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International Journal of Environmental Research
University of Tehran
ISSN: 1735-6865 EISSN: 2008-2304
Vol. 4, Num. 1, 2010, pp. 1-10

International Journal of Environmental Research, Vol. 4, No. 1, 2010, pp. 1-10

Testing Nerium Oleander as a Biomonitor for Surfactant Polluted Marine Aerosol

Gonthier, P. 1, Nicolotti, G .1*, Rettori, A.1 , Paoletti, E.2 and Gullino, M. L.3

1 Plant Pathology, University of Torino, Via Leonardo da Vinci 44, I-10095 Grugliasco (Torino), Italy
2 Plant Protection Institute –CNR, Via Madonna del Piano 10, I-50019 Sesto Fiorentino (Firenze), Italy
3 Center of Competence for the Innovation in the Agro-environmental field, University of Torino, Via Leonardo da Vinci 44, I-10095 Grugliasco (Torino), Italy
*Corresponding author E-mail: giovanni.nicolotti@unito.it

Received 1 April 2009; Revised 12 Aug. 2009; Accepted 19 Aug. 2009

Code Number: er10001

ABSTRACT

Oleander was tested as biomonitoring plant for surfactant polluted marine aerosol. Potted plants in the greenhouse were sprayed once a week for 5 weeks with seawater containing sodium dioctyl sulfosuccinate (SDS) at the following concentrations: 5, 10, 15, 30, 60, 120, 250, 500 mg/L. A significant correlation was found between SDS concentration in the spray and surfactant deposit on the leaves at the end of the 5 weeks. At that time and two months later, we assessed: leaf visible injury, foliar chloride content, damage to stomatal crypts, water potential, net photosynthesis and stomatal conductance. Relative to controls (not sprayed and sprayed either with deionized water or with seawater without surfactants), all the parameters were affected (P<0.05) by the presence of surfactant. Furthermore they were correlated (P<0.05) with the concentration of surfactant. Visible injury occurred after treatments containing concentrations of surfactant exceeding 30 mg/L.

Key words: Sea pollutants, Detergents, Bioindicator, Physiopathology, Stomata

INTRODUCTION

Studies concerning the deterioration of coastal vegetation in densely-populated areas and in proximity to river mouths started, in Italy, around the end of the 1960s (Gellini and Paiero, 1969; Lapucci et al., 1972). According to these and subsequent studies, the role of pollution caused by surfactants, i.e. the active ingredients in commercially-available detergents, is crucial in determining environmental damages to the coastal flora. Surfactants reach the vegetation carried by marine aerosols, particularly frequent when seas are heavy. Surfactants cause the leaves to absorb more sea salt, leading to degeneration of the epicuticular waxes and alteration of photosynthetic processes (Itoh et al., 1963; Helenius and Simons, 1975; Badot and Badot, 1995; Badot et al., 1995). Along with desert dust, marine aerosol represents the highest percentage of aerosol emitted into the atmosphere each year (Giorgi, 1996).

Recently the phenomenon has been reported to assume worrying proportions in some coastal areas both in Italy (Bussotti et al., 1997; Nicolotti et al., 2001; Paoletti 2001; Rettori et al., 2005) and in other Countries such as Australia, France, Spain, Turkey and Tunisia (Astorga et al., 1993; Badot and Garrec, 1993; Garrec and El Ayeb, 2001; Marull et al., 1997). Despite the ban on non-biodegradable surfactants, the situation has not improved in the last years and these substances have been persisting in marine and coastal environments. Some investigations carried out in Israel and Turkey confirm the presence of surfactants in the Mediterranean sea and rivers (Vural et al., 1997; Zoller and Hushan, 2001).

Damages by surfactant-polluted marine aerosols, while found on a worldwide scale, strike well-defined areas, located either by the mouth of rivers near highly populated centers or in other remote locations, when the marine currents carry a surfactant load along the coastline (Nicolotti et al., 2005). Damages are generally found within 500-800 m inland.The classical analytical systems for the environmental monitoring have been successfully employed for the most common pollutants, i.e. those impacting on human health. On the contrary, compounds at very low concentrations are rarely analysed, including those having a potential impact on vegetation (Bargagli, 1998). For these reasons, the use of plants for environmental monitoring should be regarded as a suitable tool to integrate classical analytical methods.Among the most impacting pollutants, surfactants within marine aerosols are not detected by the classical systems. In addition, there are a very few reports about the biomonitoring of surfactants through plants (Nali et al., 2009). Hence there is a need to identify a specific biomonitor, sensitive, rustic and ornamental, when placed in urban environments, and useful to set up a wide and not expensive monitoring net. Preliminary field observations indicated that Oleander (Nerium oleander L.) is affected by foliar symptoms of abiotic origin in densely populated areas with spillage of high quantities of surfactant into the sea (Nicolotti et al., 2005). The above symptoms occur as a progressivelyspreading yellowing of the foliar lamina which may necrotize, leading to partial leaf fall, especially on the side exposed to sea winds. The phenomenon is extremely evident all the year round as Oleander is an evergreen species. Even if surfactant polluted marine aerosols can induce aspecific symptoms on many broadleaves and conifers species, Oleander was studied as a possible surfactant biomonitor, since it is sensitive to detergents, rustic and widespread along the Mediterranean coasts. This species has been used as a bioindicator to assess the presence of airborne heavy metals in urban environments (Oliva and Mingorance, 2006; Mingorance et al., 2007).

The main aim of this study was to test Oleander as a biomonitoring species for surfactant polluted marine aerosol. In particular we studied: 1) how realistic concentrations of surfactants affect the onset of aerosol toxicity in Oleander under controlled conditions, 2) which is the concentration threshold over which visible injury occurs, and 3) which physiological parameters are better correlated with the surfactant concentration.

MATERIALS & METHODS

Plant material and growing conditions Fifty-five healthy 3-year-old Oleander plants (Single Salmon variety, Cultivar group 4, single flower Pagen, 1988), 1 to 1.20 m height, growing in 5 dm3 pots were used. Plants were watered daily. Treatments were carried out in a greenhouse where air temperature and relative humidity were 20 ± 2°C and 40–60 %, respectively. The seawater used for the treatments, collected at a depth of 2 m off the Ligurian coast, was analysed in the laboratory using the Methylene Blue Active Substances (MBAS) method (Longwell and Maniece, 1955), in order to verify the absence of surfactant. The seawater was stored at 5 °C until use.

Plant crowns were sprayed once a week, for a period of 5 weeks, with seawater containing sodium dioctyl sulfosuccinate (SDS) at the following concentrations (Polluted Seawater; PSW): 5, 10, 15, 30, 60, 120, 250, 500 mg/L. Such concentrations were chosen to ensure foliar deposits comparable with those reported in the field (Nicolotti et al., 2005). Non-sprayed (NW) plants, plants sprayed with deionized water (DW) and plants sprayed with seawater and no surfactant (SW) were used as controls. For each treatment, 5 plants were sprayed until dripping point.A completely randomized block design was used.Before the treatments, in order to avoid contaminations of the soil, the pots were covered with a polythene film that was removed after each spray and replaced before the next one. Sprays were performed with a 100-l air compressor that was connected to a spray gun with a reservoir of 1 l, and regulated at an air exit pressure of 4 atm. The flow was regulated as to obtain drops of 70–150 µm diameter, as measured by using hydrosensitive sheets of paper (Guidi et al., 1988). For each plant, the following parameters were measured: 1) visible injury, 2) surfactant deposits on leaves, 3) foliar content of chloride (Cl-), 4) damages to the stomatal crypts, 5) water potential at midday, and 6) gas exchange. Visible injury was assessed three times, as suggested by Horsfall and Barratt (1945): at the end of the 5 weekly treatments (time I), one month (time II) and two months later (time III). The other parameters were assessed twice, immediately after the 5 treatments and two months later, except surfactant deposit on leaves that was determined only after the period of treatments.

Visible injury was assessed on all leaves of three randomly selected plants per treatment. The mean percentage of injured surface area per plant (IA) was visually assessed by using the scale in Granett (1982). The percentage of injured leaves per plant (IP) was calculated. A Plant Injury Index (PII) was then calculated by combining the two parameters: PII = (IA * IP) / 100 (Paoletti et al., 2009).For the assessment of surfactant deposit on leaves, 50 g of fresh leaves were sampled from each plant, washed in 1 l of deionized water, and analyzed using the Methylene BlueActive Substances (MBAS) method (Longwell and Maniece, 1955).For the determination of chloride content, 10 g of fresh leaves per plant per treatment were sampled. To remove chloride deposited above the leaves, the samples were washed 5 times in deionized water, each washing lasting 5 min. Content of Cl- was calculated by the volumetric method (American Public Health Association, 1992).

As Oleander stomata are inside crypts, i.e. invaginations of the epidermis in which several stomata are located, and crypts are covered by trichomes (Fig. 1). it was not possible to assess alterations of individual stomata. Thus, alterations of stomatal crypts as a whole were assessed on 15 randomly selected fully-developed leaves per treatment, 3 leaves per plant. The leaves were gathered with tweezers, in order to avoid damaging the cuticles during handling, and were dried as recommended by Kurhu and Huttunen (1986). Three square-shaped areoles of 2-3 mm2 were collected from the apical portion and from the centre of each leaf, fixed on an aluminium stub, metalized (sputter coater E5000C PS3), and observed with a 15 kV Cambridge Stereoscan 200 Scanning Electron Microscope. For each leaf areole, 50 crypts were assessed by using a modified version of the damage classes described by Crossley and Fowler (1986) (Fig. 1). An index of damage (ID) was finally calculated by applying the formula of Raddi et al. (1992).Measurements of midday water potential (MWP) were performed in the hottest hours of the day (from 11 a.m. to 2 p.m.) by using a portable pressure chamber (SKPM 1400, Skye Instruments). The crowns of three randomly selected plants per treatment were ideally subdivided into three portions (upper, middle and lower). Water potential was measured on three randomly chosen mature leaves per crown portion.

Gas exchange was measured with a portable gas exchange system (ADC/LCA-3) on three plants per treatment. The measurements were taken randomly in the top third of the crown since most of the photosynthesis and transpiration occur in that portion (Turner, 1981). To reduce variability due to the stage of foliar development, only fullydeveloped leaves (three per branch on three branches per plant) and with good exposure to the sun were chosen (Wong and Dunin, 1987). Measurements were carried out in clear blue skies (from 10.30 a.m. to 3.30 p.m.), at saturating light, i.e. 1300 µmol m-2 s-1 of photosynthetically active photon flux density (PPFD).Data were analyzed either with parametric or non-parametric methods depending on their normal distribution, as assessed through the Kolmogorov-Smirnov and Lilieford tests. Analysis of variance (ANOVA) and Tukey HSD test were used to test differences among treatments for gas exchange parameters (net photosynthesis and stomatal conductance) and surfactant deposit on leaves. For the other parameters, differences were tested through the non-parametric Kruskal-Wallis test. Cut-off for significance was set at 5%. After a significant Kruskal-Wallis, the Dunn test was performed as a post hoc test. The Spearman rank order correlation test was used to test correlations between parameters and concentration of surfactant in the treatment sprays. Statistical analyses were performed using the software Statistica (StatSoft Inc., Tulsa, Oklahoma).

RESULTS & DISCUSSION

At the end of treatments (time I), visible injury occurred at concentrations equal or greater than PSW30 (Fig. 2). corresponding to a surfactant deposit on the leaf surface of about 1 mg/L/kg fw (Fig. 3). At this time, PSW d” 120 did not differ significantly from controls while PSW250 and PSW500 did. At time II and III, injury occurred on the foliage of all plants treated with PSW, irrespective of SDS concentration. Controls did not show necrosis. Severity of symptoms was higher in plants treated with PSW containing higher concentrations of SDS, and became significantly higher with respect to controls after treatments with PSW 30. Necrosis always started at the apical portion of leaves and then progressively developed to the edges, spreading rapidly towards the inner leaf edge without affecting the veins. Injury was very evident on both the upper and lower side of leaves.A significant increase in MBAS deposits on leaves (mg/L/kg fw) was observed when raising the concentration of surfactant in the aerosol (F = 2535.4539; P <0.0001) (Fig.3). After the treatments (time I), chloride content increased linearly from DW to PSW10 and then was nearly stable, ranging from 0.95 to 1.23 % d.w., up to PSW500 (Fig . 4). Chloride contents in NW and DW leaves did not significantly differ at any time. At time III, chloride content increased linearly from DW to PSW30 and then was nearly stable, ranging from 1.28 to 1.55 % d.w. Chloride contents at time III were significantly higher than at time I in the treatments from PSW30 to PSW500.

Alterations to stomatal crypts occurred after treatments with PSW e”10 mg/L (Fig. 5). With the exception of controls and PSW5, ID values were lower at time I than at time III, and such differences were significant in most treatments. The maximum ID value (1.45) was observed with PSW30 two months after treatments. PSW containing 30 mg/L or higher concentrations of surfactant resulted in damages twice as severe than PSW with lower concentrations of SDS.Water potential showed similar trends at time I and III (Fig. 6). However, water stress was greater two months after the end of treatments. Such a difference was significant from PSW5 to PSW60. The minimum water potential was observed, in both the surveys, in plants treated with PSW500.

Treatments did not affect significantly the net photosynthesis of plants after the period of treatments (F = 1.6810; P = 0.0941), but they did two months later (F = 7.1985; P <0.0001). The lowest values of net photosynthesis, ranging from 1.37 to 1.61 µmol m–2 s-1, were measured on plants treated with PSW30, PSW120, PSW250 and PSW500. These were the only treatments showing values of net photosynthesis significantly lower than controls. Photosynthetic rates of the three controls were similar and did not differ significantly.Significant differences among treatments in terms of stomatal conductance (gs) were observed both after the period of treatments (F = 2.0554; P = 0.0342) and two months later (F = 6.2055; P <0.0001). At time I, the only two treatments showing significant differences amongst them were PSW30 and PSW500 (Fig. 7). At time III, a raise in SDS concentration resulted in a progressive decrease in stomatal conductance.

All parameters were significantly correlated with the concentration of surfactant in seawater at time II and III (Table 1). At time I, correlations between the concentration of surfactant in seawater and chloride content in leaves, net photosynthesis and stomatal conductance were not significant. Damage to stomatal crypts and water potential showed higher correlations with the concentration of surfactant in seawater at time I than at time III.

CONCLUSION

The results obtained in this study highlight the sensitivity of Oleander to surfactant polluted marine aerosols. Injury under controlled conditions was similar to injury observed in areas with spillage of high amounts of surfactant into the sea during preliminary field investigations (Nicolotti et al., 2005). Significant toxicity of surfactant and seawater depositions on leaves was previously reported on Chamaerops humilis L., Genista spp., Juniperus communis L., J. phoenicea L., Phoenix canariensis Chabaud, Quercus ilex L., Rosmarinus officinalis L. and Tamarix spp. (Guidi et al., 1988; Badot et al., 1995; Nicolotti et al., 2005; Rettori et al., 2005).Increasing amounts of surfactant in the seawater resulted in an increase in phytotoxicity, associated with the presence of chloride within the foliar tissues. The increased chloride uptake into the tissues is likely due to the lowering of surface tension of the seawater caused by the surfactant (Latif and Brimblecombe, 2004).The low amount of chloride in leaves treated with seawater (SW), as well as the absence of visible injury and the very low level of damage to stomata, suggest that Oleander is a species relatively tolerant against sea aerosol, as it may be equipped with efficient natural defenses (e.g., thick cuticles, stomata protected into crypts). Our data suggest that the presence of surfactant is crucial in the lowering of plant defense leading to phytotoxicity. Such interaction among salt, surfactant and plants was first documented on some pine species (Townsend, 1989).

The fact that the maximum damage to stomatal crypts (ID), the maximum visible injury (PII) at time II, and the highest content of chloride were found in plants treated with intermediate (e.g., PSW30) rather than highest concentrations of surfactant could be explained by the rapid phylloptosis which occurred much more frequently in plants treated with high concentrations of SDS. Immediately after the period of treatments, significant differences between controls and polluted treatments were noticed for most of the parameters. Two months later, such differences became even more evident, especially for treatments with high concentration of surfactant. The PSW30 concentration, equivalent to a surfactant deposit on leaves of about 1 mg/L/kg fw, is suggested as a threshold above which visible injury occurs and is easily recognizable. Furthermore, at that concentration we observed the highest content of chloride in leaves and a marked worsening of the alteration of stomatal crypts. The aforementioned value may thus be considered as a threshold of sensitivity for Oleander to surfactant-polluted marine aerosols. Similar values have been recorded in field conditions. In the Tuscany shore, deposits of MBAS ranging from 0.1 to 50 mg/L/kg fw were found on crowns of Pinus pinea directly exposed to sea winds (Bussotti et al., 1995). Thus, the Oleander proved to be a species sensitive to surfactants up to a threshold (1 mg/L/kgfw) which may be considered a reasonable alarm signal.Although visible injury was always correlated with the concentration of surfactant in seawater, including right at the end of the treatments, we believe that a reliable prediction of SDS concentration based on visible injury could be achieved only through the assessment of symptoms one month or two months after the exposure of plants. Based on the correlation analysis, delayed rather than immediate measurements would be better also for chloride content in leaves, net photosynthesis and stomatal conductance. In contrast, the damage to stomatal crypts is a very sensitive parameter even when assessed immediately after exposure. These findings suggest that polluted marine aerosol primarily affect the functionality of stomatal crypts, then induce accumulation of chloride (cuticular penetration) and physiological alterations in leaves, and visible injury development. Water potential is a very good predictor for marine polluted aerosol both after exposure than two months later.

According to Tingey’s description (1989), Oleander may be classified as a reactor organism, i.e. very sensitive to environmental stresses. We propose Oleandear as a biomonitor for assessing surfactants in marine aerosol. The dense and evergreen crown, both in mature and young plants, makes this species suitable to intercept aerosols all the year round. Plants small in size could be easily transported and exposed in risky areas and routinely analyzed, as previously recommended for the assessment of heavy metals depositions (Sawidis et al., 1995). Our results may help a correct planning, management and protection of coasts and shoreline vegetation.

ACKNOWLEDGEMENT

Work is partially supported by the Italian Ministry of Environment, Land and Sea.

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