Indian Journal Journal of Geo-Marine of Marine Sciences Sciences Vol. 43(6), June 2014, pp.1027-10351021-1029

Environmental significance of heavy metals in leaves and stems of mangroves, SW coast of

A. Badarudeen, " K. Sajan, , Reji Srinivas.? K. Maya? & D. Padmalal"

'Departmentment of Marine Geology and Geophysics, School of Marine Sciences, Cochin University of Science and Technology, Kochi 682 016, India.

2Centre for.Earth Science Studies, Thiruvananthapuram- 695031, Kerala, India

[E-Mail: [email protected]]

Received 17 December 2012; revised 2 May 2014

Out of the seven heavy metals (Fe, Mn, Co, Pb, Cd, Cu and Zn) studied in the leaves and stems of mangroves and mangrove associates of Veli (9 ), Kochi (5 species) and Kannur (9 species) regions, odol/am, a typical mangrove associate that spread in Veti, accounts for the highest contents of Mn and Cd. Other species do not show any specific heavy metal enrichment pattern in the coastal segments chosen for the present study. A comparative evaluation of heavy metal contents in the vegetal parts (leaves and stems) with that of the sediment substratum reveals that, almost all metals are concentrated in the former than latter.

[Keywords: Coastal sedimentary environments, Mangroves and mangrove associates, Heavy metals, Southwestern coast of India.]

Introduction are some of the other adaptations exhibited by mangrove to thrive in harmony within the Mangroves, a group of salt-tolerant plant intertidal zone", Studies on the geochemical communities occurring in the land-sea interface, characteristics of mangrove environment show that contribute significant quantities of organic matter and, major, micro and trace nutrient elements to the coastal/ sediments in this zone could sink a substantial quantity nearshore environments-" Many of the world's of toxic contaminants, particularly heavy metals, important mangrove populations are at the verge of without much damage to the vegetation":". Mangrove deterioration':'. Mangrove ecosystem is very fragile vegetation plays a significant role in regulating till owing to the peculiar conditions of hydrodynamics concentration of major and micro-nutrient elements and sedimentation. These inter-tidal forest ecosystems (including heavy metals) in soil/sediments of its support diverse communities of terrestrial and aquatic habitat. organisms of direct and indirect socio-economic Mangroves of Kerala in the south western coast values": of India are at the verge of severe degradation Mangroves act as a buffer between transitional, consequent to human interventions". In Kerala, major nearshore lagoon and estuarine envircr.ments". Leaves mangrove occurrences are reported at Veli, Kollam, of many mangroves possess halophilic properties with Kumarakom, Kochi, Chetwai, Nadakavu, Edakkad, a thick cuticle and large mucilage cells. Buttress roots, Pappinisseri, Kannur and Chiteri (Fig. I). Present knee roots, stilt roots and vertical pneumatophores study has been undertaken to examine the heavy metal

211Corresponding author

, l'rcscut address: Ikpartment of Mining and Geology, Kozhikode-673 020, Kerala. India 10281022 INDIAN J MAR SCI VOL. 43 (6), JUNE 2014

ecosystems of the state, viz., Veli, Kochi and Kannur mangroves. Materials and Methods Three mangrove fields located at Veli, Kochi and Kannur of Kerala state are chosen for the present investigation (Fig.1). Mangroves of Veli spread near the mouth of Veli lake. In the Kochi and Kannur mangroves spread is noticed in landward margins and islands of the coastal logoons. All the these three mangrove fields host distinct suites of mangrove vegetation. Most dominant mangrove/mangrove associated plants covering more than 70% of the mangrove vegetation are Acrostichum aureum, Barringtonia racemosa, Acanthus ilicifolius and Avicennia officinalis in the Veli mangroves; Avicennia officinalis, Rhizophora mucronata, agallocha and Acanthus ilicifolius in Kochi mangroves and Avicennia marina, Excoecaria agallocha, Derris trifoliata and Acanthus ilicifolius in Kannur mangroves16,17. Table 1 shows the various Fig. 1–Major mangrove occurrences in Kerala (after mangroves and mangrove associated plants whose Ramachandran and Mohanan 1991). vegetal parts have been selected for heavy metal analysis. accumulations in the vegetal parts (leaves and stems) of mangroves and mangrove associated plants in Field work was carried out in the Veli, Kochi and comparison to sediments in three important mangrove Kannur mangroves for the collection of surface

Table 1–The mangroves and mangrove associated plants of Veli, Kochi and Kannur areas sampled for the present study. Sl. No. Veli mangroves Kochi mangroves Kannur mangroves (8º30’- 8º31’30’’N ; ( 9º59’- 10º11’30’’N ; (12º3’30’’- 12º5’30’’N ; 76º52’30’’- 76º54’E) 76º14’- 76º16’E) 75º13’- 75º14’30’’E) 1. * Acrostichum aureum *Avicennia officinalis * Avicennia marina 2. *Barringtonia racemosa *Rhizophora mucronata *Excoecaria agallocha 3. *Acanthus ilicifolius * Excoecaria agallocha * Derris trifoliata 4. *Avicennia officinalis *Acanthus ilicifolius * Acanthus ilicifolius 5. Vitis vitigenia Bruguiera gymnorrhiza Rhizophora mucronata 6. Sonneratia caseolaris Kandelia candel 7. Derris trifoliata Avicennia officinalis 8. Cerbera odollam Acrostichum aureum 9. Premna serratifolia Rhizophora apiculata *Most common species covering >70% of total population in the area BADARUDEEN et al: ENVIRONMENTAL SIGNIFICANCE OF HEAVY METALS 10291023 sediment samples, vegetal parts (leaves and stems) and other relevant field data for the study. Sand, silt and clay contents of the sediments were estimated following the method of Lewis18. The wet oxidation method of El Wakeel and Riley19 was applied for sediment organic carbon estimation. Representative, matured leaves as well as stem of the mangroves and mangrove associated plants were chosen for heavy Fig. 2–Ternary diagram showing sediment types of Veli, metal analysis. Ashed (at 500ºC) vegetal parts (i.e. Kochi and Kannur mangroves. S Sand, C Clay, M Mud, Z Silt, leaves and stems) and dried, powdered sediment cS Clayey sand, mS Muddy sand, zS Silty sand, sC Sandy clay, sM Sandy mud and sZ Sandy silt. samples were decomposed using HF-HClO4-HNO3 acid mixture and analysed for heavy metal composition and organic carbon loading. The content concentrations using Atomic Absorption of sand is almost similar in Veli (av. 66%) and Kochi Spectrophotometer following Rantala and Loring20. (av. 66.5%) mangroves; whereas the sand content is Metal data were checked against the international slightly lower (av. 53%) in Kannur mangroves; standards G2 and W1 and, it was found that the (Table 2). Figure 2 shows the ternary diagram showing accuracy of the analysis was ± 5% for Pb and Cu, ± the sediment types of Veli, Kochi and Kannur 10% for Zn and Mn and ± 20% of Co and Cd with mangroves. In general, muddy sand, silty sand and respect to certified values. sandy mud are the dominant sediment types of these Results and Discussions mangrove environments. Average organic carbon content in Veli, Kochi and Kannur mangroves are Sediment characteristics 3.71%, 2.62%, 4.01%, respectively. Strong positive The sediments in the Veli, Kochi and Kannur correlation of organic carbon with mud contents mangroves vary considerably in their granulometric existing in the sediments of Veli, Kochi and Kannur

Table 2–Ranges and averages of sand, silt and clay contents in the surface sediments of Veli, Kochi and Kannur mangroves along with concentration of organic carbon and heavy metals.

Sample location Sand Silt Clay C-org Fe Mn Co Pb Cd Cu Zn (%) (ppm) Veli mangroves Maximum 96.94 71.79 35.10 7.29 1.95 388 55 103 2 81 86 Minimum 8.74 5.32 3.87 0.32 0.56 27 11 16 1 20 22 Average 66.00 20.00 14.00 3.71 1.01 162 30 48 1 40 62 Kochi mangroves Maximum 93.33 50.83 27.69 4.89 7.00 171 141 56 3 71 91 Minimum 27.10 5.86 0.80 0.52 1.56 40 12 11 <1 12 15 Average 66.50 23.50 11.00 2.62 4.50 98 93 31 2 41 39 Kannur mangroves Maximum 79.97 50.11 32.33 6.03 5.49 334 70 39 6 77 87 Minimum 23.86 12.37 5.35 1.99 2.30 262 20 17 1 19 48 Average 53.00 29.00 18.00 4.01 3.71 295 52 28 2 47 66 10241030 INDIAN J MAR SCI VOL. 43 (6), JUNE 2014

mangroves (Fig.3) reveals the ability of finer detritus in the mangrove environments to trap organic matter reaching the area from autochthonous (mainly from litter fall of mangrove and mangrove associated plants) and allochthonous (brought from distant places through channel networks) sources. The increased fertility of the sediments by the way of organic matter accumulation could promote fast spreading of mangrove vegetation on one side and the stabilization of lands on the other21. Heavy metals in mangrove leaves and stems Table 3 shows the results of the heavy metal analysis of mangroves and mangrove associates of the Veli along with that of the Kochi and Kannur mangroves. Out of the 9 species subjected heavy metal analysis, four species viz; as Acrostichum aureum, Barringtonia racemosa, Acanthus ilicifolius and Avicennia officinalis, cover more than 75% of the Veli mangroves. Therefore, these plants have a significant bearing on the biogeochemical cycling of heavy metals in the Veli mangroves. Concentration of Fe in the leaf of the mangroves and mangrove associated plants of Veli region varies considerably between 0.41% (Acanthus ilicifolius) and 1.65% (Sonneratia caseolaris). The content of Fe in the stem varies between 0.81%, (Avicennia officinalis) and 1.28% (Derris trifoliata). Manganese exhibits wide variation both in leaves and, in stems of the Veli mangroves. Cerbera odollam shows the highest Mn content (5413 ppm) in its leaves compared to the other species (Table 3). The lowest concentration of Mn (495 ppm) is recorded for the species Avicennia officinalis. Like leaves, the stem of Cerbera odollam also accounts for higher Mn contents (6073 ppm). Lowest value (258 ppm) is recorded in Acrostichum aureum. The content of Co varies between 22 ppm (Acrostichum aureum) and 330 ppm (Sonneratia caseolaris) in leaf and between 42 ppm (Avicennia officinalis) and 441 ppm (Derris trifoliata) in stem of the mangroves and mangrove associated plants of Veli. Content of Cu also shows a similar trend in leaf of Acrostichum aureum (Min: - 25 ppm) and Cerbera odollam (Max:- Fig. 3–The interrelationship existing among organic carbon 179 ppm). Minimum and maximum values of this and mud contents in the sediments of (A) Veli, (B) Kochi and (C) Kannur mangroves. metal in the stem of Veli mangroves are 76 ppm BADARUDEEN et al: ENVIRONMENTAL SIGNIFICANCE OF HEAVY METALS 10251031

Table 3–Trace metal concentrations in the leaves and stems of Veli, Kochi and Kannur mangroves. Environments/samples Fe% Mn Co Pb Cd Cu Zn (ppm) Leaf VELI MANGROVES Vitis vitiginia # 0.51 887 190 79 BDL 76 156 Sonneratia caseolaris 1.65 2268 330 40 BDL 101 305 Derris trifoliata 1.47 3165 132 40 9 153 393 Cerbera odollam # 1.19 5413 132 78 12 179 92 Premna serratifolia # 1.01 2299 99 119 4 165 280 Acrostichum aureum # 0.51 1278 22 158 6 25 194 Barringtonia racemosa # 0.69 1536 242 56 3 127 512 Acanthus ilicifolius 0.41 1031 144 80 12 144 385 Avicennia officinalis 0.69 495 77 79 3 140 167 Stem Vitis vitiginia # 0.23 1062 99 119 BDL 153 372 Sonneratia caseolaris 1.19 3041 99 158 BDL 204 412 Derris trifoliata 1.28 2907 441 79 3 432 442 Cerebera odollam # 0.50 6073 276 119 6 331 604 Premna serratifolia # 1.10 2371 110 158 3 114 224 Acrostichum aureum# 1.19 258 165 238 3 280 261 Barringtonia racemosa # 1.05 1041 396 40 BDL 483 531 Acanthus ilicifolius 0.59 1753 408 119 6 432 350 Avicennia officinalis 0.18 509 42 158 BDL 76 194 Leaf KOCHI MANGROVES Avicennia officinalis 0.55 510 55 42 2 68 146 Rhizophora mucronata 0.59 1236 170 130 1 70 140 Bruguiera gymnorrhiza 1.11 1062 140 45 <1 180 170 Acanthus ilicifolius 0.78 973 290 60 1 140 160 Excoecaria agallocha 0.43 864 260 40 <1 67 230 Stem Avicennia officinalis 0.72 612 38 96 2 55 163 Rhizophora mucronata 0.59 1081 180 140 1 33 100 Bruguiera gymnorrhiza 0.56 1044 120 100 <1 125 150 Acanthus ilicifolius 0.26 916 280 52 1 120 162 Excoecaria agallocha 0.23 742 260 40 1 150 221 Leaf KANNUR MANGROVES Avicennia marina 1.05 308 29 28 BDL 33 220 10261032 INDIAN J MAR SCI VOL. 43 (6), JUNE 2014

Excoecaria agallocha 0.43 3628 75 22 BDL 87 262 Derris trifoliata 0.24 2568 120 56 3 20 210 Kandelia candel 0.27 2778 75 28 2 27 142 Rhizophora mucronata 0.74 648 125 56 BDL 87 178 Rhizophora apiculata 1.01 635 105 48 3 92 155 Acrostichum aureum 0.92 535 25 BDL 3 54 47 Acanthus ilicifolius 1.83 559 50 28 BDL 33 232 Avicennia officinalis 0.27 1749 25 28 4 47 127 Stem Avicennia marina 0.49 211 22 83 3 32 287 Excoecaria agallocha 0.32 3062 25 56 BDL 141 351 Derris trifoliata 0.20 2074 100 35 3 53 374 Kandelia candel 0.19 2244 78 56 5 87 178 Rhizophora mucronata 0.12 543 150 46 2 64 86 Rhizophora apiculata 0.82 652 104 52 3 85 142 Acrostichum aureum 0.24 235 25 BDL 1 38 107 Acanthus ilicifolius 0.11 357 26 28 5 80 150 Avicennia officinalis 0.23 712 35 29 2 47 124 BDL – Below Detection # Mangrove associates; all others are mangroves

(Avicennia officinalis) and maximum 483 ppm ilicifolius and Bruguirea gymnorrhiza) were analysed (Barringtonia racemosa). Metal Pb shows 3 times for heavy metal concentrations in Kochi mangroves. (158 ppm) enrichment in leaf and 4 times (238 ppm) Of these, the first four species together constitute in stem of Acrostichum aureum compared to that in about 80% of the total mangrove population. The sediments (50 ppm; Badarudeen, unpublished data). concentration of Fe and Mn in leaves of Kochi Second highest Pb content is noticed in Premna mangroves varies from 0.43% (Excoecaria agallocha) serratifolia which accounts for 119 ppm in leaf and to 1.11% (Bruguirea gymnorrhiza) and 510 ppm 158 ppm in stem. Lowest Pb values are observed in (Avincennia officinalis) to 1236 ppm (Rhizophora the dominant species Barringtonia racemosa (leaf mucronata), respectively. In stem, Fe ranges from 56ppm; stem 40 ppm). Barringtonia racemosa 0.23% (Excoecaria agallocha) to 0.72% (Avicennia records the highest Zn concentration both in leaf (512 officinalis) and Mn from 612 ppm (Avicennia ppm) and stem (531 ppm). Avicennia officinalis officinalis) to 1081 ppm (Rhizophora mucronata) accounts for the lowest Zn concentration in their respectively. Concentration of Co varies from 55 ppm vegetal parts (leaf 167 ppm; stem 194 ppm). Cd is to 290 ppm in leaf and 38 ppm to 280 ppm in stem detected only in very low concentrations both in leaf (Table 3). Copper ranges between 67 ppm and 180 and in stem. In some cases, the metal was below ppm in leaves and 33 ppm to 150 ppm in stems of the detection limit. Kochi mangroves. Maximum concentration of Pb is A total of five species that are predominant in recorded in the mangrove species Rhizophora Kochi mangroves (Avicennia officinalis, Rhizophora mucronata (leaf 130 ppm; stem 140 ppm) and mucronata, Excoecaria agallocha, Acanthus minimum in Excoecaria agallocha (leaf 40 ppm; stem 40 ppm). Like the case of Veli mangroves, Zn is BADARUDEEN et al: ENVIRONMENTAL SIGNIFICANCE OF HEAVY METALS 10331027 1033 enriched significantly in the leaves and stems of the Average Pb content in leaves (av. 33 ppm) and stems Kochi mangroves as well. Lowest Zn value is (av. 43 ppm) of Kannur mangroves are also well above recorded for the species Rhizophora mucronata (140 the sediment average of 28 ppm. Content of Cu shows ppm) and the highest for Excoecaria agallocha (230 a minimum of 20 ppm in the leaf of Derris trifoliata ppm). Concentration of Cd varies between <1 ppm to a maximum of 92 ppm in Rhizophora apiculata. and 2 ppm both in leaves and stems. Concentrations vary from 32 ppm to 141 ppm in the stems of Avicennia marina and Excoecaria agallocha. Out of the 9 mangroves/mangrove associated Copper concentration in the Kannur mangroves shows plants analyzed in Kannur mangroves, (Table 3), higher values in stem (av. 70 ppm) than that of leaves Avicennia marina, Excoecaria agallocha, Derris (av. 53 ppm). Metals Co and Cu show a positive trifoliata and Acanthus ilicifolius together constitute correlation with mud content, organic carbon and Fe more than 75% of the mangrove population. The other in all the locations selected for the present study. Zn mangrove plants that are occurring in limited exhibits wide variation both in leaf and stem of proportion include Kandelia candel, Rhizophora Kannur mangroves. In leaves, Zn varies between 47 mucronata, Rhizophora apiculata, Acrostichum ppm (Acrostichum aureum) and 262 ppm (Excoecaria aureum and Avicennia officinalis. Fe concentration agallocha). The Zn accumulation noticed in stem in leaves varies from 0.24% (Derris trifoliata) to shows a minimum of 86 ppm (Rhizophora mucronata) 1.83% (Acanthus ilicifolius) while Mn from 308 ppm maximum of 374 ppm (Derris trifoliata). In general, (Avicennia marina) to 2778 ppm (Kandelia candel). the mean Zn concentration in leaves and stems (av. The respective ranges of Fe and Mn in the stem are 175 ppm and 200 ppm, respectively) shows 2-3 fold 0.11% (Acanthus ilicifolius) – 0.82% (Rhizophora enhancement with respect to sediment concentration apiculata) and 211 ppm (Avicennia marina) – (av. 66 ppm). 3062ppm (Exocoecaria agallocha), respectively. Mn content shows about 5 times the enrichment in the Being a living resource mangroves are self- leaves and stems of Kannur mangroves compared to maintaining and renewable, and hence act as a that in sediments. Cobalt content varies from 25 ppm bioshield protecting land and life the coastal areas. to 125 ppm in leaves and 22 ppm to 150 ppm in stems. Further, mangroves play a pivotal role in the Lowest concentration of Co is recorded in the stem biogeochemical cycling of carbon and other major, of Avicennia marina. The average Co concentration minor and trace elements including the heavy metals. in leaf (70 ppm) and stem (63 ppm) is slightly higher Present study on the heavy metal contents in the leaves than that of sediment substratum (av. 52 ppm). and stems of the mangroves in the Kerala coast

Table 4–The interrelationship between organic carbon and heavy metals in Veli, Kochi and Kannur mangroves. Heavy metals Veli mangroves Kochi mangroves Kannur mangroves

Mud % C-org % Mud % C-org % Mud % C-org % Fe 0.08 -0.02 0.87 0.88 0.78 0.8 Mn -0.19 -0.27 0.34 0.39 0.38 0.47

Co 0.26 0.29 -0.12 -0.14 0.79 0.81

Pb 0.13 0.07 0.03 0.09 0.77 0.76 Cd -0.05 -0.08 0.17 0.16 0.54 0.59

Cu 0.04 0.06 0.05 0.09 0.97 0.96

Zn 0.01 0.28 0.47 0.57 0.82 0.79 1034 1028 INDIAN J MAR SCI VOL. 43 (6), JUNE 2014 reiterates their ability to accelerate the process of of Mn and Cd in its vegetal parts (Table 3). A natural cleansing of soil/sediments by assimilating a comparison between the common mangrove species significant proportion of toxic elements like heavy of Veli with Kochi and Kochi with Kannur reveals metals in their vegetal parts without much damage to that, with the exception of Fe and Mn, the other heavy the plants. However, due to the increasing pace of metals generally register the highest values in Veli urbanization, tourism promotion activities, mangroves followed by Kochi and Kannur unscientific fishing, etc., these plant communities mangroves. Although Kochi is the major industrial became more and more degraded in the coastal hub in Kerala, mangroves spread some distance away sedimentary environments. Situation is ratcher from the distributary channels carrying pollutant flux alarming in Kerala as the state is undergoing rapid from the industrial belt. But at Veli, the mangrove urbanization and industrialization consequent to environment receives pollutants directly from the economic development in the past 4-5 decades. industrial units23. Urban discharge from the capital city, Thiruvananthapuram, also aggravate the situation The study reveals that the distribution of organic further. An overall evaluation of the heavy metal carbon in the sediments of Veli, Kochi and Kannur concentrations in the vegetal parts of the mangroves mangroves reflects their marked textural dependency with that of the surface sediments shows that, except indicating the efficiency of finer clastics to trap Fe, all the other elements are enriched generally in excessive quantities of organic detritus in the sediment the vegetal samples than sediments. blanket, a feature also was observed elsewhere21,22. It A comparative evaluation of the average Fe is axiomatic that the mangrove environment acts as values between the three mangrove environments efficient sinks of organic carbon in the highly selected for the present study reveals that mangrove productive coastal areas. Poor correlation of organic plants of Kochi record the highest Fe content than carbon with various heavy metals in Veli and Kochi the other two mangrove environs. Metals Fe and Mn mangroves (Table 4) indicate, that mangrove litter and in sediments show positive correlation with mud and other organic detritus hardly influence the overall organic carbon contents in Kochi and Kannur distribution of heavy metals in sediments compared mangroves (Table 4). Absence of such a relation in to other contributary sources. Contrary to this, the Veli mangroves might be attributed to leaching of Kannur mangroves show a significant positive metals from the sediments by the acidic effluents correlation of heavy metals with organic carbon and reach the area from the nearby industrial mud contents reiterating the role of decayed mangrove establishments23. Pb gives strong correlation with detritus, trapped effectively by finer clastic like silt organic carbon and mud, and a marginal correlation and clay (ie., mud), in determining the heavy metal with Fe. Pb carried in solutions can get hydrolysed dispersal (Table 4) of the area. A comparative and co-precipitated and later be absorbed onto clays. evaluation of Zn accumulations in the leaves and Analysis of the relative abundance of Cd in the stems of various mangroves and mangrove associated mangrove environments reveal that, a substantial plants shows that, the Veli mangroves register the quantity of metal is found associated either with silt highest concentration (Leaf-276 ppm; Stem- 377 ppm) and clay dominated textural facies. than Kochi (Leaf-169 ppm; Stem-159 ppm) and Acknowledgements Kannur (Leaf- 175ppm; Stem- 200ppm) mangroves. Cadmium occurs in lower levels in the leaves and Authours thank the Directors of Centre for Earth stems of most of the plants of Veli, Kochi and Kannur Science Studies (CESS), Thiruvananthapuram and areas. The content of Cd varies between 1 ppm and School of Marine Sciences, Cochin University of 12 ppm (av. 4 ppm) in leaf and 1 ppm to 6 ppm (av. 3 Science and Technology for facilities. First author ppm) in stem of the mangrove palnts. The species (A Badarudeen) thanks Dr. C. N Mohanan, Former Cerbera Odallam assimilates higher concentrations Head, Environmental Sciences Division, CESS for BADARUDEEN et al: ENVIRONMENTAL SIGNIFICANCE OF HEAVY METALS 10291035 identification of mangroves and mangrove associates. sediments of mangroves lagoons and southern bay in Heads of the Departments of Chemical Sciences Florianopolis Island. Environ. Technol., 17 (10);1035-1046. Division, CESS and Chemical Oceanography 13 Tam, N.F.Y. & Yao, M.W.Y., (1998). Normalization and Division, CUSAT are acknowledged for their help in heavy metal contamination in mangrove sediments. Sci. of chemical analysis of samples. the Total Environ., 216 (1-2);33-39. 14 Amusan, A.A. & Adeniyi, I.F., (2005). Genesis, References classification and heavy metal retention potential of soils in mangrove forest, Niger delta, Nigeria. Jour. Hum. Ecol., 1 Vannucci, M., (1989). 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