Bellis Perennis - Variations of Physiological Responses in Urban Conditions

Annals of West University of Timişoara, ser. Biology, 2016, vol. 19 (1), pp.77-86

BELLIS PERENNIS - VARIATIONS OF PHYSIOLOGICAL RESPONSES IN URBAN CONDITIONS

Lorena Alina CIOBANU Department of Biology and Chemistry; West University of Timisoara, Romania Corresponding author e-mail: [email protected] Received 26 February 2016; accepted 14 April 2016

ABSTRACT In the present study, Bellis perennis were sampled from park and a nearby street in the urban area of Timisoara and in different time periods, i.e. April and July. The objectives were to examine the potential impacts of traffic pollution on the B. perennis and the repartition of water, dry matter and organic matter into different plant parts (leaves, scapes, inflorescences and roots). Our results would be helpful in understanding the resource distribution within the plant in urban environment. KEY WORDS: physiological parameters, traffic site, Bellis perennis

INTRODUCTION Bellis perennis L. (common daisy) is a perennial herbaceous plant and member of the Asteraceae family. It is widely distributed in Europe and North Africa, but is commonly found as an invasive plant in North America, South America and New Zealand (Tutin et al. 1976; Brouillet, 2006; Zangenehgheshlaghi et al . 2012; Smith et al. 2013; Al-Snafi, 2015). This herbal medicine is also well-known as an ornamental plant (Ramezanzadeh et al. 2014; Ianovici, 2015). Selected strains are cultivated for decoration (Davis, 1995). Its flowers and young leaves are edible as a salad (Koca et al. 2015). The main constituents of this plant, several triterpenoid saponins (Hiller et al. 1988; Schöpke et al. 1991), anthocyanins (Toki et al. 1991), flavonoids (Gudej & Nazaruk, 2001), polyacetylenes (Avato et al. 1997), tannins (Hegi, 1979), essential oil (Tava, 1996) and phenolic acids (e.g., caffeic, ferulic, sinapic, p-coumaric, and salicylic acids) (Grabias et al. 1995) have been isolated from the roots and flowers. The whole flowering plant of B. perennis has been used for bruises, bleeding, muscular pain, purulent skin diseases, and rheumatism in traditional medicine (Morikawa et al. 2011). B. perennis has been used as a diuretic, antispasmodic, anti-inflammatory, astringent, expectorant, antipyretic, vulnerary, ophthalmic and homeostatic (Grieve, 1982; Bown,1995; Baytop, 1999; Duke et al. 2002). The methanolic extract and its saponin constituents were found to show inhibitory effects on plasma triglyceride elevation in olive oil-loaded mice (Morikawa et al. 2008) and pancreatic lipase inhibitory activity (Morikawa et al. 2009). Antibacterial, antifungal, antioxidant (Desevedavy et al. 1989; Kavalcioglu et al . 2010a), postpartum antihemorrhagic (Oberbaum et al. 2005), and cytotoxic activities against HL-60 human promyelocytic leukemia cells (Li et al. 2005) of B. perennis have also been shown. The methanol extract of B. perennis flowers has antiproliferative effect both on human breast cancer (MCF-7) and human hepatocellular carcinoma (HepG2/C3A) cancer cells (Karakaș et al . 2015). B. perennis may produce biphasic or bipolar effects on learning performance (Karakaș et al. 2011). Traditional usage of wound healing activity of B. perennis was scientifically verified (Karakaș et al . 2012).

CIOBANU: Bellis perennis - variations of physiological responses in urban conditions

Physiological and growth responses of B. perennis to temperature (Gunn & Farrar, 1999), UV-A and UV-B irradiances (Cooley et al . 2000a, Cooley et al. 2000b) have been described. Ultraviolet light influences dry weight of flowers, leaves, and roots, leaf area, photosynthetic parameters, and transpiration rate depending on wavelength and intensity of radiation, and temperature affects plant total dry mass, leaf area, and root respiration. The flowering heads are nyctinastic, closing from dusk to possibly mid-morning on a daily basis (Faur & Ianovici, 2004). Scognamiglio et al. (2012) study evidenced a potential allelopathic role of caffeic acid derivatives from B. perennis based on inhibitory or stimulatory effects on wild coexisting species growth. Contents of phenolics and flavonoids as well as radical scavenging activity of daisy flowers vary to a relatively small extent during the year and are not dependant on the time of collection (Siatka & Kašparová, 2010). On the basis of Kavalcioglu et al . (2010b) results it is clear that there are significant variations in the field collected populations of B. perennis from different geographic and climatic locations. Street plants are exposed to a relatively high stress level, including high pollutant concentrations (Jim, 1998; Ianovici, 2007; Berlizov et al, 2007; Ianovici et al. 2009; Day et al. 2010; Harris & Manning, 2010; Ianovici et al. 2012; Demuzere et al. 2014; Ianovici et al. 2015a; Calfapietra et al. 2015; Ianovici & Latiș, 2016). The goal of this work was to analyze the physiological parameters of B. perennis during the flowering stage and possible adaptations (Ianovici et al. 2011; Ianovici et al. 2015b) to environmental conditions.

MATERIALS AND METHODS In the present study, B. perennis were sampled from park (background site -BS) and a nearby street (traffic site - TS) in the urban area of Timisoara and in different time periods, i.e. April and July. All plants of B. perennis were cut during spring (late April) and summer (mid- July). Plant materials were collected in flowering stage. Rosette populations grow logistically, probably regulated by change in birth rate. The plants remain winter green and continue to grow (Schmid & Harper, 1985; Grime et al. 1988). The species has a very long flowering season, with flowers being produced mainly from about March to November (Mitich, 1997). B. perennis is often common in grasslands and they are generally in shady habitats. This plant prefers a pH of 7.0 to 8.0. At each harvest, plants were separated into roots, scapes, leaves and inflorescences. All samples were individually weighed fresh in the laboratory (FW in g), then oven-dried and re-weighed to estimate their biomasses (DW in g). All plant parts were incinerated at 500°C for 2 hours before recording the ash weights at analytical balance (AC in g). Organic matter (OC in g) is left when the ash content subtract from dry matter (Grudnicki & Ianovici, 2014). List of non-standard abbreviations of physiological parameters calculated: IWC (%) - initial water content; MC (%) - mineral content; OC (%) - organic content; OC/MC ratio - organic content/ mineral content ratio; LRWC (%) - leaf relative water content; TD (g/kg) - tissues density; TDM (g/kg dry wt) - tissues mineral deposition. At the level of leaves we determined the other two parameters: leaf relative water content (LRWC in %) and specific leaf area (SLA in cm -2/g -1) (Cornelissen et al. 2003; Ianovici, 2011a; Ianovici, 2011b; Ianovici, 2016). Statistical analyses were performed with the software SPSS. Probability ( p) values less than 0.05 were considered significant. The data had a normal distribution. Variance between atmospheric fungal spores distributions was analyzed by one-way ANOVA between groups,

Annals of West University of Timişoara, ser. Biology, 2016, vol. 19 (1), pp.77-86

Levene 's test for homogeneity of variance (based on means) and Welch F test in the case of unequal variances. Analysis of significant differences between AFS was followed by Tukey HSD (honest significant difference) post-hoc test (Oehlert, 2010; Ianovici et al. 2013).

RESULTS AND DISCUSSIONS The analyzed physiological parameters of leaves are reported in Table 1. Regarding the leaves, the data were homogeneous for the following parameters: FW, DW, AC, OC, SLA, TD, LOC/LMC ratio, IWC and OC in %. Analysis of variance revealed that the data are significantly different for SLA, LOC/LMC ratio and OC in % fresh wt. When the data were heterogeneous, we applied Welch F test. In this case, the F was significantly different for TMD and MC in % fresh wt. Fresh leaf weight ranged between 0.0611g and 0.1120g, and dry weight between 0.0065g and 0.0111g. Organic content of samples in the summer increased compared with the spring samples. Both LRWC and IWC values were slightly lower in summer. Tukey’s pairwise comparisons for LOC/LMC ratio indicated significant differences for the following samples: spring/BS – summer/BS, spring/TS – summer/BS, summer/BS – summer/TS. The study of variations of SLA indicated significant differences but Tukey’s pairwise comparisons indicated no significant differences for the samples. However, the SLA values are higher in summer (489.6525 cm -2/g -1in background site and 441.4667 cm -2/g -1in traffic site). The results for TMD and MC fell in summer. TMD and MC values in traffic sites are greater than the background sites, in both seasons. For scapes, data were homogeneous for the following parameters: FW, TD, LOC/LMC ratio, IWC, MC in % fresh wt and OC in % (table 2). Analysis of variance revealed that the data are significantly different for FW, LOC/LMC ratio, MC in % fresh wt and OC in % fresh wt. Welch T test did not show significantly different values for the other parameters. Fresh and dry weight of scapes in summer was lower than in spring. Tukey’s pairwise comparisons for FW indicated significant differences for the following samples: spring/BS – spring/TS (p=0.02817), spring/BS - summer/BS (p=0.001224), spring/BS – summer/TS (p=0.00365). Between samples from background sites we identified significant differences for TD (p=0.03699), IWC (p=0.03699) and OC% (p=0.03861). Results for the TD and OC in % were higher in summer. IWC values fell in the summer. TMD and MC values in summer/TS are significantly higher than all other types of samples. Levene's test indicated that all parameters for inflorescences were homogeneous (table 3). Analysis of variance revealed that the data are significantly different for FW, AC and OC / MC ratio. The inflorescences were heavier the spring / BS (0.157933g). The Tukey's pairwise comparisons for FW indicated significant differences for samples: spring / BS - spring / TS (p=0.0179), spring / BS - summer / BS (p=0.01885), spring / BS - summer / TS (p=0.02215). The same differences we recorded for AC. Values OC/MC ratio are higher in the summer. IWC and TMD values decreased in summer. For roots, Levene's test showed that the values of most parameters were heterogeneous (table 4). Welch F test showed that the data are significantly different for TD and IWC. Analysis of variance revealed that the data are significantly different for OC in % fresh wt. Fresh and dry root weight was higher in the spring. Tukey’s pairwise comparisons for FW indicated the significant differences for the following samples: spring/BS – summer/TS (p=0.02701), spring/BS – summer/BS (p=0.01682). The same significant differences were 79

CIOBANU: Bellis perennis - variations of physiological responses in urban conditions

found for DW and OC in g. Tukey’s pairwise comparisons for TD, IWC and OC in % indicated significant differences for the following samples: spring/BS – spring/TS, spring/TS – summer/BS, spring/TS – summer/TS. TD and OC% values increased in summer and IWC values fell. OC / MC ratio was the highest in summer, in traffic site.

TABLE 1. Analysis of differences of leaves between the background site (BS ) and the traffic site (TS) (with significant p-values indicated in bold) Levene's One-way Welch F test Spring-BS Spring-TS Summer-BS Summer-TS test ANOVA FW- in Min 0,0239 0,0104 0,017 0,0125 F=1,5660 - g Max 0,2798 0,1483 0,174 0,1462 0,168 p=0,2092 Mean 0,1120 0,0611 0,0824 0,0795 DW- in Min 0,0022 0,0014 0,002 0,0017 F=1,849 - g Max 0,0235 0,016 0,027 0,0182 0,1405 p=0,1503 Mean 0,0111 0,0065 0,0107 0,0097 AC in g Min 0,0003 0,0001 0 0,0002 F=1,525 - Max 0,0049 0,004 0,002 0,0043 0,7115 p=0,2195 Mean 0,0019 0,0014 0,0009 0,0018 OC in g Min 0,0019 0,0011 0,002 0,0015 F=2,557 - Max 0,0186 0,0133 0,025 0,0166 0,0630 p=0,06563 Mean 0,0092 0,0050 0,0098 0,0079 LRWC Min 49,6316 59,2593 78,332 82,7027 F=1,294, -in % Max 99,3915 97,8221 91 95,0586 0,0070 - df=16,18, Mean 87,278 89,9676 85,581 86,5894 p=0,3103 SLA Min 286,65 230,3 369,41 289,8 F=3,506 - Max 334,51 398,63 558,22 570,9 0,2392 p=0,0464 Mean 316,08 339,9475 489,6525 441,4667 TD-in Min 83,9886 48,9181 105,651 83,8323 F=1,975 - g/kg Max 121,3389 204,8193 165,054 161,194 0,1207 p=0,1297 fresh wt Mean 104,2583 115,5338 134,8993 123,1302 OC/MC Min 3,7959 1,2857 4,75 2,8182 F=7,435 - ratio Max 8,6667 17 12,382 10,4894 0,1352 p=0,0003 Mean 5,7977 4,7789 10,3286 5,6036 TMD in Min 103,4483 55,5555 74,7252 87,0370 F=14,24, g/kg Max 208,5106 437,5 173,913 261,9048 df=20,84, dry wt Mean 155,4373 233,515 93,1520 178,4912 0,0002 - p=2,837E-05 IWC- in Min 87,8661 79,5180 83,4945 83,8806 F=1,975 % Max 91,6011 95,1081 89,4348 91,6167 0,1207 p=0,1297 Mean 89,5741 88,4466 86,5100 87,6869 - MC in Min 1,1538 0,5758 0,8517 1,1428 F=8,202, % fresh Max 2,0091 8,0321 2,2598 2,9737 0,0005 df=23,41, wt Mean 1,5910 2,6964 1,2546 2,1164 - p=0,0006 OC in Min 6,6476 3,0103 9,7133 6,1876 F=5,195 % fresh Max 10,8786 14,4508 15,2720 14,7164 0,3673 p=0,0033 wt Mean 8,8348 8,8569 12,2353 10,1965 -

Annals of West University of Timişoara, ser. Biology, 2016, vol. 19 (1), pp.77-86

TABLE 2. Analysis of differences of scapes between the background site (BS ) and the traff ic site (TS) (with significant p - values indicated in bold) Spring- Levene's One-way Welch F BS Spring-TS Summer-BS Summer-TS test ANOVA test FW- in g Min 0,1653 0,1139 0,0308 0,0638 F=7,832 - Max 0,2998 0,1583 0,1745 0,1496 0,124 p=0,0026 Mean 0,2425 0,1410 0,0863 0,1065 DW- in g Min 0,0188 0,0137 0,0039 0,0081 F=1,759, Max 0,0326 0,0209 0,0277 0,0215 0,0497 df=5,564, Mean 0,0267 0,0173 0,0162 0,0151 - p=0,261 AC in g Min 0,0017 0,0008 0,0002 0,0007 F=2,306, Max 0,0028 0,0022 0,0025 0,0056 0,0434 df=6,822, Mean 0,0023 0,0014 0,0014 0,0030 - p=0,1656 OC in g Min 0,0171 0,0129 0,0036 0,0074 F=3,222, Max 0,0298 0,0187 0,0251 0,0164 0,0219 df=5,544, Mean 0,0243 0,0158 0,0147 0,0120 - p=0,1104 TD-in g/kg Min 108,7392 94,8753 126,6234 126,9592 F=3,25 - fresh wt Max 113,7326 156,2774 287,7095 186,0465 0,0540 p=0,0539 Mean 110,5878 124,3097 189,3207 144,3306 Min 10,0384 7,9444 9,8203 2,2857 F=6,295 - OC/MC ratio Max 10,6428 17 12,9285 10,5714 0,0588 p=0,0063 ratio Mean 10,2467 12,4523 10,7638 5,1973 Min 85,8895 55,5555 71,7948 86,4197 F=3,144, TMD in g/kg Max 90,5923 111,8012 92,4187 304,3478 0,0247 df=6,914, dry wt Mean 88,9691 80,8095 85,9139 188,8588 - p=0,0968 Min 88,6267 84,3722 71,2290 81,3953 F=3,25 IWC- in % Max 89,1260 90,5124 87,3376 87,3040 0,0540 p=0,0539 Mean 88,9412 87,5690 81,0679 85,5669 - Min 0,9339 0,5540 0,9090 1,0971 F=6,806 MC in % Max 1,0284 1,3897 2,5139 3,9051 0,0835 p=0,0046 fresh wt Mean 0,9841 0,9990 1,6465 2,7104 - Min 9,9390 8,9335 11,7532 8,9260 F=3,349 OC in % Max 10,3448 14,4863 26,2569 15,5038 0,0598 p=0,0497 fresh wt Mean 10,0746 11,4319 17,2855 11,7226 -

CONCLUSIONS OC% is significantly different in the leaves, scapes and roots. In all cases, the samples had elevated summer for OC%. This parameter indicates a significant accumulation in roots and inflorescences. MC in% is significantly different in the leaves and scapes. The results showed that the leaves and inflorescences have lower percentages of the minerals in the summer but it is important that the percentage from TS is greater than the percentage from BS. TMD is significantly different in the leaves.This parameter has been greatly increased in TS. We also saw a marked increase for TDM of scapes in summer / TS. Values fell in summer for inflorescences and roots. IWC is significantly different in the roots. For all organs, IWC has declined during the summer but the downturn is more pronounced for roots, especially in TS. OC / MC ratio differs significantly for leaves, scapes and inflorescences. In summer, the increase in this parameter is marked for inflorescences. 81

CIOBANU: Bellis perennis - variations of physiological responses in urban conditions

TD was significantly different in the case of the roots. This parameter has the highest values for the roots. Values increased in summer, especially in TS.

TABLE 3. Analysis of differences of inflorescences between the background site (BS ) and the traffic site (TS) (with significant p-values indicated in bold) Levene's One-way Welch F Spring-BS Spring-TS Summer-BS Summer-TS test ANOVA test FW- in g Min 0,1217 0,0283 0,0398 0,061 F=4,619 - Max 0,2198 0,1277 0,0941 0,1028 0,1394 p=0,0190 Mean 0,1579 0,0759 0,0765 0,0785 DW- in g Min 0,0197 0,004 0,0067 0,0096 F=2,893 - Max 0,0337 0,021 0,0173 0,0258 0,7688 p=0,07263 Mean 0,0247 0,0121 0,0136 0,0163 AC in g Min 0,002 0,0005 0,0005 0,0009 F=4,986 - Max 0,0035 0,0022 0,0016 0,0022 0,8949 p=0,0147 Mean 0,0027 0,0015 0,0012 0,0014 OC in g Min 0,0169 0,0035 0,0061 0,0087 F=2,739 - Max 0,0302 0,0188 0,0156 0,0236 0,7572 p=0,0828 Mean 0,0219 0,0106 0,0123 0,0148 TD-in g/kg Min 153,3212 123,9024 168,3417 157,377 F=2,099 - fresh wt Max 161,8735 213,5417 184,9315 283,8284 0,1425 p=0,1463 Mean 157,471 160,7617 176,4878 205,5527 Min 6,0357 2,9285 9,3592 9 F=5,855 - OC/MC Max 9,4 8,5454 10,9642 11,4615 0,4329 p=0,0082 ratio Mean 8,0214 6,9575 10,2280 10,2244 Min 96,1538 104,7619 83,5820 80,2469 F=2,193 TMD in Max 142,132 254,5455 96,5317 100 0,1019 p=0,1343 g/kg dry wt Mean 114,0478 137,9343 89,2991 89,6051 - Min 83,8126 78,6458 81,5068 71,6171 F=2,099 IWC- in % Max 84,6678 87,6097 83,1658 84,2623 0,1425 p=0,1463 Mean 84,2529 83,9238 82,3512 79,4447 - Min 1,5117 1,3658 1,4070 1,4591 F=0,7881 MC in % Max 2,3007 4,2296 1,7747 2,4202 0,08403 p=0,5203 fresh wt Mean 1,8016 2,2355 1,5783 1,8310 - Min 13,7397 11,0243 15,3837 14,2623 F=2,822 OC in % Max 14,2101 18,75 16,8607 25,9626 0,1178 p=0,0771 fresh wt Mean 13,9455 13,8406 16,0703 18,7242 -

Annals of West University of Timişoara, ser. Biology, 2016, vol. 19 (1), pp.77-86

TABLE 4. Analysis of differences of roots between the background site (BS ) and the traffic site (TS) (with significant p -val ues indicated in bold) Levene's test One-way Welch F Spring-BS Spring-TS Summer-BS Summer-TS ANOVA test FW- in g Min 0,6949 0,3244 0,0528 0,076 F=3,337, Max 1,9989 1,931 0,3127 0,405 0,0228 df=5,102, Mean 1,2392 0,9364 0,1376 0,2188 - p=0,1118 DW- in g Min 0,178 0,0468 0,0134 0,022 F=2,282, Max 0,5011 0,374 0,1065 0,136 0,0231 df=5,144, Mean 0,3100 0,1472 0,0423 0,0715 - p=0,1937 AC in g Min 0,0111 0,0018 0,0012 0,002 F=1,172, Max 0,0821 0,0355 0,0099 0,01 0,0003 df=4,908, Mean 0,0373 0,0152 0,0038 0,0055 - p=0,409 OC in g Min 0,1669 0,0449 0,0121 0,0197 F=2,725, Max 0,419 0,3385 0,0966 0,1279 0,0373 df=5,199, Mean 0,2727 0,1319 0,0384 0,0660 - p=0,1502 TD-in g/kg Min 245,1411 51,6271 253,7879 290,066 F=20,47, fresh wt Max 256,152 201,603 340,582 341,056 0,0396 df=6,16, Mean 250,6603 155,7071 281,8277 320,3747 - p=0,0013 Min 5,1035 5,3495 9,3875 8,9545 F=0,6284, LOC/LMC Max 15,0360 23,8936 10,4285 16,3974 0,03 df=4,947, ratio Mean 10,8540 11,3464 9,9808 11,8876 - p=0,6276 TMD in Min 62,3595 40,1709 87,5 57,4797 F=0,5491, g/kg dry Max 163,8396 157,4924 96,2686 100,4566 0,0074 df=4,998, wt Mean 100,2337 106,0085 91,2090 81,2292 - p=0,6703 Min 74,3848 79,8397 65,9418 65,8944 F=20,47, IWC- in % Max 75,4858 94,8372 74,6212 70,9933 0,0396 df=6,16, Mean 74,9339 84,4292 71,8172 67,9625 - p=0,0013 Min 1,5973 0,2073 2,2932 1,9264 F=0,596 MC in % Max 4,1072 3,1750 3,1659 3,2993 0,1076 p=0,6288 fresh wt Mean 2,5103 1,8833 2,5722 2,5861 - Min 20,9615 4,9553 22,9356 26,0927 F=15,6 OC in % Max 24,0178 17,5297 30,8922 31,7349 0,1341 p=0,0001 fresh wt Mean 22,5557 13,6873 25,6105 29,4513 -

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CIOBANU: Bellis perennis - variations of physiological responses in urban conditions

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