Volatile chemical composition does not support a native status of the cryptogenic Bupleurum fruticosum (Apiaceae) in peninsular Italy

Biochemical Systematics and Ecology 88 (2020) 103966

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Volatile chemical composition does not support a native status of the cryptogenic Bupleurum fruticosum (Apiaceae) in peninsular Italy

T

Francesco Roma-Marzioa,∗, Basma Najarb, Valeria Nardib, Luisa Pistellib, Lorenzo Peruzzic a

Sistema Museale di Ateneo, Orto e Museo Botanico, University of Pisa, Via L. Ghini 13, 56126, Pisa, Italy Department of Pharmacy, University of Pisa, Via Bonanno 33, 56126, Pisa, Italy c Department of Biology, University of Pisa, Via Derna 1, 56126, Pisa, Italy b

ARTICLE INFO

ABSTRACT

Keywords: Alien species Cryptogenic species Essential oil composition Italian flora Tuscany

Cryptogenic (or doubtfully native) species could have relevant implications in biogeography and in nature conservation. Bupleurum fruticosum is native in Sicily, Sardinia, and Liguria, whereas the single Tuscan population is considered cryptogenic. Given its pharmacological activity, several studies investigated the essential oil composition of this species, but an analysis of geographic pattern of the chemical composition was never performed. In the present study, the essential oil composition of the Tuscan population was investigated for the first time, and a comparison with other populations from literature was performed in order to provide useful data to disentangle its cryptogenic status. Our results highlight a major similarity of plants from Tuscany with geographically distant populations from Portugal and France, whereas other Italian populations show a very different chemical composition. These results do not support a native status of Tuscan population, suggesting an ancient human introduction. Our analysis also revealed a high percentage of (Z)-β-ocimene in stems of plants from Tuscany.

1. Introduction In biogeography species are commonly categorised as native or alien. Native species evolved in the considered area or arrived there before the Neolithic, or independently of human activity; on the contrary, alien species reached the considered area as a direct or indirect consequence of human activities (Pyšek, 1998). Due to the historical anthropogenic global movement of plants and animals, there are many species which cannot reliably be assigned to these categories (Carlton, 1996). For these species, Carlton (1996) introduced the term “cryptogenic”, to apply to those species that are neither demonstrably native nor alien. Disentangling the cryptogenic status of a species could have interesting implications in biogeography as well as in nature conservation. The actual number of invasive species and their impacts may be underestimated because of the presence of cryptic invaders (Saltonstall, 2002) and, on the contrary, a truly native species may not be properly considered as worthy of conservation if categorised as cryptogenic. Phytochemical composition provides comparative data for understanding relationships among taxa at different taxonomic ranks, as well as to detect patterns of hybridization or geographical variation among populations (Bohm, 2009; Stuessy, 2009). Essential oil (EO)

∗

composition, and particularly monoterpenoid content, have proved to be particularly useful at the lower levels of the taxonomic hierarchy and to highlight geographic pattern among populations (Tundis et al., 2016; Passalacqua et al., 2017; Roma-Marzio et al., 2017; Peruzzi et al., 2019), being potentially useful to disentangle cases of cryptogenic species. Among the 139 cryptogenic species reported for Italy at either national or regional level (Bartolucci et al., 2018a; 2018b; Galasso et al., 2018), there is Bupleurum fruticosum L. (Apiaceae). It is a steno-Mediterranean perennial shrub, occurring from Morocco to Greece and reported as non-native in Great Britain, Germany, Ukraine, and Crimea (Hand, 2011). In Italy, this species is native to Sicily, Sardinia, and Liguria (a single population on Island of Gallinara), whereas it is considered cryptogenic in peninsular Italy (Bartolucci et al., 2018b; RomaMarzio and Peruzzi, 2018), including Tuscany. In this region, this plant is well integrated in the local maquis shrubland vegetation, but the plants are more or less close to old mansions and parks (Negri, 1946). From a phytochemical point of view, B. fruticosum was investigated by many authors, mainly for its pharmacological anti-inflammatory, antibacterial, antifungal, hepatoprotective activities, and for its effect on the reduction of uterine contractions induced by oxytocin and

Corresponding author. E-mail address: [email protected] (F. Roma-Marzio).

https://doi.org/10.1016/j.bse.2019.103966 Received 10 October 2019; Received in revised form 12 November 2019; Accepted 14 November 2019 0305-1978/ © 2019 Elsevier Ltd. All rights reserved.

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Table 1 Plant structure and sampling periods of Tuscan population and of other data available in literature. ID Sample

Country

Locality

Analysed parts

Collection period

Source of data

Tls Tsds Tsts Tlw Tsdw Tstw SAR1 SAR2 SAR3 SIC COR FRA CYR POR1 POR2 ALGl ALGs ALGf SPA

Italy Italy Italy Italy Italy Italy Italy Italy Italy Italy France France Libya Portugal Portugal Algeria Algeria Algeria Spain

Candeli (Tuscany) Candeli (Tuscany) Candeli (Tuscany) Candeli (Tuscany) Candeli (Tuscany) Candeli (Tuscany) Baunei (Sardinia) Baunei (Sardinia) Baunei (Sardinia) Messina (Sicily) Corte (Corse) Villeneuve-les-Corbières Ras-el-Hylal Cerca de Santa Comba Cerca de Santa Comba Yama Gouraya Yama Gouraya Yama Gouraya Sierra Cogollos

Leaves Seeds Stems Leaves Seeds Stems Leaves Leaves + flowers Leaves + fruits Leaves Aerial parts Fruits Aerial parts Leaves + flowers Leaves + fruits Leaves Stems Fruits Fruits

July July July February February February Not specified Not specified Not specified April September August April Not specified Not specified Not specified Not specified Not specified September

Present study Present study Present study Present study Present study Present study Maxia et al. (2011) Maxia et al. (2011) Maxia et al. (2011) Dugo et al. (2000) Liu et al. (2009) Chizzola (2008) Giampieri et al. (1998) Maxia et al. (2011) Maxia et al. (2011) Mékaoui et al. (2019) Mékaoui et al. (2019) Mékaoui et al. (2019) Lorente et al. (1989)

percent values of all compounds (Supplemental material S1). A default percentage of 0.01% was assigned to those compounds detected in traces. To evaluate relationships among populations, this matrix was directly subjected to Principal Component Analysis (PCA). All the statistical analyses were carried out by means of the PAST version 3.26 (Hammer et al., 2001; Hammer, 2019).

acetylcholine (Lorente et al., 1989; Guinea et al., 1994; Ashour and Wink, 2011; Maxia et al., 2011). For these medicinal properties, roots and stems of this species are also used in Sardinian folk medicine as an antirheumatic remedy (Ballero and Fresu, 1991; Pistelli et al., 1996). Aim of the present study is to characterize the essential oil composition (EO) of the Tuscan population of B. fruticosum and to compare its profile with data available in literature for other populations, in order to provide new data in support of the native or alien status of this species in peninsular Italy.

3. Results One hundred fifteen compounds have been identified (Table 2), representing 99.3%–100% of the total oil composition. The monoterpene hydrocarbons, with a percentage ranging between 83.8% and 97.02%, are the main class of constituents of terpene profiles in all sampled plants. The oxygenated monoterpenes are particularly high in stems and seeds from plants collected in summer (9.4% and 8.4% respectively), whereas the percentage of sesquiterpene hydrocarbons are very low only in seeds, irrespective of the sampling period (0.6% in summer and 0.7% in winter). A very low percentage of phenylpropanoid is found only in leaves and stems collected in summer (traces and 0.3%, respectively). In all the accessions, α-pinene and β-pinene are the two most abundant compounds with a percentage ranging from 41.38% (αpinene in summer leaves) to 22% (β-pinene in winter stems). Only in summer stems, the two most abundant compounds are β-phellandrene (19.31%) and (Z)-β-ocimene (19.23%). The latter compound is in high concentration (> 10%) only in stems collected both in summer (19.23%) and in winter (13.5%). Eleven compounds are found in all sampled structures and periods (α-pinene, β-pinene, β-phellandrene, p-cymene, sabinene, γ-terpinene, myrcene, α-thujene, camphene, β-elemene, β-caryophyllene), whereas many other compounds are identified only in one portion of the plant collected in a specific period. According to PCA results (Fig. 1; 96.1% of variance explained by the first three axes), all the accessions from Sardinia and Corsica are clearly separated from others. Similarly, also the populations from Cyrenaica (Libya) and fruits collected from Algeria are distinct, whereas no clear phytochemical separation is evident among all the accessions from Tuscany, France, Portugal, Spain, and leaves and stems from Algeria. The five compounds which contribute more than 25% to the observed variation pattern are: (Z)-β-ocimene (74% of explained variance on axis 3), limonene (65% of explained variance on axis 2), β-pinene (44% of explained variance on axis 1), α-pinene (43% of explained variance on axis 1) and β-phellandrene (26% of explained variance on axis 3) (Fig. 2).

2. Material & methods Leaves, stems and seeds were collected in summer 2018 and in winter 2019 from the only Tuscan population of B. fruticosum (coordinates WGS84: 43.764080 N, 11.348720 E). A herbarium voucher was prepared and deposited at PI (acronym follows Thiers, 2019), accession no. 011168 and is available at: https://herbarium.univie.ac.at/ database/detail.php?ID=1391580. For each structure and sampling period, EOs were analysed separately. All the EOs were obtained by hydrodistillation from dried aerial parts, using a Clevenger-type apparatus according to the Italian Pharmacopoeia (AOAC, 1990). The GC/MS analyses were performed with an Agilent 7890B gas chromatograph (Agilent Technologies Inc., Santa Clara, CA, USA) equipped with an Agilent HP-5MS (Agilent Technologies Inc., Santa Clara, CA, USA) capillary column (30 m × 0.25 mm; coating thickness 0.25 μm) and an Agilent 5977B single quadrupole mass detector (Agilent Technologies Inc., Santa Clara, CA, USA). Analytical conditions were as follows: injector and transfer line temperatures 220 °C and 240 °C, respectively; oven temperature programmed from (60–240) °C at 3 °C/min; carrier gas helium at 1 ml/min; injection of 1 μl (0.5% HPLC grade n-hexane solution); split ratio 1:25. The acquisition parameters were as follows: full scan; scan range: 30–300 m/z; scan time: 1.0 s. Identification of the constituents was based on a comparison of the retention times with those of the authentic samples, comparing their linear retention indices relative to the series of n-hydrocarbons. Computer matching was also used against commercial (NIST 14 and ADAMS 07) and laboratory-developed mass spectra library built up from pure substances and components of known oils and MS literature data (Adams, 1995; Davies, 1990; Jennings and Shibamoto, 1982; Masada, 1976; Stenhagen et al., 1974; Swigar and Silverstein, 1981). According to Roma-Marzio et al. (2017) and Peruzzi et al. (2019), data from the EO composition of collected plants, integrated with data available in literature from other accessions of B. fruticosum (Table 1), were used to build a matrix with mean 2

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Table 2 Comparison of the chemical composition (relative %) of the Tuscan population of Bupleurum fruticosum. Tlw: leaves collected in winter, Tsdw: seeds collected in winter, Tstw: stems collected in winter, Tls: leaves collected in summer, Tsds: seeds collected in summer, Tsts: stems collected in summer; mh: monoterpene hydrocarbons, om: oxygenated monoterpenes, sh: sesquiterpene hydrocarbons, os: oxygenated sesquiterpenes, nt: non-terpene derivatives, pp: phenylpropanoid. LRI = Linear retention index on the HP-5MS column, LRI* = Linear retention index from NIST (° = value from Adams, 2007; AOAC, 1990), vl: very low yield. Compound

Class

LRI

LRI*

Tlw

Tsdw

Tstw

Tls

Tsds

Tsts

tricyclene α-thujene α-pinene camphene thuja-2,4(10)-diene verbenene sabinene β-pinene myrcene pseudolimonene isoamyl 2-methyl butyrate α-phellandrene α-terpinene p-cymene limonene β-phellandrene δ-3-carene (Z)-β-ocimene (E)-β-ocimene γ-terpinene cis-sabinene hydrate terpinolene 6-camphenone trans-sabinene hydrate 3-methylbutyl 2-methylbutanoate methylbutyl 2-methylbutanoate isoamyl 2 methylbutyrate isopentyl isovalerate pentyl isovalerate β-thujone trans-pinene hydrate trans-p-mentha-2,8-dien-1-ol cis-p-menth-2-en-1-ol exo-fenchol α-campholenal allo-ocimene cis-p-mentha-2,8-dien-1-ol trans-pinocarveol cis-verbenol trans-sabinol trans-p-menth-2-en-1-ol trans-pinocamphone pinocarvone borneol cis-pinocamphone 4-terpineol isopinocampheol cryptone α-terpineol myrtenal myrtenol verbenone trans-carveol cis-p-mentha-1(7),8-dien-2-ol hexyl 2-methylbutyrate cumin aldehyde hexyl isovalerate methyl ether-carvacrol p-menth-1-en-7-al isobornyl acetate bornyl acetate trans-verbenyl acetate trans-pinocarvyl acetate carvacrol

mh mh mh mh mh mh mh mh mh mh nt mh mh mh mh mh mh mh mh mh om mh om om nt nt nt nt nt om om om om om om om om om om om om om om om om om om nt om om om om om om nt om nt pp om om om om om om

922 926 933 948 954 968 973 977 991 1004 1105 1006 1017 1025 1029 1030 1031 1036 1047 1058 1068 1088 1097 1098 1101 1102 1103 1106 1109 1117 1119 1120 1122 1122 1126 1132 1134 1139 1141 1142 1145 1160 1163 1165 1173 1177 1180 1186 1191 1196 1197 1210 1218 1231 1238 1239 1244 1245 1276 1286 1289 1293 1298 1302

927 930 939 954 960 968 975 979 991 1002 1100 1003 1017 1025 1029 1030 1026 1037 1050 1060 1070 1089 1097 1098 1100 1100° 1102 1103 1111 1114 1124 1123 1122 1114 1126 1131 1138 1139 1143 1140 1140 1163 1165 1169 1175 1177 1178 1186 1189 1196 1191 1205 1217 1231 1236 1242 1244 1244 1276° 1290 1289 1292 1297 1299

tr 1.3 35.6 0.5 – – 2.2 35.1 1.0 – – 0.2 tr 0.2 tr 11.2 tr 3.9 0.1 0.8 tr 0.1 – tr – – – – – – – – tr – – – – tr tr – – – – – – 0.2 – – 0.1 – – – – – – – – tr – – 0.1 – – –

tr 0.9 30.7 0.5 tr – 2.8 39.9 0.8 tr – – tr 1.1 tr 8.9 tr tr tr 0.8 0.2 tr 0.2 tr – – 0.6 2.0 1.4 – tr tr – – 1.0 – – 1.3 0.7 tr – tr 1.4 – 0.4 0.3 0.2 – tr 1.7 – tr – – tr – tr – – tr 0.4 tr 0.2 0.1

tr 0.9 22.2 0.5 – tr 2.1 22.0 1.1 – – 0.5 0.1 2.9 tr 15.4 tr 13.5 0.7 1.7 tr 0.2 – tr – – 0.3 0.3 – tr – 0.2 – tr 0.2 0.1 tr 2.6 0.9 – – tr 0.4 tr 0.4 0.8 – 0.7 0.6 tr 2.4 0.3 0.1 0.1 tr tr – 0.3 tr – 0.3 – tr –

– 1.2 41.4 0.5 – – 2.1 37.5 1.1 – – 0.1 – 0.2 – 7.9 – 2.4 0.5 0.5 – 0.2 – – – – – – – – – – – – – – – – – – – – – – – 0.2 – – 0.1 – – – – – – – – – – 0.1 – – – –

– 1.0 33.6 0.5 – – 2.9 35.4 1.1 – – 0.4 – 0.8 – 20.6 – – – 0.8 – – – – 0.9 0.3 – 0.8 – – – – – – – – – – – 0.1 – – – – 0.1 – – – – – – – – – – – – – – 0.1 – – – –

– 0.7 15.9 0.3 – – 2.2 18.4 1.4 – 0.8 0.7 0.2 1.2 – 19.3 0.1 19.2 3.4 3.0 0.1 0.2 – – 0.4 – – – – – – – – – – 0.2 – – 0.1 – 0.1 – – – – 0.7 – – 0.3 – – – – – – – – – – 0.2 – – – –

(continued on next page)

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Table 2 (continued) Compound

Class

LRI

LRI*

Tlw

Tsdw

Tstw

Tls

Tsds

Tsts

isoamyl benzyl ether cis-pinocarvyl acetate myrtenyl acetate cis-piperitol acetate δ-elemene neryl acetate cis-carvyl acetate α-ylangene α-copaene β-bourbonene β-cubebene β-elemene α-cedrene β-caryophyllene 2,5-dimethoxy-p-cymene cis-thujopsene 1-octyl 2-methylbutanoate butanoic acid, 2-methyl-, octyl ester isovaleric acid, octyl ester α-humulene 9-epi-(E)-caryophyllene cis-muurola-4(14),5-diene β-acoradiene γ-muurolene germacrene D valencene bicyclogermacrene germacrene A α-bulnesene β-bisabolene β-curcumene δ-cadinene cis-calamenene cis-sesquisabinene hydrate (E)-nerolidol (Z)-isoelemicin γ-asarone germacrene D-4-ol spathulenol caryophyllene oxide humulene epoxide II isovaleric acid, 3-phenylpropyl ester 6-methyl-2-(4-methylcyclohex-3-en-1-yl)hepta-1,5-dien-4-ol caryophylla-4(14),8(15)-dien-5-ol epi-α-cadinol selina-3,11-dien-6-α-ol α-cadinol 14-hydroxy-9-epi-(E)-caryophyllene cinnamyl isovalerate cinnamyl valerate 14-hydroxy-α -humulene 1-octadecene

nt om om om sh om om sh sh sh sh sh sh sh om sh nt nt nt sh sh sh sh sh sh sh sh sh sh sh sh sh sh os os pp pp os os os os nt os os os os os os nt nt os nt

1309 1310 1327 1335 1338 1365 1368 1375 1376 1385 1390 1392 1413 1419 1427 1429 1434 1434 1440 1453 1466 1467 1471 1477 1481 1493 1596 1505 1506 1509 1513 1524 1540 1544 1564 1570 1574 1574 1577 1582 1608 1613 1618 1633 1641 1641 1654 1670 1670 1688 1736 1790

1310 1312 1329 1332 1338 1362 1366 1375° 1377 1388 1388 1391 1412 1419 1423 1431 1427 1427 1440 1455 1466° 1463 1468 1480 1485 1496 1500 1509 1509 1506 1516 1523 1532 1544 1563 1581 1578 1576 1588 1583 1608 1613 1614 1641 1640 1640 1654 1670 1670 1688 1714° 1792

– – tr – – tr – – 0.1 tr tr 0.8 1.0 0.9 – – – – – 0.4 tr tr – – 1.5 – 0.3 1.5 – 0.5 – 0.1 tr – tr – – 0.2 – tr – – – – tr – 0.1 – 0.1 – – –

tr tr 0.3 – tr – tr tr tr – – 0.1 tr 0.1 tr – tr – – tr – – – tr – tr – – 0.1 0.3 – – – – – – – – – 0.2 tr – – tr – 0.1 – tr – 0.2 – –

– – tr tr – tr tr – 0.1 – tr 0.2 0.5 0.2 – – – tr tr 0.1 tr tr tr tr 0.7 – 0.2 0.3 – 1.0 – tr tr tr – tr tr – 0.1 0.3 0.1 – 0.2 0.1 – – tr tr tr 1.4 0.2 tr

– – – – – – – – – – – 0.6 – 0.5 – 0.3 – – – 0.3 – – – – 1.5 – 0.1 0.8 – – – – – – – – – – – – – – – – – – – – – – – –

– – – – – – – – – – – 0.1 – 0.1 – – – – – – – – – – 0.2 – – 0.2 – – – – – – – – – – – – – – – – – – – – – – – –

– – – – – – – – 0.2 – – 0.2 0.6 0.4 – – – – – 0.2 – – – – 1.7 – 0.4 0.7 – 1.3 0.2 – – – – – – – – – – 0.2 – – – – 0.1 – 0.7 3.2 – –

Yield % (w/w)

0,52

0.07

0.26

0.82

vl

vl

Class of compounds

Tlw

Tsdw

Tstw

Tls

Tsds

Tsts

92.2 0.4 7.1 0.3 0.1 tr

86.4 8.4 0.6 0.3 4.2 –

83.8 9.4 3.3 1 2.7 0.3

95.6 0.4 4.0 – – –

97.0 0.3 0.7 – 2.0 –

86.3 1.8 5.8 0.1 5.3 –

100

99.9

100

100

100

99.3

Monoterpene hydrocarbons Oxygenated monoterpens Sesquiterpene hydrocarbons Oxygenated sesquiterpenes Non-terpene derivatives Phenylpropanoid

mh om sh os nt pp

Total identified

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below 2% (Liu et al., 2009; Maxia et al., 2011). In the phytochemical and plant systematic literature, there are many examples of chemotypes related with geographical distribution (Viljoen et al., 1995; Binns et al., 2002; Christensen et al., 2014). This variation could partially reflect different environmental conditions, but genetic differences may be also involved (Figueiredo et al., 2008), so that they represent a useful tool to disentangle cases of cryptogenic species. Our results suggest a possible human introduction of B. fruticosum in Tuscany, followed by a spontaneous naturalization. The native status of Bupleurum fruticosum in Tuscany is also not supported by its regional distribution: literature data (Baroni, 1897–1908; Montelucci, 1933; Negri, 1946) and herbarium specimens housed in FI and PI highlight that, with the exception of the sampled population considered as cryptogenic (Bartolucci et al., 2018b), all other available data refer to cultivated plants. Furthermore, since B. fruticosum is a pioneer species that rapidly occupies the first successional stages (Marcenò et al., 2011), the presence of plants almost limited in an area subject to woodcuts (Bartolucci et al., 2018b), could support the hypothesis of a naturalization that could benefit of human activities. Other cases of rare plant species, found in small and isolated populations, are documented as introduced populations that became locally naturalized, hence resembling native populations (Decocq, 2019). The essential oil of the different plant structures collected in two different periods, although containing almost the same compounds, shows some quantitative differences, particularly in (Z)-β-ocimene and other major compounds. These seasonal and anatomical differences fall within the intra-individual variation of an individual, and are documented in many other species (Flamini et al., 1999; Novak et al., 2005; Reidel et al., 2018; Mékaoui et al., 2019). This clearly addresses the importance to provide this kind of information in phytochemical studies, so that they can also be used as a comparative tool in plant systematics. In conclusion, our results do not support a native origin of Bupleurum fruticosum in Tuscany. Anyway, we highlight the importance to integrate different sources of data (e.g., a phylogeographic study) to clarify the cryptogenic status of a species (De Castro et al., 2013).

Fig. 1. PCA 3D scatter plot based on phytochemical data (Component 1: 81.8%, Component 2: 11.0%, Component 3: 3.3% of the observed variance). Light blue bubbles: Sardinia; grey bubble: Corsica; black bubble: Libya; yellow bubble: Sicily; green bubbles: Tuscany; purple bubbles: Algeria; red bubbles: Portugal; blue bubble: France, light green bubble: Spain. For Tuscan population the Id sample is reported: Tls: leaves collected in summer, Tsts: stems collected in summer, Tsds: seeds collected in summer, Tlw: leaves collected in winter, Tstw: stems collected in winter, Tsdw: seeds collected in winter.

4. Discussion Our phytochemical results show that the EOs profile of Tuscan population of Bupleurum fruticosum is closer to that of more geographically distant populations and particularly to plants from Portugal, France, Spain, Algeria, and Sicily. These populations could be included in the chemotype α-pinene/β-pinene (Lorente et al., 1989; Maxia et al., 2011). On the contrary, populations from Sardinia and Corsica could be included in the chemotype β-phellandrene since this compound is higher than 50% (Liu et al., 2009; Maxia et al., 2011). Also the population from Libya is characterized by a high percentage of β-phellandrene (49%), together with a level of α-pinene higher than 15% (Giamperi et al., 1998). On the contrary, the populations from Corsica and Sardinia show low levels of this latter compound, with a percentage

Fig. 2. Map of Bupleurum fruticosum populations with chemotypes expressed by pie charts indicating the proportion of the four compounds which contributed more than 25% to the variation pattern documented in the PCA analysis. 5

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Declaration of competing interest

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