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Published yearly: 

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ISSN: 2320-964X (Online) 

ISSN: 2320-7817  (Print)



Dr. Santosh Pawar 




Int. Journal of Life Sciences, 2018; 6(1): 18-28      |                 Available online, February 24, 2018

Heavy Metal Accumulation and Mycorrhizal Association of the Common Agroforestry Crops in the Ultramafic Soils of Dinagat Islands, Philippines

Aribal Lowell G, Mancile Danilo S, Marin Rico A, Bruno Angela Grace T



Central Mindanao University, Musuan, Maramag, Bukidnon,


Received : 09.11.2017   |   Accepted : 05.02.2018     |     Published : 24.02.2018

Common Agroforestry crops in the ultramafic soils of Santo Niño, Cagdianao, Dinagat Islands were studied to determine their heavy metal accumulation and mycorrhizal association. Three Agroforestry farms were sampled for the crops such as coconut, sweet potato, and banana.  On each farm, plant parts were collected separating the edible and the non-edible parts such as shoots and roots and were tested for accumulation of nickel and chromium via atomic absorption spectrophotometry.  Soil samples within the rhizosphere of the crops were also collected for mycorrhizal studies. Results showed that all Agroforestry crops accumulated nickel and chromium on roots and shoots above the normal range at 0.05-10 mg/kg, however, only banana has nickel concentration exceeding the normal range of 5-25 mg/kg.  For the edible parts, all Agroforestry crops have nickel and chromium concentration above the safety limits of 0.0028 and 0.3 mg/kg body weight per day for nickel and chromium, respectively. Only sweet potato has shoot/root quotient or translocation factor greater than one for both nickel and chromium which was 12.73 and 11.09, respectively, thus considered as hyperaccumulator species.  Six genera of mycorrhiza were identified in all crops with Glomus as the most abundant followed by Acaulospora, Scutellospora, Entrophospora, Sclerocystis, and Gigaspora. 


Keywords: Heavy metal, Agroforestry crops, ultramafic soil, mycorrhiza



Editor: Dr.Arvind Chavhan


Cite this article as:

Aribal Lowell G, Mancile Danilo S, Marin Rico A, Bruno Angela Grace T (2018) Heavy Metal Accumulation and Mycorrhizal Association of the Common Agroforestry Crops in the Ultramafic Soils of Dinagat Islands, Philippines, Int. J. of. Life Sciences, Volume 6(1): 18-28. 


Conflicts of interest: The authors stated that no conflicts of interest.



Copyright: © 2018 | Author(s), This is an open access article under the terms of the Creative Commons Attribution-Non-Commercial - No Derives License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.



Aitio A, Attfield M, Cantor K, Demers P, Fowler B., Fubini B, Gérin M, Goldberg M, Grandjean P, Hartwig A, Heinrich U, Henderson R, Ikeda  M, Infante P, Kane A, Kauppinen T, Landrigan P, Lunn R, Merletti F, Muhle H, Rossman T, Samet J, Siemiatycki J, Stayner L, Waalkes M, Ward E and Ward, J (2012) Nickel and nickel compounds. IARC monographs 100 c. World Health Organization, Lyon.

Alban JD, Altamirano RA, Batangan E, Gonzales M, Hilario MV, Narvades V and Gaerlan F (2004) Mts. Kambinliw & Redondo Loreto, Dinagat Island, Surigao del Norte: Integrating Forest Conservation With Local Governance. Quezon City, Philippines: Haribon Foundation, 20 & 72.

Allan R (2009) Soil tests & interpretation. Hill laboratories. Date Accessed: June 15, 2017.

Andersen A, Baker D, Beyersmann D, Costa M, De Flora S, Gilman JPW, Grandjean P, Gray CN, Kasprzak KS, Levy, LS, Møller Jensen O, Mottet NK, Norseth T, Peto J, Schaller K-H, Simonato L, Stern R, Sunderman EW, Swierenga S, and Tossavainen A (1990) IARC monographs on the evaluation of carcinogenic risks to humans. Chromium, nickel, and welding. World Health Organization, Lyon, 49, 257–445.

Aribal L, Marin RA, Paquit JC, and Zanoria J (2017) Abundance and distribution of arbuscular mycorrhiza in the ultramafic soils of Mt. Kiamo in Bukidnon, Philippines. International Journal of Scientific Research in Environmental Sciences, 5(2), 36-41.

Baker AJM, Proctor J, van Balgooy MMJ and Reeves RD (1992) Hyperaccumulation of Nickel by the Flora of the Ultramafics of Palawan, Republic of the Philippines. In: Baker AJM, J. Proctor and RD. Reeves (eds.), The Vegetation of Ultramafic (Serpentine) Soils: Proceedings of the First International Conference on Serpentine Ecology. Pp 291-304.

Baker AJM and Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements- a review of their distribution, ecology and phytochemistry, Biorecovery, 1, 81-126.

Becker W, and Kumpulainen J (1991) Contents of essential and toxic mineral elements in Swedish market-basket diets in 1987. British Journal of Nutrition, 66, 151–160.

Benford D, Ceccatelli S, Cottrill B, DiNovi M, Dogliotti E, Edler L, Farmer P, Fürst P, Hoogenboom L, Knutsen HK, Lundebye A-K, Metzler, M, Mutti A, Nebbia CS, O’Keeffe M, Petersen A, Rietjens I, Schrenk D, Silano V, van Loveren H, Vleminckx C and Wester P (2014) Scientific opinion on the risks to public health related to the presence of chromium in food and drinking water. EFSA Journal, 12(3): 3595, 261.


Benford D, Ceccatelli S, Cottrill B, DiNovi M, Dogliotti E, Edler L, Farmer P, Fürst P, Hoogenboom L, Knutsen HK, Lundebye A-K, Metzler M, Mutti A, Nebbia CS, O’Keeffe M, Petersen A, Rietjens, I, Schrenk D, Silano V, van Loveren H, Vleminckx C and Wester P (2015) Scientific opinion on the risks to public health related to the presence of nickel in food and drinking water. EFSA Journal, 13(2): 4002, 202. doi:10.2903/j.efsa.2015.4002

Bhalerao S, Sharma A and Poojari A  (2015) Toxicity of nickel in plants. International Journal of Pure Applied Biosciences, 3(2), 345-355.

Bouamri R, Dalpé Y, Serrhini MN and Bennani A (2006) Arbuscular mycorrhizal fungi species associated with rhizosphere of Phoenix dactylifera L. in Morocco. African Journal of Biotechnology. 5(6), 510-516.

Brooks R (1987) Serpentine & its Vegetation. Portland, Oregon. Dioscorides Press.

Brundrett M, Bougher N, Dell B, Grove T and Malajczu KN (1996) 'Working with mycorrhizas in forestry and agriculture. Australian Centre for International Agricultural Research: Canberra. 179-181.

Brundrett MC and Kendrick B (1988) The mycorrhizal status, root anatomy, and phenology of plants in a sugar maple forest. Canada Journal of Botany, 66: 1153-1173.

Carrasco L, Azcon R, Kohler J, Roldán A and Caravaca F (2011) Comparative effects of native filamentous arbuscular mycorrhizal fungi in the establishment of an autochthonous, leguminous shrub growing in a metal-contaminated soil.  Science of the Total Environment, 409 (6), 1205-1209.

Cempel M and Nickel G (2006) Nickel: A review of its sources and environmental toxicology. Polish Journal of Environmental Studies, 15, 375–382.

Chen BD, Zhu Y, Duan J, Xiao XY and Smith SE (2007) Effects of the arbuscular mycorrhizal fungus Glomus mosseae on growth and metal uptake by four plant species in copper mine tailings. Environmental Pollution Journal 147(2), 374-380.

Clarkson TW (1988) Biological monitoring of toxic metals. New York. Plenum Press. Pp 265-282. 

Committee on Medical Aspects of Food Policy (COMA) (1991) Dietary references values for food energy and nutrients for the United Kingdom. Department of Health Report 41, HMSO, London. 181-182pp.

Daniels BA and Skipper HD (1982) Methods for the recovery and quantitative estimation of propagules from soil. In: Schenck, NC (edition). Methods and principles of mycorrhizal research. The American Phytopathological Society. St. Paul. 29-35.

Dioka CE, Oresakwe OE, Adeniyi FA, and Meludu SC (2004) Liver and renal function tests in artisans occupationally exposed to lead in mechanic village in Nnewi, Nigeria. International Journal of Environmental Research and Public Health, 1, 21–25.

Duda-Choda, K and Blaszczyk U (2008) The impact of nickel on human health. Journal of Elementology, 13, 685–696.

Elmore, WC (2006) Population and identification of mycorrhizal fungi in St. Augustine grass in Florida and their effect on soil-borne Pathogens. Ph.D. Dissertation. University of Florida.

Eom AH, Hartnett DC, and Wilson GWT (2000) Host plant effects on arbuscular mycorrhizal fungal communities in tall-grass prairie. Oecologia, 122, 435-444.

Fawell JK, Grawé K, Cotruvo J, Giddings M, Jackson P, Magara Y, Ohanian E, Bartram J, Vickers C, Bos R, Ward P and Sheffer M (2007) Nickel in Drinking Water. WHO/SDE/ WSH/07.08/55. Geneva. Available at: Nickel110805.pdf

Fernando ES, MH Suh, J Lee, and DK Lee (2008) Forest Formations of the Philippines ASEAN-Korea Environmental Cooperation Unit (AKECU). GeoBook Publishing Company, 232pp.

Havel R, Calloway D, Gussow J, Mertz W and Nesheim M (1989) Recommended dietary allowances, 10th Edition. Washington, DC. National Academy Press.

Heijden VD, Klironomos MGA, Ursic JN, Moutoglis M, and Streitwolf-Engel P (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability, and productivity. Nature, 396, 69-72.

Hepper CM (1984) Isolation and culture of VA mycorrhizal (VAM) fungi. In: VA Mycorrhizae. (Eds. CL Powell, DJ Bagyaraj) CRC Press, Florida, USA, Pp 95-122.

Ianson D and Smeenk J (2014) Mycorrhizae in the Alaska landscape. Alaska: University of Alaska Fairbanks Cooperative Extension Service, Pp 1-2.

Lasat M (2000) The use of plants for the removal of toxic metals from contaminated soils, Unpublished Manuscript from the US EPA, American Association for Advancement of Sciences Fellowship Program, Pp 34.

Leblanc JC, Guerin T, Noel L, Calamassi-Tran G, Volatier  JL and Verger P (2005) Dietary exposure estimates of 18 elements from the 1st French Total Diet Study. Food Additives and Contaminants, 22, 624–641.

Lee PJ and  Koske RE (1994) Gigaspora gigantia: Seasonal, abundance, and aging of spores in a sand dune. Mycological Research Journal, 98, 453-457.

Martina J and Vosatka M (2005) Response to cadmium of Daucus carota hairy roots dual cultures with Glomus intraradices or Gigaspora margarita. Mycorrhiza 15(3), 217-224.

Morton J (1988) Taxonomy of mycorrhizal fungi: classification, nomenclature, and identification. Mycotaxon (32), 267-324.

Morton JB and Benny GL (1990) Revised classification of arbuscular mycorrhizal fungi (Zygomycetes) a new order, Glomales: A sub-order Glomenieae and Gigasporanieae and two new families Acaulosporaceae and Gigasporaceae with an emendation of Glomaceae. Mycorrhizal Taxonomy, 37, 439-448.

Noël L, Chekri R, Millour S, Vastel C, Kadar A, Sirot V, Leblanc J  and Guérin T (2012)  Li, Cr, Mn, Co, Ni, Cu, Zn, Se and Mo levels in foodstuffs from the Second French TDS. Food Chemistry, 132, 1502–1513.

Proctor J (1999) Toxins, nutrient shortages & droughts: The serpentine challenge. Trees, 14, 334-335.

Reeves RD (2015)  Hyperaccumulation of trace elements by plants. DOI:10.1007/1-4020-4688-X_2

Reeves RD and Baker AJM (2000) Phytoremediation of toxic metals: Using plants to clean up the environment. New York. John Wiley and Sons, Inc.

Regvar M, Vogel K, Irgel N, Wraber T, Hildebrandt U, Wilde P, and Bothe H (2003) Colonization of pennycresses Thalspi sp. of the Brassicaceae by arbuscular mycorrhizal fungi. Journal of Plant Physiology, 160, 615-626.

Rose M,  Baxter M, Brereton N and Baskaran C (2010) Dietary exposure to metals and other elements in the 2006 UK Total Diet Study and some trends over the last 30 years. Food Additives and Contaminant Part A, 27, 1380–1404.

Rotkittikhun R, Kruatrachue M, Chaiyarat R, Ngernsansaruay P, Pokethitiyook C, Paijitprapaporn A, Baker AJM (2006) Uptake & accumulation of lead by plants from the Bo Ngamlead mine area in Thailand. Environmental Pollution Journal, 144, 681-688.

Rusell R,  Beard J, Dunn J, Ferland G,  Hambidge KM, Lynch S, Penland J,  Ross AC, Stoeker B, Suttie J, Turnlund J, West K and Zlotkin S (2001) Chromium. In: Dietary reference intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. Panel on Micronutrients, Subcommittees on Upper Reference Levels of Nutrients and of Interpretation and Use of Dietary Reference Intakes, and the Standing Committee on the Scientific Evaluation of Dietary Reference Intakes, Food and Nutrition Board, Institute of Medicine (IOM). Washington, DC. National Academy Press (NAP), 197-223. 

Samantaray S, Rout GR and Das P (1997)  Tolerance of rice to nickel in nutrient solution. Biologia Plantarum, 40, 295– 298.

Santonen T, Zitting  A,  Riihimäki V, and Howe P (2009a) Inorganic chromium (III) compounds. Concise International Chemical Assessment Document 76. Available online: 

Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC,  Klironomos, JN,  Abbott LK and Pringle A (2006) The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecology Letters, 9, 501-515.

Shanker AK,  Cervantes C,  Loza-Tavera H and Avudainayagam S (2005) Chromium toxicity in plants. Environment International Journal, 31, 739-753.

Silva JA and Uchida R (2000) Essential nutrients for plant growth: nutrient functions and deficiency symptoms. University of Hawaii, Manoa. College of Tropical Agriculture and Human Resources, 31-55.

Seregin IV and Ivanov VB (2001) Physiological aspects of cadmium and lead toxic effects on higher plants. Russian Journal of Plant Physiology English Translation, 523–544.

Tommerup IE (1988) The vesicular-arbuscular mycorrhizas. Advances in Plant Pathology, 6, 81-91.

Turk MA, Assaf TA,  Hameed KM, and Al-Tawaha AM (2006) Significance of mycorrhizae. World Journal of Agricultural Sciences, 2(1), 16-20.

Verbruggen N, Hermans C  and  Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytologist, 181, 759-776.


Ward R (1993) Soil and irrigation water interpretation manual. 2nded. U.S.A. Hach Company.

Welch RM and Cary EE (1975) Concentration of chromium, nickel, and vanadium in plant materials. Journal of Agriculture and Food Chemistry, 23, 479-482.

Wilbur S, Abadin H, Fay M, Yu D, Tencza B, Ingerman L, Klotzbach J, James S, Beyersmann D, Wise JP and Sedman R (2012) Toxicological profile of chromium. Agency for Toxic Substances and Disease Registry, U.S. Department of Health and Human Services. Available online:

Zaefarian F, Rezvani M, Rejali F, Ardakani MR and Noormohammadi G (2010) The ability of Glomus mosseae-Alfalfa (Medicago sativa L.) association for heavy metal phytoextraction from soil.  Environmental Science Journal, 7(3), 77-90.








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