Stocktake Sale on now: wide range of books at up to 70% off!
Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

A new morphological marker of the effects of acid rain in the tropics on the stem of Libidibia ferrea var. leiostachya (Leguminosae–Caesalpinioideae)

Guilherme Carvalho Andrade https://orcid.org/0000-0002-7970-9551 and Luzimar Campos Silva https://orcid.org/0000-0003-1100-988X *
+ Author Affiliations
- Author Affiliations

A Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, MG, Brazil.

* Correspondence to: luzimar@ufv.br

Handling Editor: Lynda Prior

Australian Journal of Botany 69(8) 491-499 https://doi.org/10.1071/BT21027
Submitted: 26 February 2021  Accepted: 5 July 2021   Published: 21 September 2021

© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Some of the largest remaining fragments of the Atlantic rainforest are affected by acid rain. Knowing the responses of its native plant species to acidity may be crucial to use them as bioindicators in affected areas. We tested the effects of pH 3.0 simulated acid rain on the stem of Libidibia ferrea (Mart. ex Tul.) L.P. Queiroz var. leiostachya (Benth.) L.P. Queiroz (ironwood, “pau-ferro”). Visual symptomatology consisted in dark spots on the stem that initiated on and irradiated from lenticels. As they grew larger, adjacent spots coalesced, conferring a blackened aspect to a large extension of the organ. Anatomically, the damage started with hypertrophy and increased accumulation of phenolic compounds in the outermost cell layers of the young, still subepidermal cork, which is what conferred the blackened aspect to the stem. In addition, epidermal cells showed turgor loss and ultimately collapsed, resulting in alteration of cell shape and a consequent alteration of epidermal relief. The stem of L. ferrea var. leiostachya was shown to be a more sensitive organ to the impacts of acid rain than the leaf. The dark spots visualised on the stem may be a promising macroscopic marker to be used in the biomonitoring of acid rain.

Keywords: acid rain, acidity, bioindicators, biomarker, biomonitoring, plant anatomy, pollution, stem necrosis.


References

Ahmad SH, Reshi Z, Ahmad J, Iqbal M (2005) Morpho-anatomical responses of Trigonella foenum graecum Linn. to induced cadmium and lead stress. Journal of Plant Biology 48, 64–84.
Morpho-anatomical responses of Trigonella foenum graecum Linn. to induced cadmium and lead stress.Crossref | GoogleScholarGoogle Scholar |

Alves ES, Moura BB, Pedroso ANV, Tresmondi F, Machado SR (2016) Cellular markers indicative of ozone stress on bioindicator plants growing in a tropical environment. Ecological Indicators 67, 417–424.
Cellular markers indicative of ozone stress on bioindicator plants growing in a tropical environment.Crossref | GoogleScholarGoogle Scholar |

Andrade GC, Silva LC (2017) Responses of tropical legumes from the Brazilian Atlantic Rainforest to simulated acid rain. Protoplasma 254, 1639–1649.
Responses of tropical legumes from the Brazilian Atlantic Rainforest to simulated acid rain.Crossref | GoogleScholarGoogle Scholar | 27933452PubMed |

Andrade GC, Castro LN, Silva LC (2020) Micromorphological alterations induced by simulated acid rain on the leaf surface of Joannesia princeps Vell. (Euphorbiaceae). Ecological Indicators 116, 106526
Micromorphological alterations induced by simulated acid rain on the leaf surface of Joannesia princeps Vell. (Euphorbiaceae).Crossref | GoogleScholarGoogle Scholar |

Anjos TBO, Louback E, Azevedo AA, Silva LC (2018) Sensibility of Spondias purpurea L. (Anacardiaceae) exposed to fluoride-simulated fog. Ecological Indicators 90, 154–163.
Sensibility of Spondias purpurea L. (Anacardiaceae) exposed to fluoride-simulated fog.Crossref | GoogleScholarGoogle Scholar |

Batool R, Hameed M, Ashraf M, Fatima S, Nawaz T, Ahmad MSA (2014) Structural and functional response to metal toxicity in aquatic Cyperus alopecuroides Rottb. Limnologica 48, 46–56.
Structural and functional response to metal toxicity in aquatic Cyperus alopecuroides Rottb.Crossref | GoogleScholarGoogle Scholar |

Castro PS, Ribeiro JC, Ribeiro GA, Soares VP, Barros NF, Gomes LCL, Neves JCL, Souza AL, Galvão DM, Valente OF (1987) Preliminary studies on the chemical composition of the precipitation in the Rio Doce Valley industrial region, Minas Gerais state, Brazil. Final report. (SIF/IBDF: Viçosa, MG, Brazil) [in Portuguese]

Debnath B, Ahammed GJ (2020) Effect of acid rain on plant growth and development: physiological and molecular interventions. In ‘Contaminants in agriculture – sources, impacts and management’. (Eds M Naeem, AA Ansari, SS Gill) pp. 103–114. (Springer Nature: Cham, Switzerland)

De Mello Lemos MC (1998) The politics of pollution control in Brazil: state actors and social movements cleaning up Cubatão. World Development 26, 75–87.
The politics of pollution control in Brazil: state actors and social movements cleaning up Cubatão.Crossref | GoogleScholarGoogle Scholar |

de Vasconcellos TJ, Cunha M, Callado CH (2017) A comparative study of cambium histology of Ceiba speciosa (A. St.-Hil.) Ravenna (Malvaceae) under urban pollution. Environmental Science and Pollution Research 24, 12049–12062.
A comparative study of cambium histology of Ceiba speciosa (A. St.-Hil.) Ravenna (Malvaceae) under urban pollution.Crossref | GoogleScholarGoogle Scholar | 26739992PubMed |

Dickison WC (2000) ‘Integrative plant anatomy.’ (Academic Press: San Diego, CA, USA)

Domingos M, Bulbovas P, Camargo CZS, Aguiar-Silva C, Brandão SE, Dafre-Martinelli M, Dias APL, Engela MRGS, Gagliano J, Moura BB, Alves ES, Rinaldi MCS, Gomes EPC, Furlan CM, Figueiredo AMG (2015) Searching for native tree species and respective potential biomarkers for future assessment of pollution effects on the highly diverse Atlantic Forest in SE-Brazil. Environmental Pollution 202, 85–95.
Searching for native tree species and respective potential biomarkers for future assessment of pollution effects on the highly diverse Atlantic Forest in SE-Brazil.Crossref | GoogleScholarGoogle Scholar | 25818087PubMed |

Douchiche O, Chaïbi W, Morvan C (2012) Cadmium tolerance and accumulation characteristics of mature flax, cv. hermes: contribution of the basal stem compared to the root. Journal of Hazardous Materials 235–236, 101–107.
Cadmium tolerance and accumulation characteristics of mature flax, cv. hermes: contribution of the basal stem compared to the root.Crossref | GoogleScholarGoogle Scholar | 22858130PubMed |

Evans LS (1984) Botanical aspects of acidic precipitation. The Botanical Review 50, 449–490.
Botanical aspects of acidic precipitation.Crossref | GoogleScholarGoogle Scholar |

Evans LS, Gmur NF, Costa F (1977) Leaf surface and histological perturbations of leaves of Phaseolus vulgaris and Helianthus annuus after exposure to simulated acid rain. American Journal of Botany 64, 903–913.
Leaf surface and histological perturbations of leaves of Phaseolus vulgaris and Helianthus annuus after exposure to simulated acid rain.Crossref | GoogleScholarGoogle Scholar |

Gbaguidi AE, Wang Z, Wang W, Yang T, Chen H-S (2018) Source tagging modeling study of regional contributions to acid rain in summer over Liaoning Province, Northeastern China. Environmental Pollution 235, 780–790.
Source tagging modeling study of regional contributions to acid rain in summer over Liaoning Province, Northeastern China.Crossref | GoogleScholarGoogle Scholar | 29353797PubMed |

Groh B, Hübner C, Lendzian KJ (2002) Water and oxygen permeance of phellems isolated from trees: the role of waxes and lenticels. Planta 215, 794–801.
Water and oxygen permeance of phellems isolated from trees: the role of waxes and lenticels.Crossref | GoogleScholarGoogle Scholar | 12244445PubMed |

Huang J, Wang H, Zhong Y, Huang J, Fu X, Wang L, Teng W (2019) Growth and physiological response of an endangered tree, Horsfieldia hainanensis Merr., to simulated sulfuric and nitric acid rain in southern China. Plant Physiology and Biochemistry 144, 118–126.
Growth and physiological response of an endangered tree, Horsfieldia hainanensis Merr., to simulated sulfuric and nitric acid rain in southern China.Crossref | GoogleScholarGoogle Scholar | 31563092PubMed |

Karnovsky MJ (1965) A formaldehyde–glutaraldehyde fixative of high osmolarity for use in electron microscopy. The Journal of Cell Biology 27, 137A–138A.

Kerstiens G (1994) Air pollutants and plant cuticles: mechanisms of gas and water transport, and effects on water permeability. In ‘Air pollutants and the leaf cuticle’. (Eds KE Percy, JN Cape, R Jagels, CJ Simpson) pp. 39–53. (Springer-Verlag: Berlin, Germany)

Kerstiens G (1996) Barrier properties of the cuticle to water, solutes and pest and pathogen penetration in leaves of plants grown in polluted atmospheres. In ‘Plant responses to air pollution’. (Eds M Yunus, M Iqbal) pp. 167–178. (Wiley: Chichester, UK)

Klumpp A, Klumpp G, Domingos M (1994) Plants as bioindicators of air pollution at the Serra do Mar near the industrial complex of Cubatão, Brazil. Environmental Pollution 85, 109–116.
Plants as bioindicators of air pollution at the Serra do Mar near the industrial complex of Cubatão, Brazil.Crossref | GoogleScholarGoogle Scholar | 15091691PubMed |

Kurczyńska EU, Dmuchowski W, Włoch W, Bytnerowicz A (1997) The influence of air pollutants on needles and stems of scots pine (Pinus sylvestris L.) trees. Environmental Pollution 98, 325–334.
The influence of air pollutants on needles and stems of scots pine (Pinus sylvestris L.) trees.Crossref | GoogleScholarGoogle Scholar |

Kurczyńska EU, Bastrup-Birk A, Mortensen L (1998) Influence of ozone and soil nitrogen content on the stem anatomy of Norway spruce saplings grown in open-top chambers. Environmental and Experimental Botany 40, 113–121.
Influence of ozone and soil nitrogen content on the stem anatomy of Norway spruce saplings grown in open-top chambers.Crossref | GoogleScholarGoogle Scholar |

Lendzian KJ (2006) Survival strategies of plants during secondary growth: barrier properties of phellems and lenticels towards water, oxygen, and carbon dioxide. Journal of Experimental Botany 57, 2535–2546.
Survival strategies of plants during secondary growth: barrier properties of phellems and lenticels towards water, oxygen, and carbon dioxide.Crossref | GoogleScholarGoogle Scholar | 16820395PubMed |

Louback E, Pereira TAR, Souza SR, Oliveira JA, Silva LC (2016) Vegetation damage in the vicinity of an aluminum smelter in Brazil. Ecological Indicators 67, 193–203.
Vegetation damage in the vicinity of an aluminum smelter in Brazil.Crossref | GoogleScholarGoogle Scholar |

Martins RSL, Abessa DMS, Fornaro A, Borrely SI (2014) Rainwater toxicity and contamination study from São Paulo metropolitan region, Brazil. Environmental Monitoring and Assessment 186, 1183–1194.
Rainwater toxicity and contamination study from São Paulo metropolitan region, Brazil.Crossref | GoogleScholarGoogle Scholar |

Moura BB, Alves ES, Marabesi MA, Souza SR, Schaub M, Vollenweider P (2018) Ozone affects leaf physiology and causes injury to foliage of native tree species from the tropical Atlantic Forest of southern Brazil. Science of the Total Environment 610–611, 912–925.
Ozone affects leaf physiology and causes injury to foliage of native tree species from the tropical Atlantic Forest of southern Brazil.Crossref | GoogleScholarGoogle Scholar |

O’Brien TP, Feder N, Mccully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59, 368–373.

Qu Y, An J, He Y, Zheng J (2016) An overview of emissions of SO2 and NOx and the long-range transport of oxidised sulfur and nitrogen pollutants in East Asia. Journal of Environmental Sciences 44, 13–25.
An overview of emissions of SO2 and NOx and the long-range transport of oxidised sulfur and nitrogen pollutants in East Asia.Crossref | GoogleScholarGoogle Scholar |

Rodrigues DA, Sales JF, Vasconcelos-Filho SC, Rodrigues AA, Costa AC, Rodrigues CL, Silva FHL, Müller C (2020a) Spondias mombin, a potential bioindicator of potassium fluoride pollution. Ecological Indicators 114, 106314
Spondias mombin, a potential bioindicator of potassium fluoride pollution.Crossref | GoogleScholarGoogle Scholar |

Rodrigues DA, Sales JF, Vasconcelos Filho SC, Rodrigues AA, Teles EMG, Costa AC, Reis EL, Silva TAC, Müller C (2020b) Bioindicator potential of Ricinus communis to simulated rainfall containing potassium fluoride. PeerJ 8, e9445
Bioindicator potential of Ricinus communis to simulated rainfall containing potassium fluoride.Crossref | GoogleScholarGoogle Scholar | 32676226PubMed |

Rodríguez-Sánchez VM, Rosas U, Calva-Vásquez G, Sandoval-Zapotitla E (2020) Does acid rain alter the leaf anatomy and photosynthetic pigments in urban trees? Plants 9, 862
Does acid rain alter the leaf anatomy and photosynthetic pigments in urban trees?Crossref | GoogleScholarGoogle Scholar |

Sant’Anna-Santos BF, Silva LC, Azevedo AA, Aguiar R (2006a) Effects of simulated acid rain on leaf anatomy and micromorphology of Genipa americana L. (Rubiaceae). Brazilian Archives of Biology and Technology 49, 313–321.
Effects of simulated acid rain on leaf anatomy and micromorphology of Genipa americana L. (Rubiaceae).Crossref | GoogleScholarGoogle Scholar |

Sant’Anna-Santos BF, Silva LC, Azevedo AA, Araújo JM, Alves EF, Silva EAM, Aguiar R (2006b) Effects of simulated acid rain on the foliar micromorphology and anatomy of tree tropical species. Environmental and Experimental Botany 58, 158–168.
Effects of simulated acid rain on the foliar micromorphology and anatomy of tree tropical species.Crossref | GoogleScholarGoogle Scholar |

Santana BVN, Araújo TO, Andrade GC, Freitas-Silva L, Kuki KN, Pereira EG, Azevedo AA, Silva LC (2014) Leaf morphoanatomy of species tolerant to excess iron and evaluation of their phytoextraction potential. Environmental Science and Polluttion Research 21, 2550–2562.
Leaf morphoanatomy of species tolerant to excess iron and evaluation of their phytoextraction potential.Crossref | GoogleScholarGoogle Scholar |

Schönherr J, Ziegler H (1980) Water permeability of Betula periderm. Planta 147, 345–354.
Water permeability of Betula periderm.Crossref | GoogleScholarGoogle Scholar | 24311086PubMed |

Silva LC, Azevedo AA, Silva EAM, Oliva MA (2000) Fluoride in simulated rain: Symptomatology and effects on leafstructure and on growth of woody plants. Brazilian Journal of Botany 23, 383–391.
Fluoride in simulated rain: Symptomatology and effects on leafstructure and on growth of woody plants.Crossref | GoogleScholarGoogle Scholar |

Silva LC, Azevedo AA, Silva EAM, Oliva MA (2005a) Effects of simulated acid rain on the growth of five Brazilian tree species and anatomy of the most sensitive species (Joannesia princeps). Australian Journal of Botany 53, 789–796.
Effects of simulated acid rain on the growth of five Brazilian tree species and anatomy of the most sensitive species (Joannesia princeps).Crossref | GoogleScholarGoogle Scholar |

Silva LC, Oliva MA, Azevedo AA, Araújo JM, Aguiar RM (2005b) Micromorphological and anatomical alterations caused by simulated acid rain in Restinga plants: Eugenia uniflora and Clusia hilariana. Water, Air, & Soil Pollution 168, 129–143.
Micromorphological and anatomical alterations caused by simulated acid rain in Restinga plants: Eugenia uniflora and Clusia hilariana.Crossref | GoogleScholarGoogle Scholar |

Silva LC, Freitas-Silva L, Rocha DI, Pereira JSC, Assis DEF (2020) Leaf morpho-anatomical structure determines differential response among Restinga species exposed to emissions from an iron ore pelletizing plant. Water, Air, & Soil Pollution 231, 152
Leaf morpho-anatomical structure determines differential response among Restinga species exposed to emissions from an iron ore pelletizing plant.Crossref | GoogleScholarGoogle Scholar |

Tyagi K, Sharma S, Rashmi R, Kumar S, Khair S (2013) A comparative study of histo-pharmacognosy of Chenopodium album Linn. under the impact of bicycle industry effluent. Journal of Pharmacy Research 6, 667–673.
A comparative study of histo-pharmacognosy of Chenopodium album Linn. under the impact of bicycle industry effluent.Crossref | GoogleScholarGoogle Scholar |

Vieira-Filho MS, Lehmann C, Fornaro A (2015) Influence of local sources and topography on air quality and rainwater composition in Cubatão and São Paulo, Brazil. Atmospheric Environment 101, 200–208.
Influence of local sources and topography on air quality and rainwater composition in Cubatão and São Paulo, Brazil.Crossref | GoogleScholarGoogle Scholar |

Vollenweider P, Günthardt-Goerg MS, Menard T, Baumgarten M, Matyssek R, Schaub M (2019) Macro- and microscopic leaf injury triggered by ozone stress in beech foliage (Fagus sylvatica L.). Annals of Forest Science 76, 71
Macro- and microscopic leaf injury triggered by ozone stress in beech foliage (Fagus sylvatica L.).Crossref | GoogleScholarGoogle Scholar |

Wali B, Iqbal M, Mahmooduzzafar (2007) Anatomical and functional responses of Calendula officinalis L. to SO2 stress as observed at different stages of plant development. Flora 202, 268–280.
Anatomical and functional responses of Calendula officinalis L. to SO2 stress as observed at different stages of plant development.Crossref | GoogleScholarGoogle Scholar |

Wei H, Liu W, Zhang J, Qin Z (2017) Effects of simulated acid rain on soil fauna community composition and their ecological niches. Environmental Pollution 220, 460–468.
Effects of simulated acid rain on soil fauna community composition and their ecological niches.Crossref | GoogleScholarGoogle Scholar | 27697382PubMed |

Zhang C, Yi X, Gao X, Wang M, Shao C, Lv Z, Chen J, Liu Z, Shen C (2020a) Physiological and biochemical responses of tea seedlings (Camellia sinensis) to simulated acid rain conditions. Ecotoxicology and Environmental Safety 192, 110315
Physiological and biochemical responses of tea seedlings (Camellia sinensis) to simulated acid rain conditions.Crossref | GoogleScholarGoogle Scholar | 32058162PubMed |

Zhang C, Yi X, Zhou F, Gao X, Wang M, Chen J, Huang J, Shen C (2020b) Comprehensive transcriptome profiling of tea leaves (Camellia sinensis) in response to simulated acid rain. Scientia Horticulturae 272, 109491
Comprehensive transcriptome profiling of tea leaves (Camellia sinensis) in response to simulated acid rain.Crossref | GoogleScholarGoogle Scholar |

Zhou X, Xu Z, Liu W, Wu Y, Zhao T, Jiang H, Zhang X, Zhang J, Zhou L, Wang Y (2019) Chemical composition of precipitation in Shenzhen, a coastal mega-city in South China: influence of urbanisation and anthropogenic activities on acidity and ionic composition. Science of the Total Environment 662, 218–226.
Chemical composition of precipitation in Shenzhen, a coastal mega-city in South China: influence of urbanisation and anthropogenic activities on acidity and ionic composition.Crossref | GoogleScholarGoogle Scholar |

Zobel AM (1996) Phenolic compounds in defense against air pollution. In ‘Plant response to air pollution’. (Eds M Yunus, M Iqbal) pp. 241–266. (Wiley: Chichester, UK)

Zobel A, Nighswander JE (1991) Accumulation of phenolic compounds in the necrotic areas of Austrian and red pine needles after spraying with sulphuric acid: a possible bioindicator of air pollution. New Phytologist 117, 565–574.
Accumulation of phenolic compounds in the necrotic areas of Austrian and red pine needles after spraying with sulphuric acid: a possible bioindicator of air pollution.Crossref | GoogleScholarGoogle Scholar |