n i ć , 1960; A b a d ž i ć , 1986/87; Š o l j a n & M u r a t o v i ć , 2000; Š o l j a n , 2011; M e m i š e v i ć -H o d ž i ć et al., 2015; S a r a j l i ć et al., 2016; S u l j i ć et al., 2016). This paper presents a list of hitherto recorded alien species and a brief analysis of the alien flora of the city of Sarajevo. The inventory of 82 taxa is provided based on the field work performed in 2015, 2016 and 2017, updating previous floristic knowledge for the investigated area. Material and methods Study area The city of Sarajevo is located in the Sarajevo valley, on the banks of Miljacka river, at an average altitude between 520 and 750 m a. s. l. (Fig. 1). The central parts of the city are situated in the lower parts of Fig. 1. Geographical position of investigated area (the yellow line limits the area in which the survey was performed) BIOLOGICA NYSSANA 8 (2)  December 2017: 129-136 Sarajlić, N., Jogan, N.  Alien flora of the city of Sarajevo… 131 Sarajevo polje, and the suburbs are scattered on the slopes of surrounding hills and mountains. The area of Sarajevo is under influence of mid-European continental climate from the North, and the Mediterranean from the South. Field investigation The field survey was performed in the urban part of four municipalities (Novi Grad, Novo Sarajevo, Centar, Stari Grad) of the city of Sarajevo (Fig. 1), in an area of 32 km2, from the summer of 2015 to the autumn of 2017. Only taxa that had not been deliberately planted were recorded. Data analysis The nomenclature follows Euro+Med PlantBase and The International Organization for Plant Information Database. Asteraceae family was considered in wider sense (incl. Cichoriaceae). The taxa are listed in alphabetic order, followed by designations for life form (phanerophyte - Ph, chamaephyte - Ch, hemicryptophyte - H, geophyte - G, hydrophyte - Hy and therophyte - T), period of introduction (archaeophytes - ARC and neophytes – NEO), estimated mode of introduction into the region (deliberate, by planting – DEL, accidental – ACC or in both modes - D-A) geographic origin and reported first record for the Sarajevo area. Life forms were given according to R a u n k i a e r (1934), and time and mode of introduction and geographic origin according to P y š e k et al. (2002), M o s y a k i n & Y a v o r s k a (2003) and I g n a t i e v a & K o n e c h n a y a (2004). First records for the area of Sarajevo were given according to available literature sources (see References and Appendix 1). The indicators of anthropogenic changes in the flora of Sarajevo were calculated after J a c k o w i a k (1990, 2006), according to W i t o s ł a w s k i & B o m a n o w s k a (2009) as in Tab. 1. Results During this research, a total of 82 alien plant taxa from 71 genera and 38 families were recorded. The families with the highest number of alien taxa were Asteraceae (21%), Poaceae (10%), Brassicaceae (7%), Fabaceae (6%), Amaranthaceae (5%) and Solanaceae (5%) (Tab. 2). The other families were represented only with one or two taxa. Table 2. The most abundant families in the alien flora of the city of Sarajevo Family No. of taxa % of total alien flora Asteraceae 17 20.73 Poaceae 8 9.75 Brassicaceae 6 7.31 Fabaceae 5 6.09 Amaranthaceae 4 4.88 Solanaceae 4 4.88 Analysis of life forms showed the domination of therophytes with 47 taxa (57%), followed by phanerophytes with 14 taxa (17%) geophytes (10 taxa, 12%), hemicryphophytes (10 taxa, 12%), and chamaephytes (1 or 1%). The alien flora of the city of Sarajevo consisted of 28 (34%) archaeophytes and 54 (66%) neophytes. Analysis of the geographical origin of the alien flora of Sarajevo (Tab. 3) showed that the majority of species originated from N. and S. America (37 taxa, 45%), followed by those originating from Asia (24 taxa, 24%), Mediterranean (13 taxa, 16%), Eurasia (10 taxa, 12%) and Africa (2 taxa, 2%). Table 1. Indicators of anthropogenic changes (An – total number of alien species, Sp – number of native species, Mt – number of permanently established alien species (Ar + Kn - Df), Ar – number of archaeophytes, Kn – number of kenophytes (neophytes), Df – number of diaphytes (casual aliens)). Indicator Formula for calculation Indicator of total anthropophytization IAnt = An/(Sp+An) ×100% Indicator of permanent anthropophytization IAnp = Mt/(Sp+Mt) ×100% Indicator of total archaeophytization IArt = Ar/(Sp+An) ×100% Indicator of permanent archaeophytization IArp = Ar/(Sp+Mt) ×100% Indicator of total kenophytization IKnt = Kn/(Sp+An) ×100% Indicator of permanent kenophytization IKnp = Kn/(Sp+Mt) ×100% Indicator of modernization IM = Kn/Mt ×100% Indicator of fluctuation changes IF = Df/(Sp+An) ×100% BIOLOGICA NYSSANA 8 (2)  December 2017: 129-136 Sarajlić, N., Jogan, N.  Alien flora of the city of Sarajevo… 132 Table 3. An analysis of the geographical origin of the alien flora of the city of Sarajevo Region Subregion No. of taxa % of total alien flora Africa 2 2.44 East (Af-E) 1 1.22 North (Af-N) 1 1.22 America 37 45.12 South (Am-S) 7 8.54 North (Am-N) 30 36.58 Asia 24 29.27 Asia (As) 4 4.88 Central (As-C) 1 1.22 East (As-E) 8 9.76 South-West (As-SW) 4 4.88 West (As-W) 3 3.66 Eurasia (Eu-As) 10 12.19 Mediterranean (M) 13 15.85 TOTAL 82 100.00 Indicators of anthropogenic changes values in the flora of Sarajevo are presented in Tab. 4. Table 4. Indicators of anthropogenic changes in the city of Sarajevo Indicator % IAnt 12.09 IAnp 8.17 IArt 4.13 IArp 4.31 IKnt 7.96 Iknp 8.32 IM 65.85 IF 4.45 According to our research, which has been taking place since summer 2015, the urban flora of Sarajevo consists of 678 taxa. The indicators of anthropophytization (IAnt = 12.09%; IAnp = 8.17%) showed the considerable anthropogenic influence on the total flora of Sarajevo, and higher indicator values of kenophytization (IKnt = 7.96%; IKnp = 8.32%) showed that the flora of Sarajevo is more influenced by neophytes than by archaeophytes (IArt = 4.13%; IArp = 4.31%). In both archaeophytes and neophytes, the values of total and permanent indicators were similar, showing that alien flora is well established. This was confirmed by the low value of the indicator of fluctuating changes (IF = 4.45%). Discussion Cities usually contain large proportion of alien plants (W i t t i g , 2004), due to developed transport network and diversity of habitats that can be easily colonized by alien species. During this research, we found that the families with the highest number of taxa were Asteraceae and Poaceae. Those two families were also dominant in alien flora of Zagreb (H u d i n a et al., 2012), Sisak (P r u š a et al., 2013), Podgorica (S t e š e v i ć et al., 2014) and Mostar (M a s l o , 2015), probably due to high reproduction rate and specialised dispersion structures on the seeds (P y š e k , 1997). In alien flora of Sarajevo, therophytes were the dominant life-form. The same was recorded in Sisak (Croatia) by P r u š a et al. (2013) and in Mostar by M a s l o (2015). The domination of therophytes is due to the warm and dry microclimate (the “urban heat-island effect”) that characterize urban environments, providing conditions that allow many alien species with higher temperature requirements and tolerance for arid environments to become established. All mentioned cities have the significant share of phanerophytes in their alien flora, mostly due to woody ornamental aliens escaping from cultivation. During this research, neophytes were more numerous than archaeophytes. More neophytes (55%) were also recorded in alien flora of Mostar by M a s l o (2015). According to d e l T r e d i c i (2010), the ratio of neophytes to archaeophytes rises in direct relation to the intensity of human disturbance. This is due to the fact that archaeophytes are typically associated with traditional rural environments or intermediate levels of anthropogenic activities (P r e s t o n et al., 2004), and neophytes are more common in highly disturbed modern anthropogenous habitats covering huge areas with little vegetation coverage and with developed transport facilities and industrial infrastructure contributing to the ‘urban heat-island effect’, which provides distinctive environmental conditions that favor the establishment of species from warmer and drier areas (P y š e k , 1998; P y š e k et al., 2002; G o d e f r o i d & K o e d a m , 2007; L a S o r t e et al., 2007). Also, the cultivation of numerous foreign species along roads, in parks and gardens, presents the source for neophyte colonization (W i t t i g , 2004). The analysis of the geographical origin of the alien flora of Sarajevo showed that the most plants originated from N. and S. America and Asia. The same was found in the city of Podgorica (S t e š e v i ć et al., 2014) and Mostar (M a s l o , 2015). The alien plants originating from N. and S. America and Asia BIOLOGICA NYSSANA 8 (2)  December 2017: 129-136 Sarajlić, N., Jogan, N.  Alien flora of the city of Sarajevo… 133 also dominate in urban flora of Italian cities (C e l e s t i G r a p o w & B l a s i , 1998). This is in a relation with the increased number of neophytes in urban areas, due to the fact that archaeophytes originate primarily from southern Europe and the Near East, and neophytes from North America and Eastern Asia (P y š e k et al., 2002; L a S o r t e et al., 2007). The indicators of anthropophytization (IAnt = 12.09%; IAnp = 8.17%) showed considerable anthropogenic influence on the total flora of the city of Sarajevo, but were not as high as in Savica park area near Zagreb (IAnt = 28.78%; IAnp = 26.76%) calculated by A l e g r o et al. (2013) or Rzeszów Foothills in Poland (IAnt = 21.3%) by Jaźwa & S t a d n i c k a -F u t o m a (2015). This is probably due to the fact that some habitats in the city of Sarajevo (forests and natural grasslands in the suburban parts of city) had very small number of aliens in comparison to the native plants. According to available literature sources, the first alien plants reported from the area of Sarajevo were Panicum miliaceum, Linum usitatissimum, Aesculus hippocastanum, Capsella bursa-pastoris, Conyza canadensis, Helianthus annuus, H. tuberosus, Juglans regia, Phalaris canariensis, Pyrus communis, Sinapis arvensis and Syringa vulgaris (H o f m a n n , 1882). On the other hand, species recorded only recently before our study were Acer negundo, Ailanthus altissima, Antirrhinum majus, Oenothera biennis (T o m o v i ć - H a d ž i a v d i ć & Š o l j a n , 2006), Sedum sarmentosum (Š o l j a n , 2011) and Reynoutria japonica (S a r a j l i ć et al., 2016). During our research, 37 taxa for which there was no earlier data for the area of Sarajevo were found (Appendix 1). Conclusion The results of 3-years research showed that the alien flora of the city of Sarajevo consisted of 82 species from 71 genera and 38 families, of which the Asteraceae (21%) were the most numerous, followed by Poaceae (10%) and Brassicaceae (7%). The analysis of life forms showed the domination of therophytes (57%), followed by phanerophytes (17%). Neophytes (66%) were more numerous than archaeophytes (34%). Analysis of the mode of introduction showed that most aliens (49%) were introduced to Europe deliberately, as horticultural or agricultural plants. 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Tomović-Hadžiavdić V., Šoljan, D. 2006: Urbana flora Sarajeva. Glasnik Zemaljskog muzeja (prirodne nauke), Nova sveska, 32, 121–135. Witosławski, P., Bomanowska, A. 2009: Southern European species in the flora of towns in the central Poland. Botanica Serbica, 33 (2): 115-129. Wittig, R. 2004: The origin and development of the urban flora of Central Europe. Urban Ecosystems, 7: 323–333. Appendix 1. Alien flora of the city of Sarajevo (LF-life form, PI-period of introduction, MI-mode of introduction, O- origin) Species Family LF PI MI O 1st record 1. Abutilon theophrasti Medik. Malvaceae T ARC ACC As-E 2. Acer negundo L. Aceraceae Ph NEO DEL Am-N Tomović-Hadžiavdić & Šoljan (2006) 3. Aesculus hippocastanum L. Hippocastanaceae Ph NEO DEL M Hofmann (1882) 4. Ailanthus altissima (Mill.) Swingle Simaroubaceae Ph NEO DEL As-E Tomović-Hadžiavdić & Šoljan (2006) 5. Alcea rosea L. Malvaceae H NEO DEL M 6. Amaranthus albus L. Amaranthaceae T NEO ACC Am-N Maly (1919) 7. Amaranthus caudatus L. Amaranthaceae T NEO DEL Am-S 8. Amaranthus graecizans L. Amaranthaceae T NEO ACC Af-E 9. Amaranthus retroflexus L. Amaranthaceae T ARC ACC Am-N Beck (1887a) 10. Ambrosia artemisiifolia L. Asteraceae T NEO ACC Am-N Maksimović (1990) 11. Anagallis arvensis L. Primulaceae T ARC ACC M Beck (1887b) 12. Angelica archangelica L. Apiaceae H ARC D-A As-E 13. Antirrhinum majus L. Scrophulariaceae T ARC D-A M Tomović-Hadžiavdić & Šoljan (2006) 14. Armoracia rusticana Gaertn, May & Scherb. Brassicaceae G ARC D-A Eu-As Beck (1916) 15. Artemisia annua L. Asteraceae T NEO ACC As-E Beck (1887b) 16. Bassia scoparia (L.) A. J. Scott Chenopodiaceae T NEO DEL As-C Maly (1910) 17. Bidens frondosus L. Asteraceae T NEO ACC Am-N 18. Brassica rapa (L.) L. Brassicaceae T ARC DEL M Maly (1904) 19. Calendula officinalis L. Asteraceae T ARC DEL M 20. Capsella bursa-pastoris (L.) Medik. Brassicaceae H ARC ACC Eu-As Hofmann (1882) 21. Catalpa bignonioides Walter Bignoniaceae Ph NEO DEL Am-N 22. Commelina communis L. Commelinaceae G NEO DEL As-E 23. Cuscuta campestris Yuncker Cuscutaceae T NEO ACC Am-N 24. Datura stramonium L. Solanaceae T NEO ACC Am-N Beck (1887b) 25. Eleusine indica (L.) Gaertn. Poaceae T NEO ACC As 26. Erigeron annuus (L.) Desf. Asteraceae T NEO ACC Am-N Maly (1910) 27. Erigeron canadensis L. Asteraceae T NEO ACC Am-N Hofmann (1882) 28. Euphorbia prostrata Aiton Euphorbiaceae T NEO ACC Am-N 29. Galinsoga parviflora Cav. Asteraceae T NEO ACC Am-N Maly (1933) 30. Galinsoga quadriradiata Ruiz & Pav. Asteraceae T NEO ACC Am-N 31. Gleditsia triacanthos L. Fabaceae Ph NEO DEL Am-N Šoljan et al. (2006) 32. Helianthus annuus L. Asteraceae T NEO DEL Am-N Hofmann (1882) 33. Helianthus tuberosus L. Asteraceae G NEO DEL Am-N Hofmann (1882) BIOLOGICA NYSSANA 8 (2)  December 2017: 129-136 Sarajlić, N., Jogan, N.  Alien flora of the city of Sarajevo… 136 34. Hemerocallis fulva (L.) L. Xanthorrhoeaceae G NEO DEL As-E Maly (1928) 35. Hesperis matronalis L. Brassicaceae H ARC ACC Eu-As 36. Impatiens balfourii Hook. f. Balsaminaceae T NEO DEL As 37. Impatiens glandulifera Royle Balsaminaceae T NEO DEL As 38. Iris germanica L. Iridaceae G ARC DEL Eu-As 39. Juglans regia L. Juglandaceae Ph ARC DEL As-SW Hofmann (1882) 40. Juncus tenuis Willd. Juncaceae H NEO ACC Am-N 41. Lepidium virginicum L. Brassicaceae T NEO ACC Am-N 42. Linum usitatissimum L. Linaceae T ARC D-A As-W Formanek (1889) 43. Lonicera nitida E.H. Wilson Caprifoliaceae Ph NEO DEL Az-SW 44. Lycopersicon esculentum Mill. Solanaceae T NEO DEL Am-S 45. Matricaria discoidea DC Asteraceae T NEO ACC Am-N Maly (1912) 46. Medicago arabica (L.) Huds. Fabaceae T ARC ACC M Beck (1887b) 47. Medicago sativa L. Fabaceae H ARC ACC Eu-As Beck (1896) 48. Morus nigra L. Moraceae Ph ARC DEL As-SW 49. Oenothera biennis L. Onagraceae H NEO DEL Am-N Tomović-Hadžiavdić & Šoljan (2006) 50. Oenothera erythrosepala Borbas Rosaceae H NEO DEL Am-N 51. Oxalis dillenii Jacq. Oxalidaceae H NEO ACC Am-N Maly (1928) 52. Oxalis fontana Bunge Oxalidaceae H NEO ACC Am-N 53. Panicum capillare L. Poaceae T NEO ACC Am-N 54. Panicum miliaceum L. Poaceae T ARC D-A As-E Formanek (1888) 55. Papaver rhoeas L. Papaveraceae T ARC ACC M Beck (1916) 56. Parthenocissus quinquefolia (L.) Planch. Vitaceae Ph NEO DEL Am-N 57. Paspalum dilatatum Poir. Poaceae T NEO ACC Am-S 58. Petunia × hybrida (Hook.) Vilm. Solanaceae T NEO DEL Am-S 59. Persicaria maculosa Gray Polygonaceae T ARC ACC Eu-As Komša (1928) 60. Phalaris canariensis L. Poaceae T NEO ACC M Hofmann (1882) 61. Platycladus orientalis (L.) Franco Cupressaceae Ph ARC DEL Eu-As 62. Portulaca oleracea L. Portulacaceae T ARC ACC M Beck (1906) 63. Pyrus communis L. Rosaceae Ph ARC DEL Eu-As Hofmann (1882) 64. Ranunculus arvensis L. Ranunculaceae T ARC ACC M Beck (1891) 65. Reynoutria japonica Houtt. Polygonaceae G NEO DEL As-E Sarajlić et al. (2016) 66. Rhus typhina L. Anacardiaceae Ph NEO DEL Am-N 67. Robinia pseudoacacia L. Fabaceae Ph NEO DEL Am-N Maly (1928) 68. Sedum sarmentosum Bunge Crassulaceae Ch NEO DEL As Šoljan (2011) 69. Senecio inaequidens DC. Asteraceae T NEO ACC Af-S 70. Sinapis arvensis L. Brassicaceae T ARC D-A M Hofmann (1882) 71. Solanum tuberosum L. Solanaceae G NEO DEL Am-S 72. Solidago canadensis L. Asteraceae G NEO DEL Am-N 73. Solidago gigantea Aiton Asteraceae G NEO DEL Am-N 74. Sorghum halepense (L.) Pers. Poaceae G ARC ACC M 75. Syringa vulgaris L. Oleaceae Ph ARC DEL Eu-As Hofmann (1882) 76. Tagetes patula L. Asteraceae T NEO DEL Am-S 77. Tanacetum parthenium (L.) Sch.Bip. Asteraceae T NEO DEL As-W Maly (1904) 78. Trifolium arvense L. Fabaceae T ARC DEL Eu-As Maly (1904) 79. Triticum aestivum L. Poaceae T ARC DEL As-SW 80. Veronica persica Poir. Scrophulariaceae T NEO ACC As-W Beck (1887b) 81. Xanthium strumarium L. Asteraceae T NEO ACC Am-N Maly (1912) 82. Zea mays L. Poaceae T NEO DEL Am-S Beck (1887a) Abbreviations: Life forms: Ph - Phanerophyte, Ch - Chamaephyte, H - Hemicryptophyte, G - Geophyte, T - Therophyte; Period of introduction: ARC - Archaeophyte, NEO – Neophyte; Mode of introduction: ACC - Accidental, DEL - Deliberate, D-A - in both ways.