Phytoremediation of Mangrove species exposed to effluents of mining ultramafic soils

Paper Details

Research Paper 01/02/2020
Views (403) Download (13)

Phytoremediation of Mangrove species exposed to effluents of mining ultramafic soils

Joel A. Mercado, Lowell G. Aribal
J. Bio. Env. Sci.16( 1), 50-70, February 2020.
Certificate: JBES 2020 [Generate Certificate]


The study was conducted to determine the phytoremediation potentials of some mangrove species inside a mine site of Platinum Group Metals Corporation (PGMC) in Claver, Surigao del Norte. For comparison purposes, a separate mangrove forest located at Nasipit, Agusan del Norte (ADN) free from mining activities was also studied. Plant tissues of the three species with the highest SIV in both study sites were analyzed using Microwave Plasma-Atomic Emission Spectrometer and Acid Digestion. Lumnitzera racemosa, L. littorea and Quassia indica had the highest importance values at PGMC and Avicennia officinalis, L. racemosa, and Ceriops tagal at Nasipit, ADN. The two sites differ in species composition manifested by low similarity index. Quassia indica at PGMC and C. tagal at Nasipit, ADN exhibited characteristics of a hyperaccumulator for Molybdenum, Manganese, Lead, Chromium and Nickel. L. racemosa, L. littorea and A. officinalis were possible excluders of Molybdenum, and A. officinalis was a probable indicator of Lead. Salinity is highly encouraged for inclusion in studies of this kind as it also affects species composition, while verification studies should be conducted to validate the results of the study on the phytoremediation potentials of the species examined due to antagonistic and synergistic behaviors of heavy metals.


Abou Seedo K, Abido M, Salih A, Abahussain A. 2017. Assessing heavy metals accumulation in the leaves and sediments of urban mangroves (Avicennia marina (Forsk.) Vierh.) in Bahrain, International Journal of Ecology 2017(1), 48-55.

Abou Seedo K, Abido M, Salih A, Abahussain A. 2017. Structure and Composition of Mangrove Associations in Tubli Bay of Bahrain as affected by municipal wastewater discharge and anthropogenic sedimentation, International Journal of Biodiversity 2017(1), 1-9. DOI: 10.1155/2017/2084256

Agilent Technologies. 2016. Microwave plasma atomic emission spectroscopy (MP-AES) application eHandbook. Retrieved from https://www.agilent. com/en-us/agilent404? library/applications/5991-7282en_mp-aes-ebook.pdf

Ahmed W, Shahid S. 2015. Status of mangroves of North-Western part of Indus Delta: Environmental characteristics and population structure. Pakistan Journal of Marine Science 24(1&2), 61-85. retrieved from publication/ 321016480_status_of_mangroves_of_north-western _part_of_indus_delta_environmental_characteristics_and_population_structure

Al Hagibi H, Nagi H, Al-Selwi K, Al-Shwafi N. 2018. Assessment of heavy metals concentration in mangroves leaves of the Red Sea Coast of Yemen. Journal of Ecology & Natural Resources 2(1), 1-13. DOI: 10.23880/jenr-16000120

Alberto A, Vizmonte J, Sigua G. 2015. Assessing diversity and phytoremediation potential of mangroves for Copper contaminated sediments in Subic Bay, Philippines. International Journal of Plant, Animal and Environmental Sciences 5(4), 50-59. Retrieved from /publication/283327818_Diversity_and_phytoremediation_potential_of_mangroves_for_copper_contaminated_sediments_in_Subic_Bay_Philippines

Allahnouri M, Aghbash F, Pazhouhan I. 2018. Traffic effects on leaf macro- and micro-morphological traits. Folia Oecologica 45(2). doi: 10.2478/foecol-2018-0010

Alloway B, Ayres D. 2007. Chemical principles of environmental pollution, Second Edition. London, UK: Blackie Academic and Professional.

Alzahrani D, Em S, Em M. 2018. Ecological assessment of heavy metals in the grey mangrove (Avicennia marina) and associated sediments along the Red Sea Coast of Saudi Arabia. Oceanologia 60(4), 513-526. DOI: 10.1016/j.oceano.2018.04.

Appannagari R. 2017. Environmental pollution causes and consequences: A study. North Asian International Research Journal of Social Science & Humanities 3(8). 151-161. Retrieved from

Arellano P, Tansey K, Balzter H, Tellkamp M. 2017. Plant family-specific impacts of petroleum pollution on biodiversity and leaf chlorophyll content in the Amazon rainforest of Ecuador. PLoSONE 12(1), 1-18. DOI: 10.1371/journal.pone.0169867

Aribal L, Llamos E, Bruno A, Medina M. 2016. Comparative leaf morphometrics of two urban tree species: an assessment to air pollution impacts. J. Bio. Env. Sci 9(1), 106-115. Retrieved from

Aribal L, Marin R, Miras N. 2016. The metallophytes in the ultramafic soil of Mt. Kiamo in Malaybalay, Bukidnon, Philippines. Journal of Biodiversity and Environmental Sciences 8(4), 142-150.

Arif T, Mudsser A, Kehkashan S, Arif A, Inho C, Qazi M, Rizwanul H. 2015. Heavy metals and human health: mechanistic insight into toxicity and counter defense system of antioxidants. International Journal of Molecular Science 16(12), 29592–29630. doi: 10.3390/ijms161226183

Ashfaque F, Inam A, Sahay S, Iqbal S. 2016. Influence of heavy metal toxicity on plant growth, metabolism and its alleviation by phytoremediation – a promising technology. Journal of Agriculture and Ecology Research International 6(2), 1-19. DOI: 10.9734/jaeri/2016/23543

Ata J, Luna A, Tinio C, Quimado M, Maldia L, Abasolo W, Fernando E. 2016. Rapid Assessment of Plant Diversity in Ultramafic Soil Environments in Zambales and Surigao del Norte, Philippines. Asian Journal of Biodiversity 7. doi: 10.7828/ajob.v7i1.864

Ayodele O, Olubunmi S, Temitope B. 2014. Heavy metal pollution assessment of granite quarrying operations at Ikole-Ekiti, Nigeria. International Journal of Environmental Monitoring and Analysis 2(6), 333-339. DOI: 10.11648/ j.ijema.20140206.16

Barbante C, Boutron C, Moreau AL. 2002. Seasonal variations in nickel and vanadium in Mont Blanc snow and ice dated from the 1960s and 1990s. Journal of Environmental Monitoring 4(6), 1-19. DOI: 10.1039/b208142c

Bhalerao S, Sharma A, Poojari A. 2015. Toxicity of nickel in plants. International Journal of Pure and Applied Biosciences 3(2), 345-355. Retrieved from,%20issue%202/IJPAB-2015-3-2-345-355.pdf

Bitantos B, Abucay M, Dacula J, Recafort R. 2017. Mangrove in the grove: diversity, species composition, and habitat in Pamintayan, Dumanquillas Bay, Philippines. AES Bioflux 9(3), 183-192. Retrieved from http://www.aes. bioflux.

Borymski S, Cycon M, Beckmann M, Mur L, Piotrowska-Seget Z. 2018. Plant species and heavy metals affect biodiversity of microbial communities associated with metal-tolerant plants in metalliferous soils. Front. Microbiol 2018(9), 1-18. DOI: 10.3389/fmicb.2018.01425

Bothe H. 2011. Plants in heavy metal soils. In Sherameti, I. & Varma, A., (Eds.), Detoxification of heavy metals. Soil Biology 30, 35-57. DOI: 10.1007/978-3-642-21408-0_2

Bruno A, Aribal L, Lustria MG, Marin R. 2016. Phytoremediation potential of mangrove species at Pangasihan Mangrove forest reserve in Mindanao, Philippines. Journal of Biodiversity and Environmental Sciences 9, 142-149. Retrieved from

Bubb IM, Lester JN. 1996. Factors controlling the accumulation of metals within fluvial systems. Environ Monit Assess 41(1), 87-105. https://

Cañizares LP, Seronay RA. 2016. Diversity and species composition of mangroves in Barangay Imelda, Dinagat Island, Philippines. AACL Bioflux 9(3). 518-526. Retrieved from http://www. bioflux.

Cempel M, Nikel G. 2006. Nickel: A Review of Its Sources and Environmental Toxicology. Polish Journal of Environmental Studies 15(3), 375-382. Retrieved from,87881,0,2.html

Chakraborty D, Subhajit B, Majumdar M, Santra S. 2013. Heavy metal pollution and phytoremediation potential of Avicennia officinalis L. in the southern coast of the Hoogly estuarine system. International Journal of Environmental Sciences 3(6), 2291-2303. DOI: 10.6088/ijes.2013030600045

Chibuike GU, Obiora SC. 2014. Heavy metal polluted soils: effect on plants and bioremediation methods. Applied and Environmental Soil Science 2014, 1-12. DOI: 10.1155/2014/752708

Chiroma TM, Ebewele RO, Hymore FK. 2014. Comparative assessment of heavy metal levels in soil, vegetables and urban grey waste water used for irrigation in Yola And Kano. International Refereed Journal of Engineering and Science 3(2), 1-9.

Claveria R. 2012. Phytoremediation: An environmental option to mine rehabilitation [PowerPoint slides]. Retrieved from

Dahdouh-Guebas F. (Ed.). 2018. World mangroves database. Lumnitzera racemosa Willd. Retrieved from: /mangroves/aphia.php?p=taxdetails&id=235053

Dahdouh-Guebas F, Koedam N. 2008. Long-term retrospection on mangrove development using transdisciplinary approaches: A review. Aquatic Botany 89(2), 80-92. DOI: 10.1016/j.aquabot. 2008.03.012

Dangan-Galon F, Dolorosa RG, Sespeñe JS, Mendoza NI. 2016. Diversity and structural complexity of mangrove forest along Puerto Princesa Bay, Palawan Island, Philippines. Journal of Marine and Island Cultures 5(2), 118-125. https://

De Wolf H, Ulomib SA, Backeljau T, Pratap CHB, Blust R. 2015. Heavy metal levels in the sediments of four Dar es Salaam mangroves accumulation in, and effect on the morphology of the periwinkle, Littoraria scabra (Mollusca: Gastropoda). Environment International 26(4). Retrieved from pubmed/11341292

Defew LH, Mair JM, Guzman HM. 2005. An assessment of metal contamination in mangrove sediments and leaves from Punta Mala Bay, Pacific Panama. Marine Pollution Bulletin 50(5), 47-52. DOI: 10.1016/j.marpolbul.2004.11.047

Department of Environment and Natural Resources – Mines and Geo-Sciences Bureau, Mining Tenements Management Division. 2017. Mineral Production Sharing Agreement (MRMS Report No. 002A). Retrieved from http://mgb. mpsa

Department of Environment and Natural Resources – Pollution Adjudication Board. 2000. Mining Related Incidents. Unpublished public record.

Dexter E, Rollwagen-Bollens G, Bollens SM. 2018. The trouble with stress: A flexible method for the evaluation of nonmetric multidimensional scaling. Limnology and Oceanography Methods 16, 434-443. DOI: 10.1002/lom3.10257

Dudani S, Lakhmapurkar J, Gavali D, Patel T. 2017. Heavy metal accumulation in the mangrove ecosystem of South Gujarat Coast, India. Turkish Journal of Fisheries and Aquatic Sciences 17(4), 755-766. DOI: 10.4194/1303-2712-v17_4_11

Echevarria. 2018. Genesis and Behaviour of Ultramafic Soils and Consequences for Nickel Biogeochemistry. In van der Ent A, Echevarria G, Baker AJM, Morel JL. (Eds.), Agromining: Farming for Metals (pp.135-156). DOI: 10.1007/978-3-319-

Ellenberg Н, Mueller-Dombois D. 1974. Aims and methods of vegetation ecology. New York: John Wiley and Sons.

Ellison AM. 2008. Mangrove ecology – applications in forestry and coastal zone management. Aquatic Botany 89(2008), 77. DOI: 10.1016/j.aquabot.2008.

Emamverdian A, Yulong D, Farzad M, Yinfeng X. 2015. Heavy metal stress and some mechanisms of plant defense response. The Scientific World Journal 2015, 1-18. DOI: ORG/10.1155/2015/756120

Erakhrumen A. 2015. Assessment of in-situ natural dendroremediation capability of Rhizophora racemosa in a heavy metal polluted mangrove forest, Rivers State, Nigeria. Journal of Applied Sciences and Environmental Management 19(1), 21-27.

Ernst W. 2006. Evolution of metal tolerance in higher plants. Forest Snow and Landscape Research 80(3), 251-274. Retrieved from https://www.researc /publication/279562675_evolution_of_ metal_tolerance_in_higher_plants

Fernando ES. 2010. Checklist of species in FBS 21 – Taxonomy of forest plants, 13th Revised Edition [Class handout]. Los Baños, Philippines: University of the Philippines, FBS21.

Gall E, Robert J, Robert B, Rajakaruna N. 2015. Transfer of heavy metals through terrestrial food webs: A review. Environmental Monitoring and Assessment 187(4), 187-201. DOI: 10.1007/s10661

Garcia K, Gevaña D, Malabrigo P. 2013. Philippines’ Mangrove Ecosystem: Status, Threats, and Conservation. In Faridah-Hanum I, Latiff A, Hakeem KR, Ozturk M. (Eds.). Mangrove Ecosystems of Asia: Status, Challenges and Management Strategies (pp. 82-92). DOI: 10.1007/978-1-4614-858

Gevorgyan GA, Movsesyan HS, Grigoryan KV, Ghazaryan KA. 2015. Environmental risks of heavy metal pollution of the soils around Kajaran town, Armenia. Proceedings of the Yerevan State University. Chemistry and Biology, 2015(2), 50-55.

Giesen W, Wuffraat S, Sieren S, Scholten ML. 2007. Mangrove guidebook for Southeast Asia. Bangkok, Thailand: FAO Regional Office for Asia and the Pacific.

Global Ferronickel Holdings Inc. 2016. Annual Report 2016 (Report No. 17-A). Retrieved from pdf/ other-disclosures/FNI%2017A%20year%202016.pdf

Grosse S, Matte T, Schwartz J, Jackson R. 2002. Economic gains resulting from the reduction in children’s exposure to lead in the United States. Environ Health Perspect 110(6), 563-569. Retrieved from /pubmed/ 12055

Grygorieva O, Klymenko S, Vinogradova Y, Ilyinska A, Piorecki N, Brindza J. 2018. Leaf characteristics as important morphometric discriminators for chestnut (Castanea sativa Mill.) Genotypes. Agrobiodiversity for Improving Nutrition, Health and Life Quality 2018, 146-158. doi: http://10.15414/agrobiodiversity.2018.2585-8246.

Hammer O, Harper D, Ryan P. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 1-9. Retrieved from

Harasim P, Filipek T. 2015. Nickel in the environment. Journal of Elementology 20(2), 525-534. DOI: 10.5601/jelem.2014.19.3.651

Helena L, Chaves L, Alexandra Estrela M, Sena De Souza R. 2011. Effect on plant growth and heavy metal accumulation by sunflower. Journal of Phytology 3(12), 4-9. doi: https://www.researchgate. net/publication/266589410_Effect_on_plant_growth_and_heavy_metal_accumulation_by_sunflower

Hernández J, Pastor J. 2008. Relationship between plant biodiversity and heavy metal bioavailability in grasslands overlying an abandoned mine. Environmental Geochemistry and Health 30, 127-33. DOI: 10.1007/s10653-008-9150-4

Jaishankar M, Mathew B, Shah M, Gowda K. 2014. Biosorption of few heavy metal ions using agricultural wastes. Journal of Environment Pollution and Human Health 2(1), 1-6. doi:10.12691/jephh-2

Jaishankar M, Tseten T, Anbalagan N, Mathew B, Beeregowda K. 2014. Toxicity, mechanism and health effects of some heavy metals. Interdisciplinary Toxicology 7(2), 60-72. DOI: 10.2478/intox-2014-0009

Jamila Alfaraas AM, Jusoh K, Ismail BS, Talip N. 2016. Effects of heavy metal exposure on the morphological and microscopical characteristics of the paddy plant. Journal of Environmental Biology 37(5), 955-963. Retrieved from https://www.

Jorgenson A, Dunlap R. 2012. Environmental Problems. The Wiley-Blackwell Encyclopedia of Globalization. DOI: 10.1002/9780470670590.wbeog

Kaewtubtim P, Meeinkuirt W, Seepom S, Pichtel J. 2016. Heavy metal phytoremediation potential of plant species in a mangrove ecosystem. Applied Ecology and Environmental Research 14(1), 367-382. DOI:

Kannan N, Thirunavukkarasu N, Suresh A, Rajagopal K. 2016. Analysis of heavy metals accumulation in mangroves and associated mangroves species of ennore mangrove ecosystem, East Coast India. Indian Journal of Science and Technology 9(46), 1-12. DOI: 10.17485/ijst/2016

Kanter J. 2007. UN issues “final wake-up call” on population and environment. International Herald Tribune. Retrieved from articles/2007/10/25/europe/environ.php

Kiran B, Prasad M. 2017. Ricinus communis L. (Castor bean), a potential multi-purpose environmental crop for improved and integrated phytoremediation. The EuroBiotech Journal 1(2), 101-116. DOI: 10.24190/ISSN2564-615X/2017/02.01

Kumar J, Kumar ME, Vijay G, Rajanna K, Sagar M, Naik AS, Kumar K, Pandey A, Manjappa N, Pal J. 2014. Ecological Benefits of Mangrove. Life sciences Leaflets 48, 85-88. Retrieved from https://www.r 271933133_ecological_benefits_ of_mangrove

Kupper H, Lombi E, Zhao FJ, Weishammer G, McGrath SP. 2001. Cellular compartmentation of nickel in the hyperaccumulators Allysum lesbiacum, Allysum bertolonii, and Thiaspe goesingense. Journal of Experimental Botany 52, 2291-2300. Retrieved from

Kutty A, Al-Mahaqeri S. 2016. An investigation of the levels and distribution of selected heavy metals in sediments and plant species within the vicinity of ex-iron mine in Bukit Besi. Journal of Chemistry 16(12), 1-12. DOI: org/10.1155/2016/2096147

Laghlimi M, Baghdad B, El Hadi H, Bouabdli A. 2015. Phytoremediation mechanisms of heavy metal contaminated soils: a review. Open Journal of Ecology 5, 375-388. Doi: org/10.4236/oje.2015.58031

Mahalakshmi M, Marisamy K, Ramasubramanian V. 2017. Cadmium toxicity induced changes on morphological, photosynthetic, biochemical and antioxidative enzymes level in Vigna mungo (L.) Hepper Environment and Ecology Research 5(6), 422-426. DOI: 10.13189/eer.2017.0

Maldonado-Román M, Jiménez-Collazo J, Malavé-Llamas K, Musa-Wasill JC. 2016. Mangroves and their response to a heavy metal polluted wetland in the North Coast of Puerto Rico. Journal of Tropical Life Science 6(3), 210-218.

Malhado AC, Malhi Y, Whittaker RJ, Ladle RJ, Stegee H, Phillips OL, Butt N, Arag-ao LEOC, Quesada CA, Araujo-Murakami A, Arroyo L, Peacock J, Lopez-Gonzalez G, Baker TR, Anderson LO, Almeida S, Higuchi N, Killeen TJ, Monteagudo A. 2009. Spatial trends in leaf size of Amazonian Rainforest Trees, Biogeo 6. 1563–1576.

Malik ZH, Ravindran KC, Sathiyaraj G. 2017. Phytoremediation: a novel strategy and eco-friendly green technology for removal of toxic metals. International Journal of Agricultural and Environmental Research 3(1), 1-18. Retrieved from

Marques A, Moreira H, Rangel A, Castro P. 2019. Heavy metal accumulation and relation with soil contamination in Rubus ulmifolius growing in Esteiro de Estarreja, Portugal. https://repositorio itstream/10400.14/5789/1/trab_inter

Martinez M, Buot JrI. 2018. Mangrove assessment in Manamoc Island for coastal retreat mitigation. Journal of Marine and Island Cultures 7(1), 65-83.

Massoud R, Hadiani MR, Hamzehlou P, Khosravi-Darani K. 2019. Bioremediation of heavy metals in food industry: Application of Saccharomyces cerevisiae. Electronic Journal of Biotechnology 37, 56-60.

McKee K, Feller I, Lovelock C, Uta B, Samantha J, Ball M. 2010. Biocomplexity in mangrove ecosystems. Annual review of marine science 2, 395-417. DOI: 10.1146/annurev. marine. 010908.163809

Meeinkuirt W, Kaewtubtim P, Seepom S, Pichtel J. 2017. Metal uptake and accumulation by mangrove plant species in Pattani Bay, Thailand. 3rd World Congress on New Technologies, Rome, Italy June 6-8, 2017. DOI: 10.11159/icepr17.158

Mehes-Smith M, Nkongolo K, Cholewa E. 2013. Coping mechanisms of plants to metal contaminated soil. Environmental Change and Sustainability 53-90.

Mehran J, Sahar K. 2017. Grey mangrove Avicennia marina (Forsk.) Vierh. as a bio-indicator to measure nickel, mercury and cadmium: a case study at persian gulf port shoreline, Khuzestan, Iran. Environmental Engineering & Management Journal 16(9), 2133-2138. DOI: 10.30638/eemj.2017.220

Mendez P, Acevedo Sandoval J, García P, González NT. 2018. Phytoremediation of soils contaminated with heavy metal. Biodiversity International Journal 2(4), 362‒376. DOI: 10.15406/bij.2018.02.0008

Merrill E. 1903. A dictionary of the plant names of the Philippine islands. Manila: Bureau of Public Printing.

Mganga N, Manoko M, Rulangaranga Z. 2011. Classification of plants according to their heavy metal content around North Mara gold mine, Tanzania: Implication for phytoremediation. Tanzania Journal of Science 37, 109-119. DOI: 10.4314/tjs.v37i1

Miller G, Lugo A. 2009. Guide to the ecological systems of Puerto Rico. Gen. Tech. Rep. IITF-GTR-35. San Juan, PR: U.S. Department of Agriculture, Forest Service, International Institute of Tropical Forestry 437 p.

Miththapala S. 2008Mangroves. Coastal Ecosystems Series Volume 2 pp 1-28 + iii, Colombo, Sri Lanka: Ecosystems and Livelihoods Group Asia, IUCN.

Morais S, Garcia F, Costa E, Pereira M. 2012. Heavy metals and human health. In Prof. J. Oosthuizen (Ed.), Environmental health-emerging issues and practice (pp. 228-246). DOI: 978-953-307-854-0

Mueller-Dombois Dieter, Ellenberg, Heinz. 1974. Aims and methods of vegetation ecology. Retrieved from publication/259466952_Aims_and_methods_of_ vegetation_ecology

Nagajyoti P, Lee K, Sreekanth T. 2010. Heavy metals, occurrence and toxicity for plants: a review. Environmental Chemistry Letters 8(3), 199-216.

Nath B, Cholakov G. 2009. Pollution control technologies. In G. Cholakov, & B. Nath (Eds.), Encyclopedia of Life Support Systems 1, 1-49. Retrieved from https://www.researchgate .net/

Ngole V, Fonge B, Tabot P, Mumbang C. 2016. Impact of logging activities in a tropical mangrove on ecosystem diversity and sediment heavy metal concentrations. Journal of Coastal Conservation 20, 245-255. DOI: 10.1007/s11852-016-0435-y

Numbere A. 2018. Mangrove species distribution and composition, adaptive strategies and ecosystem services. In Sharma, S. (Ed.), Mangrove Ecosystem Ecology and Function (pp. 17-39). http:// /10.5772/intechopen.79028

Ogundiran M. 2014. Lead and Cadmium phytoremediation potentials of plants from four lead smelting slags contaminated sites. Natural Environment 2(3), 33-38.

OHIO EPA. 2002. Pollution prevention opportunities for PBT chemicals nickel and nickel compounds. No. 97.

Ojekunle Z, Adebojem R, Taiwo A, Sangowusi R, Taiwo A, Ojekunle V. 2014. Tree leaves as bioindicator of heavy metal pollution in mechanic village, Ogun State. Journal of Applied Science Environmental Management 18(4), 639-644.

Oves M, Saghir K, Huda Qari A, Nadeen F, Almeelbi T. 2016. Heavy metals: biological importance and detoxification strategies. Journal of Bioremediation Biodegradation 7(2), 1-15. DOI: 10.4172/2155-6199.1000334

Pandey B, Agrawal M, Singh S. 2014. Coal mining activities change plant community structure due to air pollution and soil degradation. Ecotoxicology, 2014. DOI: 10.1007/s10646-014-1289-4

Pant P, Tripathi A. 2014. Impact of heavy metals on morphological and biochemical parameters of Shorea robusta plant. Ekológia (Bratislava) 33(2), 116-126. DOI:10.2478/eko-2014-0012

Paulo J, Favas J, Mayank V, D’souza R, Manoj S. 2014. Phytoremediation of soils contaminated with metals and metalloids at mining areas: potential of native flora. Biodiversity International Journal 2(4), 362-376.

Philippine Development Plan. 2011-2016. Conservation, Protection and Rehabilitation of the Environment and Natural Resources pp 308.

Primavera J. 2009. Field Guide to Philippine Mangroves.

Primavera JH, Sadaba RS, Lebata MJHL, Altamirano JP. 2004. handbook of mangroves in the Philippines – Panay. Southeast Asian Fisheries Development Center/AQD and UNESCO.

Rahman JK. 2015. Response of two crop plants to dust de-position. Zanco Journal of Pure and Applied Sciences 27(2), 1-6. DOI:10.21271/zjpas.v27i2.144

Rajeswari R, Sailaja N. 2014. Impact of heavy metals on environmental pollution. Journal of Chemical and Pharmaceutical Sciences 3, 175-181. Retrieved from /Special%20issue3/42%20jchps%20si3%20addn%20sailaja%20175-181.pdf

Rathor G, Chopra N Adhikari T. 2014. Nickel as a pollutant and its management. International Research Journal of Environment Sciences 3(10), 94-98. Retrieved from /Archive/v3/i10/15.ISCA-IRJEvS-2014-189.pdf

Razzaq. 2017. Phytoremediation: an environmental friendly technique – a review. Journal of Environmental Analytical Chemistry 4(2), 1-4. DOI: 10.4172/2380-2391.1000195

Reeves RD. 2003. Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant and Soil 249, 57-65. DOI: 10.1023/A:1022572517197

Relacion PR, Sy AS, Rodas GAN, Cayanan ALC, Marcelino DRC, Sakamoto KC, Medina LR, Pabalate HD, Nacua AE, Clemente KJE. 2018. Floristic composition assessment of urban mangroves in Batasan river, Metro Manila, Philippines. AACL Bioflux 2018 11(4). Retrieved from

Rojo J. 1999. Lexicon of Philippine trees. College, Laguna, Philippines: Forest Products Research and Development Institute.

Romero-Freire A, Olmedo-Cobo JA, Gómez-Zotano J. 2018. Elemental concentration in serpentinitic soils over ultramafic bedrock in Sierra Bermeja (Southern Spain). Minerals 2018 8, 1-14. DOI: 10.3390/min8100447

Ronald E. 1998. Nickel hazards to fish, wildlife, and invertebrates: a synoptic review. Contaminant Hazard Reviews (Report No. 34). Retrieved from United States Geological Survey website:

Sadeghi A, Etemadi N, Shams M, Niazmand F. 2015. Effects of drought stress on morphological and physiological characteristics of Festuca arundinacea and Agropyron desertorum. Horticultural Science 28(4), 544-553. DOI: 10.1800/10483476.2015.752347

Sáez-Plaza P, Navas M, Wybraniec S, Michałowski T, Garcia Asuero A. 2013. An overview of the kjeldahl method of nitrogen determination. Part II. Sample preparation, working scale, instrumental finish, and quality control. Critical Reviews in Analytical Chemistry 43, 224-272. DOI: 10.1080/10408347.2012.751787

Salem M, Mercer E. 2012. The economic value of mangroves: a meta-analysis. Sustainability 4, 359-383; DOI: 10.3390/su4030359

Sintayehu DW. 2018. Impact of climate change on biodiversity and associated key ecosystem services in Africa: a systematic review. Ecosystem Health and Sustainability 4(9), 225-239.

Solmaz I, Sari N, Dasgan H, Aktas H, Yetisir H, Unlu H. 2013. The effect of salinity on stomata and leaf characteristics of dihaploid melon lines and their hybrids. Journal of Food, Agriculture and Environment 9(3), 172-176.

Spiegel J, Maystre L. 2011. Environmental pollution control and prevention. Encyclopaedia of Occupational Health and Safety 4th Edition.

Stammer AJ. 2015. Plant tissue analysis to assess phosphorus and potassium nutritional status of corn and soybean in Iowa (Thesis). Iowa state University, Iowa, United States of America.

Suarez N, Medina E. 2005. Salinity effect on plant growth and leaf demography of the mangrove, Avicennia germinans L. Trees 19, 722-728. DOI: 10.1007/s00468-005-0001-y

Den Berg M, Zar H, Landrigan PJ. 2016. Environmental pollution: an under-recognized threat to children’s health, especially in low- and middle-income countries. Environ Health Perspect 124(3). DOI: 10.1289/ehp.1510517

Taherdoost H. 2016. Sampling methods in research methodology; how to choose a sampling technique for research. International Journal of Academic Research in Management 5, 18-27. DOI: 10.2139/ssrn.3205035

Talule & Naik. 2014. Impacts of indiscriminate mining on agriculture and biodiversity in the state of Goa in India. Universal Journal of Agricultural Research 2(6), 211-215. DOI: 10.13189/ujar.2014.02

Tan KH. 2007. Mangrove plant diversity in the southeast and East Asia. A presentation shown during the UNEP/GEF SCS Project Training Course on Sustainable Mangrove Management. 25 April – 8 May 2007, Penang, Malaysia.

Tangahu B, Abdullah S, Basri H, Idris M, Anuar N, Mukhlisin M. 2011. Review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. International Journal of Chemical Engineering 2011, 1-31. DOI:10.1155/2011/939161

Traiser C, Klotz S, Uhl D, Mosbrugger V. 2005. Environmental signals from leaves – a physiognomic analysis of European vegetation. New Phytol 166(2), 46-484. DOI: 10.1111/j.1469-8137.2005.01316.x

Tundermann J, Tien J, Howson T. 2005. Nickel and nickel alloys. In: Kirk-Othmer Encyclopedia of Chemical Technology. Volume 17. (online edition)

Ugwu E, Nwadinigwe A, Agbo B. 2019. Phytoremediation of heavy metals in spent engine oil polluted soil by Senna alata L. bioRxiv 2019, 1-20. DOI:

UNEP-WCMC. 2014. Biodiversity A-Z website: www., UNEP-WCMC, Cambridge, UK.

Van der Ent A, Jaffré T, L’Huillier L, Gibson N, Reeves RD. 2015. The flora of ultramafic soils in the Australia–Pacific Region: state of knowledge and research priorities. Australian Journal of Botany. DOI: 10.1071/BT15038

Vidya P, Patil RK. 2016. Heavy metal distribution in mangrove sediment cores from selected sites along western coast off India. Journal of Threatened Taxa 8(11), 9356-9364. htp://

Villarin JT, Algo JL, Cinco TA, Cruz FT, De Guzman RG, Hilario FD, Narisma GT, Ortiz AM, Siringan FP, Tibig LV. 2016. 2016 Philippine Climate Change Assessment (PhilCCA): The Physical Science Basis. The Oscar M. Lopez Center for Climate Change Adaptation and Disaster Risk Management Foundation Inc. and Climate Change Commission.

WHO. 2014. Global Health Observatory (GHO) Data Repository. Estimated Deaths, Data by Region. Geneva: World Health Organization. Retrieved from 14117

Widyastuti A, Yani E, Nasution E, Kolya R. 2018. Diversity of mangrove vegetation and carbon sink estimation of Segara Anakan Mangrove Forest, Cilacap, Central Java, Indonesia. Biodiversitas 19(1), 246-252. DOI: 10.13057/biodiv/d190133

Xiaolu Y, Miao L, Jingqiu Z, Jinting G, Wen W. 2018. How human activities affect heavy metal contamination of soil and sediment in a long-term reclaimed area of the Liaohe River Delta, North China. Sustainability 2018(10), 1-19. DOI: 10.3390/su10020338