Skip to main content
SpringerLink
Log in

Ecotoxicological effects of heavy metal bioaccumulation in two trophic levels

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The pollution generated by the heavy metals (HM) contained in mining wastes (tailings) is a worldwide recognized environmental concern. Due to the persistence, toxicity, bioaccumulation, and biomagnification capacity through the food chains, the release of HM into the environment causes negative effects on human health and the ecosystems. Wigandia urens Kunth (Boraginaceae) is a plant species that naturally establishes and grows in tailings and is consumed by the grasshopper Sphenarium purpurascens Charpentier (Orthoptera: Pyrgomorphidae). HM accumulation in this plant and their subsequent consumption by defoliating insects allow these contaminants to enter the food webs and favor their biomagnification. This study evaluated the effect of HM bioaccumulation in the leaf tissue of W. urens on the characteristics associated with its physical defense against herbivores and the effect of HM exposure on population parameters of grasshoppers through their ontogeny under controlled conditions. The results showed a significant increase in leaf hardness and in the number of simple and glandular trichomes in the leaves of W. urens growing on mine tailing substrate compared to those grown on the control substrate without HM. W. urens individuals growing on mine tailing substrate presented the following heavy metal foliar bioaccumulation pattern: Fe > Zn > Pb > Cu. These metals were also bioaccumulated in individuals of S. purpurascens fed with leaves of the plants exposed to mine tailings, observing differences in their concentration pattern through ontogeny. Grasshoppers fed on leaf tissue containing HM showed higher mortality in the first two developmental instars and lower body biomass throughout their ontogeny in comparison to the individuals fed on leaf tissue of plants growing on the control treatment without HM. In conclusion, W. urens is a species with phytoremediation potential for soils contaminated with HM, since it is naturally established in contaminated sites, has a wide geographic distribution, and bioaccumulates significant amounts of different HM. Furthermore, as was observed in this report, the W. urens physical and chemical defense against herbivores was enhanced by HM exposure, compromising the fitness and development of the herbivore S. purpurascens through its ontogeny and thus interrupting the entry and transfer of heavy metal through the food chain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

Please contact author for data request.

References

  • Al-Dhafar Z, Sharaby A (2012) Effect of zinc sulfate against the red palm weevil rhynchophorus ferrugineus with reference to their histological changes on the larval midgut and adult reproductive system. J Agric Sci Technol 888–900

  • Ali H, Khan E (2018) What are heavy metals? Long-standing controversy over the scientific use of the term “heavy metals” – proposal of a comprehensive definition. Toxicol Environ Chem 100:6–19. https://doi.org/10.1080/02772248.2017.1413652

    Article  CAS  Google Scholar 

  • Ali S, Ullah MI, Saeed MF et al (2019) Heavy metal exposure through artificial diet reduces growth and survival of Spodoptera litura (Lepidoptera: Noctuidae). Environ Sci Pollut Res 26:14426–14434. https://doi.org/10.1007/s11356-019-04792-0

    Article  CAS  Google Scholar 

  • Alia N, Sardar K, Said M et al (2015) Toxicity and bioaccumulation of heavy metals in spinach (Spinacia oleracea) grown in a controlled environment. Int J Environ Res Public Heal 12:7400–7416. https://doi.org/10.3390/ijerph120707400

    Article  CAS  Google Scholar 

  • Amadio ME, Pietrantuono AL, Lozada M, Fernández-Arhex V (2020) Effect of plant nutritional traits on the diet of grasshoppers in a wetland of Northern Patagonia. Int J Pest Manag 67:1–10. https://doi.org/10.1080/09670874.2020.1766156

    Article  Google Scholar 

  • Aquino-Olmeda TS (2015) Efecto de la temperatura y humedad en el ciclo biológico del chapulín Sphenarium purpurascens Charpentier. Dissertation, Instituto Politécnico Nacional, Mexico

  • Baghban A, Sendi JJ, Zibaee A, Khosravi R (2014) Effect of heavy metals (Cd, Cu, and Zn) on feeding indices and energy reserves of the cotton boll worm Helicoverpa armigera Hübner (Lepidoptera: Noctuidae). J Plant Prot Res 54:367–373. https://doi.org/10.2478/jppr-2014-0055

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Behemer ST, Lloyd CM, Raubenheimer D et al (2005) Metal hyperaccumulation in plants: mechanisms of defense against insect herbivores. Funct Ecol 19:55–66. https://doi.org/10.1146/annurev-arplant-042809-112156

    Article  CAS  Google Scholar 

  • Berner D, Blanckenhorn WU, Körner C (2005) Grasshoppers cope with low host plant quality by compensatory feeding and food selection: N limitation challenged. Oikos 111:525–533. https://doi.org/10.1111/j.1600-0706.2005.14144.x

    Article  Google Scholar 

  • Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448. https://doi.org/10.1016/j.tree.2005.05.001

    Article  Google Scholar 

  • Boyd RS (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293:153–176. https://doi.org/10.1007/s11104-007-9240-6

    Article  CAS  Google Scholar 

  • Boyd RS (2012) Plant defense using toxic inorganic ions: Conceptual models of the defensive enhancement and joint effects hypotheses. Plant Sci 195:88–95. https://doi.org/10.1016/j.plantsci.2012.06.012

    Article  CAS  Google Scholar 

  • Boyd RS, Martens SN (1992) The raison d’etre for metal hyperaccumulation by plants. In: Proctor J, Reeves R (eds) The Vegetation of ultramafic (Serpentine) soils. Intercept, GB-Andover: pp 279–289

  • Boyd RS, Moar WJ (1999) The defensive function of Ni in plants: response of the polyphagous herbivore Spodoptera exigua (Lepidoptera: Noctuidae) to hyperaccumulator and accumulator species of Streptanthus (Brassicaceae). Oecologia 118:218–224. https://doi.org/10.1007/s004420050721

    Article  Google Scholar 

  • Cano-Santana Z (1987) Ecología de la relación entre Wigandia urens y sus herbívoros en el Pedregal de San Angel, D. F (México). Dissertation, Universidad Nacional Autónoma de México, Mexico

  • Cano-Santana Z (1994). Flujo de energía a través de Sphenarium purprascens (Orthoptera: Acrididae) y productividad primaria neta áerea en una comunidad xerófita. Dissertation, Universidad Nacional Autónoma de México, Mexico

  • Cano-Santana Z (1997) Identificación de los estadios de desarrollo de Sphenarium purpurascens Charpentier (Orthoptera: Pyrgomorphidae) por el tamaño de su cabeza. Folia Entom Mex 100:65–66

    Google Scholar 

  • Cano-Santana Z, Oyama K (1992) Variation in leaf trichomes and nutrients of Wigandia urens (Hydrophyllaceae) and its implications for herbivory. Oecologia 92:405–409. https://doi.org/10.1007/BF00317467

    Article  Google Scholar 

  • Cano-Santana Z, Oyama K (1994) Wigandia urens (Hydrophyllaceae): Un mosaico de recursos para sus insectos herbívoros. Acta Bot Mex 28:29–39

    Article  Google Scholar 

  • Castañeda-Espinoza J, Salinas-Sánchez DO, Mussali-Galante P, et al (2022) Dodonaea viscosa (Sapindaceae) as a phytoremediator for soils contaminated by heavy metals in abandoned mines. Environ Sci Pollut Res 1–21. https://doi.org/10.1007/s11356-022-22374-5

  • Castellanos-Vargas I, Cano-Santana Z (2009) Historia natural y ecología de Sphenarium purpurascens (Orthoptera : Pyrgomorphidae). In: Lot A and Cano-Santana Z (eds) Biodiversidad del ecosistema del Pedregal de San Ángel, Universidad Nacional Autónoma de México, Mexico, pp 337–346

  • Castellanos-Vargas I (2001) Ecología de la oviposición de Sphenarium purpurascens (Orthoptera: Pygomorphidae) en la Reserva del Pedregal de San Ángel, México, D.F. Dissertation, Universidad Nacional Autónoma de México, Mexico

  • Cerritos R, Cano-Santana Z (2008) Harvesting grasshoppers Sphenarium purpurascens in Mexico for human consumption: a comparison with insecticidal control for managing pest outbreaks. Crop Prot 27:473–480. https://doi.org/10.1016/j.cropro.2007.08.001

    Article  Google Scholar 

  • Chapman RF, Joern A (1990) Biology of grasshoppers. Wiley, New York

    Google Scholar 

  • Chen XQ, Zhang ZT, Liu R et al (2011) Effects of the metals lead and zinc on the growth, development, and reproduction of Pardosa astrigera (Araneae: Lycosidae). Bull Environ Contam Toxicol 86:203–207. https://doi.org/10.1007/s00128-011-0194-2

    Article  CAS  Google Scholar 

  • Cheruiyot DJ, Boyd RS, Moar WJ (2013) Exploring lower limits of plant elemental defense by cobalt, copper, nickel, and zinc. J Chem Ecol 39:666–674. https://doi.org/10.1007/s10886-013-0279-y

    Article  CAS  Google Scholar 

  • Clissold FJ (2007) The biomechanics of chewing and plant fracture: mechanisms and implications. Adv in Insect Phys 34:317–372. https://doi.org/10.1016/S0065-2806(07)34006-X

    Article  Google Scholar 

  • Cortés-Jiménez EV, Mugica-Álvarez V, González-Chávez MCA et al (2013) Natural revegetation of alkaline tailing heaps at Taxco, Guerrero, México. Int J Phytoremediation 15:127–141. https://doi.org/10.1080/15226514.2012.683208

    Article  CAS  Google Scholar 

  • Cuypers A, Remans T, Weyens N, Colpaert J (2013) Soil-plant relationships of heavy metals and metalloids. In: Alloway BJ (ed) Heavy metals in soils, 3rd edn. Springer, Dordrecht, pp 161–193

  • Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J:1–17. https://doi.org/10.1155/2015/756120

  • Eun SO, Youn HS, Lee Y (2000) Lead disturbs microtubule organization in the root meristem of Zea mays. Physiol Plant 110:357–365. https://doi.org/10.1111/j.1399-3054.2000.1100310.x

    Article  CAS  Google Scholar 

  • Fuentes-Reza A (2020) Bioacumulación de metales pesados en tejido foliar y su impacto sobre los mecanismos de defensa física: el caso de Wigandia urens. Dissertation, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, Mexico

  • Gamboa de Buen A, Orozco-Segovia A (2008) Hydrophyllaceae seeds and germination. Seed Sci Biotechnol 2:15–26

    Google Scholar 

  • Gardea-Torresdey J, Peralta-Videa J, Montes M et al (2004) Bioaccumulation of cadmium, chromium and copper by Convolvulus arvensis L.: impact on plant growth and uptake of nutritional elements. Bioresour Technol 92:229–235. https://doi.org/10.1016/j.biortech.2003.10.002

    Article  CAS  Google Scholar 

  • Ghemari C, Waterlot C, Ayari A et al (2019) Effects of heavy metals artificial contamination on Porcellio laevis (Latreille, 1804) (Crustacea: Isopoda: Oniscidea). Bull Environ Contam Toxicol 103:416–420. https://doi.org/10.1007/s00128-019-02684-0

    Article  CAS  Google Scholar 

  • Ghori N-H, Ghori T, Hayat MQ et al (2019) Heavy metal stress and responses in plants. Int J Environ Sci Technol 16:1807–1828. https://doi.org/10.1007/s13762-019-02215-8

    Article  CAS  Google Scholar 

  • Gold K, León LP, Way M (2004) Manual de recolección de semillas de plantas silvestres para conservación a largo plazo y restauración ecológica [online]. La Serena, Chile: Boletín INIA - Instituto de Investigaciones Agropecuarias. no. 110. Available from: https://hdl.handle.net/20.500.14001/7000

  • Gomes MP, de Nogueira M, OG, Castro EM de, et al (2011) Ecophysiological and anatomical changes due to uptake and accumulation of heavy metal in Brachiaria decumbens. Sci Agric 68:566–573. https://doi.org/10.1590/S0103-90162011000500009

    Article  CAS  Google Scholar 

  • Guo YG, Huang P, Zhang WG et al (2013) Leaching of heavy metals from Dexing copper mine tailings pond. Trans Nonferrous Met Soc China 23:3068–3075. https://doi.org/10.1016/S1003-6326(13)62835-6

    Article  CAS  Google Scholar 

  • Hernández-Canalla L, Olvera-Torres F, Luna-Hernández VG, Sanchez de la Luz C (2020) Diseño y determinación del valor nutritivo de una formulación de un alimento enriquecido con Sphenarium purpurascens. EDUCATECONCIENCIA 25:57–69

  • Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:1–37. https://doi.org/10.1155/2012/872875

    Article  CAS  Google Scholar 

  • Hunt JW, Dean AP, Webster RE et al (2008) A novel mechanism by which silica defends grasses against herbivory. Ann Bot 102:653–656. https://doi.org/10.1093/aob/mcn130

    Article  CAS  Google Scholar 

  • Izasa-Guzmán G (2013) Efecto del plomo sobre la inhibición, germinación y crecimiento de Phaseolus vulgaris L. y Zea mays L. Biotecnol Veg 13:1–10

    Google Scholar 

  • Jiang RF, Ma DY, Zhao FJ, McGrath SP (2005) Cadmium hyperaccumulation protects Thlaspi caerulescens from leaf feeding damage by thrips (Frankliniella occidentalis). New Phytol 167:805–814. https://doi.org/10.1111/j.1469-8137.2005.01452.x

    Article  CAS  Google Scholar 

  • Kariyat RR, Smith JD, Stephenson AG et al (2017) Non-glandular trichomes of Solanum carolinense deter feeding by Manduca sexta caterpillars and cause damage to the gut peritrophic matrix. Proceeding R Soc B 284:1–9. https://doi.org/10.1098/rspb.2016.2323

    Article  Google Scholar 

  • Koul M, Thomas L, Karmakar K (2021) Functional aspects of solanaceae trichomes in heavy metal detoxification. Nord J Bot 1–14. https://doi.org/10.1111/njb.03171

  • Llorens N, Arola L, Bladé C, Mas A (2000) Effects of copper exposure upon nitrogen metabolism in tissue cultured Vitis vinifera. Plant Sci 160:159–163. https://doi.org/10.1016/S0168-9452(00)00379-4

    Article  CAS  Google Scholar 

  • Manara A, Fasani E, Furini A, DalCorso G (2020) Evolution of the metal hyperaccumulation and hypertolerance traits. Plant Cell Environ 43:2969–2986. https://doi.org/10.1111/pce.13821

    Article  CAS  Google Scholar 

  • Manzoor J, Sharma M, Wani KA (2018) Heavy metals in vegetables and their impact on the nutrient quality of vegetables: a review. J Plant Nutr 0:1–20. https://doi.org/10.1080/01904167.2018.1462382

  • Marshall AT (1983) X-ray microanalysis of copper and sulphur-containing granules in the fat body cells of homopteran insects. Tissue Cell 15:311–315. https://doi.org/10.1016/0040-8166(83)90025-3

    Article  CAS  Google Scholar 

  • Martens SN, Boyd RS (1994) The ecological significance of nickel hyperaccumulation: a plant chemical defense. Oecologia 98:379–384. https://doi.org/10.1007/BF00324227

    Article  Google Scholar 

  • Massey F, Hartley S (2009) Physical defences wear you down: Progressive and irreversible impacts of silica on insect herbivores. J Anim Ecol 78:281–291. https://doi.org/10.1111/j.1365-2656.2008.01472.x

    Article  Google Scholar 

  • Mathews S, Ma LQ, Rathinasabapathi B, Stamps RH (2009) Arsenic reduced scale-insect infestation on arsenic hyperaccumulator Pteris vittata L. Environ Exp Bot 65:282–286. https://doi.org/10.1016/j.envexpbot.2008.09.010

    Article  CAS  Google Scholar 

  • Miura K, Ohsaki N (2004) Relationship between physical leaf characteristics and growth and survival of polyphagous grasshopper nymphs, Parapodisma subastris (Orthoptera: Catantopidae). Popul Ecol 46:179–184. https://doi.org/10.1007/s10144-004-0177-9

    Article  Google Scholar 

  • Muro-González DA, Mussali-Galante P, Valencia-Cuevas L et al (2020) Morphological, physiological, and genotoxic effects of heavy metal bioaccumulation in Prosopis laevigata reveal its potential for phytoremediation. Environ Sci Pollut Res 27:40187–40204. https://doi.org/10.1007/s11356-020-10026-5

    Article  CAS  Google Scholar 

  • Mussali-Galante P, Tovar-Sánchez E, Mahara V, Rojas E (2013) Biomarkers of exposure for assessing environmental metal pollution: From molecules to ecosystems. Rev Int Contam Ambient 29:117–140

    CAS  Google Scholar 

  • Mwangi MN, Oonincx DGAB, Stouten T et al (2018) Insects as sources of iron and zinc in human nutrition. Nutr Res Rev 31:248–255. https://doi.org/10.1017/S0954422418000094

    Article  CAS  Google Scholar 

  • Navarrete-Gutiérrez DM, Pons MN, Cuevas-Sánchez JA, Echevarria G (2018) Is metal hyperaccumulation occurring in ultramafic vegetation of central and southern Mexico? Ecol Res 33:641–649. https://doi.org/10.1007/s11284-018-1574-4

    Article  CAS  Google Scholar 

  • Nica DV, Bura M, Gergen J et al (2012) Bioaccumulative and conchological assessment of heavy metal transfer in a soil-plant-snail food chain. Chem Cent J 6:55. https://doi.org/10.1186/1752-153X-6-55

    Article  CAS  Google Scholar 

  • Nichol H, Law J, Winzerling J (2002) Iron metabolism in insects. Annu Rev Entomol 47:535–559. https://doi.org/10.1146/annurev.ento.47.091201.145237

    Article  CAS  Google Scholar 

  • Odendaal JP, Reinecke AJ (2004) Effect of metal mixtures (Cd and Zn) on body weight in terrestrial isopods. Arch Environ Contam Toxicol 46:377–384. https://doi.org/10.1007/s00244-003-2303-7

    Article  CAS  Google Scholar 

  • Orozco-Segovia A, Gamboa-deBuen A, Barradas-Miranda V (2009) La diversidad funcional del ecosistema. In: Lot A, Cano-Santana Z (eds) Biodiversidad del ecosistema del pedregal de San Ángel, 1st edn. Universidad Nacional Autónoma de México, Mexico, pp 295–316

  • Pérez-Estrada LB, Cano-Santana Z, Oyama K (2000) Variation in leaf trichomes of Wigandia urens: environmental factors and physiological consequences. Tree Physiol 20:629–632. https://doi.org/10.1093/treephys/20.9.629

    Article  Google Scholar 

  • Pourrut B, Shahid M, Dumat C et al (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–136. https://doi.org/10.1007/978-1-4419-9860-6_4

    Article  CAS  Google Scholar 

  • Raghavendra-Rao M, Acharya Y, Bala A, et al (2017) Study of heavy metals in abnormal growth and development using and alternative animal model: Heretometrus fulvipes. Int J Life Sci Sci Res 3:800–807. https://doi.org/10.21276/ijlssr.2017.3.1.9

  • Rai GK, Rai PK, Basu U et al (2021) Insights into decontamination of soils by phytoremediation: a detailed account on heavy metal toxicity and mitigation strategies. Physiol Plant 173:287–304. https://doi.org/10.1111/ppl.13433

    Article  CAS  Google Scholar 

  • Rathinasabapathi B, Rangasamy M, Froeba J et al (2007) Arsenic hyperaccumulation in the Chinese brake fern (Pteris vittata) deters grasshopper (Schistocerca americana) herbivory. New Phytol 175:363–369. https://doi.org/10.1111/j.1469-8137.2007.02099.x

    Article  CAS  Google Scholar 

  • Rebollo-Salinas D (2019) Biomagnificación de metales pesados en una cadena trófica en los jales de Huautla, Morelos. Dissertation, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, Mexico

  • Riddick EW, Simmons AM (2014) Do plant trichomes cause more harm than good to predatory insects? Pest Manag Sci 70:1655–1665. https://doi.org/10.1002/ps.3772

    Article  CAS  Google Scholar 

  • Rosas-Ramírez M (2018) Relación entre la bioacumulación de metales pesados y la concentración de clorofila en Sanvitalia procumbens. Dissertation, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, Mexico

  • Rosas-Ramírez M (2021) Fitoestabilización de metales pesados provenientes de jales. Dissertation, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, Mexico

  • Rzedowski GC de, Rzedowski (2005) Flora fanerogámica del Valle de México, 2nd edn. Instituto de Ecología, A.C. and Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Pátzcuaro Michoacán, Mexico

  • Salas-Luévano MA, Manzanares-Acuna E, Letechipia-de Leon C, Vega-Carrillo HR (2009) Tolerant and hyperaccumulators autochthonous plant species from mine tailing disposal sites. Asian J Exp Sci 23:27–32

    Google Scholar 

  • Sanabria-Urbán S, Song H, Oyama K et al (2015) Body size adaptations to altitudinal climatic variation in Neotropical grasshoppers of the genus Sphenarium (Orthoptera: Pyrgomorphidae). PlosOne 10(12):e0145248

    Article  Google Scholar 

  • Santoyo-Martínez M (2020) Estudio ecotoxicológico sobre la bioacumulación de metales pesados en dos especies vegetales asociadas a los jales de Huautla, Morelos. Dissertation, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, Mexico

  • Santoyo-Martínez M, Mussali-Galante P, Hernández-Plata I et al (2020) Heavy metal bioaccumulation and morphological changes in Vachellia campechiana (Fabaceae) reveal its potential for phytoextraction of Cr, Cu, and Pb in mine tailings. Environ Sci Pollut Res 27:11260–11276. https://doi.org/10.1007/s11356-020-07730-7

    Article  CAS  Google Scholar 

  • Schofield RMS, Nesson MH, Richardson KA (2002) Tooth hardness increases with zinc-content in mandibles of young adult leaf-cutter ants. Naturwissenschaften 89:579–583. https://doi.org/10.1007/s00114-002-0381-4

    Article  CAS  Google Scholar 

  • SENASICA-DGSV (2020) Chapulines de importancia económica en México en cultivo de frijol: Brachystola magna, Brachystola mexicana, Melanoplus differentials, Sphenarium purpurascens, Taeniopoda eques y Boopedon diabolicum (Orthoptera: Romaleidae; Acrididae; Pyrgomorphidae). Sader-Senasica. Dirección General de Sanidad Vegetal-Centro Nacional de Referencia Fitosanitaria. Ficha técnica. Tecámac, Estado de México, p 36

  • Simpson SJ (1982) Changes in the efficiency of utilisation of food throughout the fifth-instar nymphs of Locusta migratoria. Entomol Exp Appl 31:265–275. https://doi.org/10.1111/j.1570-7458.1982.tb03144.x

    Article  Google Scholar 

  • Soliman MM, El-Shazly M (2017) Bioaccumulation of heavy metals by grasshoppers and a mantid along a pollution gradient. Ecol Balk 9:7–21

    Google Scholar 

  • Solís-Miranda M (2016) Aislamiento de bacterias de jales mineros y análisis de su potencial para la remediación de sitios contaminados con metales pesados. Dissertation, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, Mexico

  • Sridhar BBM, Witter JD, Wu C, et al (2014) Effect of biosolid amendments on the metal and nutrient uptake and spectral characteristics of five vegetable plants. Water Air Soil Pollut 225–2092. https://doi.org/10.1007/s11270-014-2092-9

  • Statsoft INC (2007) STATISTICA for Windows. Tulsa, USA

  • Strong DR, Lawton JH, Southwood SR (1984) Insects on plants. Community patterns and mechanisms. Blackwell Scientific Publicatons

  • Sun HX, Dang Z, Xia Q et al (2011) The effect of dietary nickel on the immune responses of Spodoptera litura Fabricius larvae. J Insect Physiol 57:954–961. https://doi.org/10.1016/j.jinsphys.2011.04.008

    Article  CAS  Google Scholar 

  • Tang X, Zhou B (2013) Iron homeostasis in insects : Insights from Drosophila studies. IUBMB Life 65:863–872. https://doi.org/10.1002/iub.1211

    Article  CAS  Google Scholar 

  • Tovar-Sánchez E, Hernández-Plata I, Martínez MS, et al (2018) Heavy metal pollution as a biodiversity threat. Heavy Met. https://doi.org/10.5772/intechopen.74052

  • Volke-Sepúlveda T, Velasco-Trejo J, Perez D la R (2005) Suelos contaminados por metales y metaloides, 1st. edn. INE-SEMARNAT, Mexico

  • War AR, Paulraj MG, Ahmad T et al (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320

    Article  Google Scholar 

  • Wen M, Zhao H, Liu G et al (2018) Effect of zinc supplementation on growth performance, intestinal development, and intestinal barrier-related gene expression in Pekin ducks. Biol Trace Elem Res 183:351–360. https://doi.org/10.1007/s12011-017-1143-7

    Article  CAS  Google Scholar 

  • Whitman DW (2008) The significance of body size in the Orthoptera: a review. J Orthoptera Res 17:117–134. https://doi.org/10.1665/1082-6467-17.2.117

    Article  Google Scholar 

  • Woodward G, Ebenman B, Emmerson M et al (2005) Body size in ecological networks. Trends Ecol Evol 20:402–409. https://doi.org/10.1016/j.tree.2005.04.005

    Article  Google Scholar 

  • Zar J. (2010) Biostatistical analysis, 5th edn. Prentice-Hall/Pearson, Upper Saddle River

  • Zhu D, Wei Y, Zhao Y et al (2018) Heavy metal pollution and ecological risk assessment of the agriculture soil in Xunyang mining area, Shaanxi province, Northwestern China. Bull Environ Contam Toxicol 101:178–184. https://doi.org/10.1007/s00128-018-2374-9

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the support received from the postgraduate program Doctorado en Ciencias Naturales of the Universidad Autónoma del Estado de Morelos (UAEM) for the facilities granted to carry out this project.

Funding

This research was supported by a CONACyT scholarship grant to J.E.A. (Grant: 784276). Also, we thank Rosalind Pearson Hedge for her comments and English edition that improved our manuscript.

Author information

Authors and Affiliations

  1. Doctorado en Ciencias Naturales, Universidad Autónoma del Estado de Morelos, Av. Universidad 1001, Col. Chamilpa, C.P. 62209, Cuernavaca, Morelos, México

    Janeth Esteves-Aguilar

  2. Centro de Investigación en Biotecnología, Universidad Autónoma del Estado de Morelos, Av. Universidad 1001, Col. Chamilpa, C.P. 62209, Cuernavaca, Morelos, México

    Patricia Mussali-Galante & Alexis Rodríguez

  3. Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de Morelos, Av. Universidad 1001, Col. Chamilpa, C.P. 62209, Cuernavaca, Morelos, México

    Leticia Valencia-Cuevas, Alexis Ariel García-Cigarrero & María Luisa Castrejón-Godínez

  4. Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos, Av. Universidad 1001, Col. Chamilpa, C.P. 62209, Cuernavaca, Morelos, México

    Efraín Tovar-Sánchez

Authors
  1. Janeth Esteves-Aguilar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patricia Mussali-Galante
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leticia Valencia-Cuevas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexis Ariel García-Cigarrero
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexis Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. María Luisa Castrejón-Godínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Efraín Tovar-Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: ET-S; methodology, ET-S, PM-G, JE-A, AAG-C; validation: ET-S, LV-C, PM-G; formal analysis: ET-S; writing-original draft preparation: ET-S, LV-C, JE-A; writing-review and editing: ET-S, PM-G, LV-C, AR-S, MLC-G, JE-A; supervision: ET-S; all authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Efraín Tovar-Sánchez.

Ethics declarations

Ethics approval and consent to participate

The study did not violate ethics, and all participants agreed to publish the paper.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Philippe Garrigues

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Esteves-Aguilar, J., Mussali-Galante, P., Valencia-Cuevas, L. et al. Ecotoxicological effects of heavy metal bioaccumulation in two trophic levels. Environ Sci Pollut Res 30, 49840–49855 (2023). https://doi.org/10.1007/s11356-023-25804-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-023-25804-0

Keywords

Search

Navigation