Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Plant growth-promoting bacteria as a tool to improve salinity tolerance in sweet pepper

Francisco M. del Amor A B and Paula Cuadra-Crespo A
+ Author Affiliations
- Author Affiliations

A Equipo de Calidad Alimentaria, Instituto Murciano de Investigación y Desarrollo Agrario y Alimentario (IMIDA), Calle Mayor, 30150 Murcia, Spain.

B Corresponding author. Email: franciscom.delamor@carm.es

Functional Plant Biology 39(1) 82-90 https://doi.org/10.1071/FP11173
Submitted: 19 May 2011  Accepted: 21 September 2011   Published: 7 November 2011

Abstract

To characterise the effect of bacterial inoculants (Azospirillum brasilense and Pantoea dispersa) on the response of sweet pepper (Capsicum annuum L.) to saline stress, plants were exposed to 0, 40, 80 and 120 mM NaCl in solution. The effect on plant growth; leaf gas exchange; NO3, Cl, K+ and Na+ accumulation; and chlorophyll fluorescence and content were investigated. Total plant DW was reduced significantly by salinity but when inoculants were applied, DW was increased. Inoculated plants showed higher DW accumulation in the roots. Salinity levels up to 80 mM NaCl did not affect the net assimilation rate in inoculated plants but 40 mM NaCl was enough to reduce this parameter in non-inoculated plants. The leaf area ratio was not modified substantially by inoculation. The leaf Cl concentration of inoculated plants was reduced at the highest salinity, compared with control plants, and NO3 concentration increased markedly. A higher K+ : Na+ ratio was found in inoculated plants. Leaf photosynthesis and stomatal conductance were impaired significantly at moderate, but not low, salinity, the effect of inoculation being enough to maintain higher stomatal conductance under higher stress. The photochemical efficiency of PSII and the relative chlorophyll content were not affected by the inoculants. Thus, the effects of the inoculants on the response to salinity were due mainly to stomatal regulation of photosynthesis rather than effects on biochemical limitations on photosynthesis. These results indicate the benefits of these bacterial inoculants in ameliorating the deleterious effect of NaCl in a salt-sensitive crop like sweet pepper.

Additional keywords: Azospirillum, Capsicum annuum L., growth analysis, nitrogen, salt stress.


References

Ayers R, Westcot W (1985) ‘Water quality for agriculture. Irrigation and Drainage Paper No. 29.’ (Food and Agriculture Organization of the United Nations: Rome)

Bar Y, Apelbaum A, Kafkafi U, Goren R (1997) Relationship between chloride and nitrate and its effect on growth and mineral composition of avocado and citrus plants. Journal of Plant Nutrition 20, 715–731.
Relationship between chloride and nitrate and its effect on growth and mineral composition of avocado and citrus plants.CrossRef | 1:CAS:528:DyaK2sXjsFeitLo%3D&md5=79fbda97ce9190a92d807e66f06dfafcCAS |

Barassi CA, Ayrault G, Creus CM, Sueldo RJ, Sobrero MT (2006) Seed inoculation with Azospirillum mitigates NaCl effects on lettuce. Scientia Horticulturae 109, 8–14.
Seed inoculation with Azospirillum mitigates NaCl effects on lettuce.CrossRef | 1:CAS:528:DC%2BD28Xks1OksLo%3D&md5=a50238675995b9fba81fff80b634a19fCAS |

Bashan Y (1998) Azospirillum plant growth-promoting strains are nonpathogenic on tomato, pepper, cotton, and wheat. Canadian Journal of Microbiology 44, 168–174.

Bashan Y, de-Bashan LE (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth – a critical assessment. Advances in Agronomy 108, 77–136.
How the plant growth-promoting bacterium Azospirillum promotes plant growth – a critical assessment.CrossRef | 1:CAS:528:DC%2BC3cXhsFKgurrI&md5=c615dbe8a2aec16e5dd620d308a281c9CAS |

Bashan Y, Holguin G (1997) Azospirillum–plant relationships: environmental and physiological advances (1990–1996). Canadian Journal of Microbiology 43, 103–121.
Azospirillum–plant relationships: environmental and physiological advances (1990–1996).CrossRef | 1:CAS:528:DyaK2sXhsFGmsr0%3D&md5=0bb5449956a7b4fb33ed29a49262390eCAS |

Bashan Y, Holguin G (1998) Proposal for the division of plant growth-promoting rhizobacteria into two classifications: biocontrol-PGPB (plant growth-promoting bacteria) and PGPB. Soil Biology & Biochemistry 30, 1225–1228.
Proposal for the division of plant growth-promoting rhizobacteria into two classifications: biocontrol-PGPB (plant growth-promoting bacteria) and PGPB.CrossRef | 1:CAS:528:DyaK1cXktlKms7c%3D&md5=d535f240f56fa3b514759a30c96451b6CAS |

Bashan Y, Ream Y, Levanony H, Sade A (1989) Nonspecific responses in plant growth, yield, and root colonization of non-cereal crop plants to inoculation with Azospirillum brasilense Cd. Canadian Journal of Botany 67, 1317–1324.
Nonspecific responses in plant growth, yield, and root colonization of non-cereal crop plants to inoculation with Azospirillum brasilense Cd.CrossRef |

Bashan Y, Holguin G, de-Bashan LE (2004) Azospirillum–plant relationships: physiological, molecular, agricultural, and environmental advances (1997–2003). Canadian Journal of Microbiology 50, 521–577.
Azospirillum–plant relationships: physiological, molecular, agricultural, and environmental advances (1997–2003).CrossRef | 1:CAS:528:DC%2BD2cXptlOlsL0%3D&md5=9c14007d110043d63f43fc1536169255CAS |

Bashan Y, Bustillos JJ, Leyva LA, Hernandez JP, Bacilio M (2006) Increase in auxiliary photoprotective photosynthetic pigments in wheat seedlings induced by Azospirillum brasilense. Biology and Fertility of Soils 42, 279–285.
Increase in auxiliary photoprotective photosynthetic pigments in wheat seedlings induced by Azospirillum brasilense.CrossRef | 1:CAS:528:DC%2BD28Xit1Cjtr0%3D&md5=95abcdd148c3a91ee1ce8c8d3dde7cf5CAS |

Blom-Zandstra M, Vogelzang SA, Veen BW (1998) Sodium fluxes in sweet pepper exposed to varying sodium concentrations. Journal of Experimental Botany 49, 1863–1868.
Sodium fluxes in sweet pepper exposed to varying sodium concentrations.CrossRef | 1:CAS:528:DyaK1cXnsFCmsrc%3D&md5=189b23885998e3460d49d479896cf94aCAS |

Cassán F, Maiale S, Masciarelli O, Vidal A, Luna V, Ruiz O (2009) Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation. European Journal of Soil Biology 45, 12–19.
Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation.CrossRef |

Cram WJ (1973) Internal factors regulating nitrate and chloride influx in plant cells. Journal of Experimental Botany 24, 328–341.
Internal factors regulating nitrate and chloride influx in plant cells.CrossRef | 1:CAS:528:DyaE3sXksVWgsLc%3D&md5=31f1e65791d4c21a6e5db30e0e633388CAS |

Cramer GR, Epstein E, Läuchli A (1990) Effects of sodium, potassium and calcium on salt stressed barley. I. Growth analysis. Physiologia Plantarum 80, 83–88.
Effects of sodium, potassium and calcium on salt stressed barley. I. Growth analysis.CrossRef | 1:CAS:528:DyaK3cXlvVyhsLc%3D&md5=d35f56cc02de4ec29e77968e7ad4c1eeCAS |

Creus CM, Sueldo RJ, Barassi CA (1997) Shoot growth and water status in Azospirillum-inoculated wheat seedlings grown under osmotic and salt stresses. Plant Physiology and Biochemistry 35, 939–944.

Curtis PS, Läuchli A (1986) The role of leaf area development and photosynthetic capacity in determining growth of kenaf under moderate saline stress. Australian Journal of Plant Physiology 13, 553–565.
The role of leaf area development and photosynthetic capacity in determining growth of kenaf under moderate saline stress.CrossRef |

del Amor FM (2007) Yield and fruit quality response of sweet pepper to organic and mineral fertilization. Renewable Agriculture and Food Systems 22, 233–238.
Yield and fruit quality response of sweet pepper to organic and mineral fertilization.CrossRef |

del Amor FM, Cuadra-Crespo P (2011) Alleviation of salinity stress in broccoli using foliar urea or methyl-jasmonate: analysis of growth, gas exchange, and isotope composition. Plant Growth Regulation 63, 55–62.
Alleviation of salinity stress in broccoli using foliar urea or methyl-jasmonate: analysis of growth, gas exchange, and isotope composition.CrossRef | 1:CAS:528:DC%2BC3cXhsFKjurjO&md5=1cb7846423105f2f4f78daf319895e55CAS |

del Amor FM, Porras I (2009) Effects of PGPB on growth and yield of pepper under limited nitrogen supply. Canadian Journal of Plant Science 89, 349–358.
Effects of PGPB on growth and yield of pepper under limited nitrogen supply.CrossRef | 1:CAS:528:DC%2BD1MXltlymurw%3D&md5=49231989ba8ce1fa7dc9cce5d245311dCAS |

del Amor FM, Serrano-Martínez A, Fortea MI, Legua P, Núñez-Delicado E (2008) The effect of plant-associative bacteria (Azospirillum and Pantoea) on the fruit quality of sweet pepper under limited nitrogen supply. Scientia Horticulturae 117, 191–196.
The effect of plant-associative bacteria (Azospirillum and Pantoea) on the fruit quality of sweet pepper under limited nitrogen supply.CrossRef | 1:CAS:528:DC%2BD1cXotlOjur0%3D&md5=d51e58645cfebe61eb6d9371ac16b726CAS |

del Amor FM, Cuadra-Crespo P, Walker DJ, Cámara JM, Madrid R (2010) Effect of foliar application of antitranspirant on photosynthesis and water relations of pepper plants under different levels of CO2 and water stress. Journal of Plant Physiology 167, 1232–1238.
Effect of foliar application of antitranspirant on photosynthesis and water relations of pepper plants under different levels of CO2 and water stress.CrossRef | 1:CAS:528:DC%2BC3cXhtVaqsLbF&md5=d62394f478386ba512781ae6846a00fcCAS |

Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant, Cell & Environment 32, 1682–1694.
Plant–rhizobacteria interactions alleviate abiotic stress conditions.CrossRef | 1:CAS:528:DC%2BD1MXhsFKrsrvI&md5=0acb47b0bf2427eee402717450ac8d49CAS |

Dobbelaere S, Croonenborghs A, Thys A, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Aguirre JF, Kapulnik Y, Brener S, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Australian Journal of Plant Physiology 28, 871–879.

Elanchezhian R, Panwar JDS (1997) Effects of 2, 4-D and Azospirillum brasilense on nitrogen fixation, photosynthesis and grain yield in wheat. Journal of Agronomy and Crop Science 178, 129–133.
Effects of 2, 4-D and Azospirillum brasilense on nitrogen fixation, photosynthesis and grain yield in wheat.CrossRef | 1:CAS:528:DyaK2sXltVGgtbc%3D&md5=867466bd5ce7ca893167b3827aacd41aCAS |

Evans GC (1972) ‘The quantitative analysis of plant growth.’ (Blackwell Scientific Publications: Oxford)

Food and Agriculture Organisation (FAO) (2008) FAO land and plant nutrition management service. (FAO: Rome). Available at: http://www.fao.org/nr/land/en/ [Verified 13 October 2011]

Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biology 6, 269–279.
Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants.CrossRef | 1:STN:280:DC%2BD2c3ksVOlug%3D%3D&md5=f2a0cae51905d2136c2c452166476294CAS |

Flowers TJ, Yeo AR (1995) Breeding for salinity resistance in crop plants: where next? Australian Journal of Plant Physiology 22, 875–884.
Breeding for salinity resistance in crop plants: where next?CrossRef |

Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G (2007) Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Applied Microbiology and Biotechnology 76, 1145–1152.
Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium.CrossRef | 1:CAS:528:DC%2BD2sXhtVCns77F&md5=7eef0ba1551ce24bfaf3797aa51a9d7cCAS |

Galal YGM, El-Ghandour IA, Aly SS, Soliman S, Gadalla A (2000) Non-isotopic method for the quantification of biological nitrogen fixation and wheat production under field conditions. Biology and Fertility of Soils 32, 47–51.
Non-isotopic method for the quantification of biological nitrogen fixation and wheat production under field conditions.CrossRef | 1:CAS:528:DC%2BD3cXmvFWrsbc%3D&md5=5c2adc0c7a72d11b6784748e7ec3aadcCAS |

García JAL, Probanza A, Ramos B, Ruiz Palomino M, Gutiérrez Mañero FJ (2004) Effect of inoculation of Bacillus licheniformis on tomato and pepper. Agronomie 24, 169–176.
Effect of inoculation of Bacillus licheniformis on tomato and pepper.CrossRef |

Hamdia MA, El-Komy HM (1997) Effect of salinity, gibberellic acid and Azospirillum inoculation on growth and nitrogen uptake of Zea mays. Biologia Plantarum 40, 109–120.
Effect of salinity, gibberellic acid and Azospirillum inoculation on growth and nitrogen uptake of Zea mays.CrossRef | 1:CAS:528:DyaK1cXhtlSltLw%3D&md5=ed88efbe9a4edc9624a30df6f66c6dacCAS |

Hamdia ABE, Shaddad MAK, Doaa MM (2004) Mechanisms of salt tolerance and interactive effects of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regulation 44, 165–174.
Mechanisms of salt tolerance and interactive effects of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions.CrossRef | 1:CAS:528:DC%2BD2cXhtFWqsb%2FP&md5=5345ec60d8e8bba17feb5e132cee7f14CAS |

Hawkins HJ, Lewis OAM (1993) Effect of NaCl salinity, nitrogen form, calcium and potassium concentration on nitrogen uptake and kinetics in Triticum aestivum L. cv. Gametos. New Phytologist 124, 171–177.
Effect of NaCl salinity, nitrogen form, calcium and potassium concentration on nitrogen uptake and kinetics in Triticum aestivum L. cv. Gametos.CrossRef | 1:CAS:528:DyaK3sXmsVKjurw%3D&md5=c6d5d85ad91672fc43e91e5433656f71CAS |

Jifon JL, Sylvertsen JP, Whaley E (2005) Growth environment and leaf anatomy affect nondestructive estimates of chlorophyll and nitrogen in Citrus sp. leaves. Journal of the American Society for Horticultural Science 130, 152–158.

Jiménez MS, Gonzélez-Rodriguez AM, Morales D, Cid MC, Socorro AR, Caballero M (1997) Evaluation of chlorophyll fluorescence as a tool for salt stress detection in roses. Photosynthetica 33, 291–301.
Evaluation of chlorophyll fluorescence as a tool for salt stress detection in roses.CrossRef |

Karlidag H, Esitken A, Yildirim E, Donmez MF, Turan M (2011) Effects of plant growth promoting bacteria on yield, growth, leaf water content, membrane permeability, and ionic composition of strawberry under saline conditions. Journal of Plant Nutrition 34, 34–45.
Effects of plant growth promoting bacteria on yield, growth, leaf water content, membrane permeability, and ionic composition of strawberry under saline conditions.CrossRef | 1:CAS:528:DC%2BC3cXhsV2gu7jE&md5=7e63e1104f3ee5e47b14c0cf4b54d529CAS |

Kloepper JW, Schroth MN (1978) Plant growth-promoting rhizobacteria on radishes. In ‘Proceedings of the 4th International Conference on Plant Pathogenic Bacteria 2’. pp. 879–882. (Station de Pathologie Vegetale et Phytobacteriologie, INRA: Angers, France)

Kloos K, Mergel A, Rösch C, Bothe H (2001) Denitrification within the genus Azospirillum and other associative bacteria. Australian Journal of Plant Physiology 28, 991–998.

Liu K, Fu H, Bei Q, Luan S (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiology 124, 1315–1325.
Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements.CrossRef | 1:CAS:528:DC%2BD3cXotlWqs7k%3D&md5=cc628320a82270c0c300ebdff6d23d29CAS |

Lycoskoufis IH, Savvas D, Mavrogianopoulos G (2005) Growth, gas exchange, and nutrient status in pepper (Capsicum annuum L.) grown in recirculation nutrient solution as affected by salinity imposed to half of the root system. Scientia Horticulturae 106, 147–161.
Growth, gas exchange, and nutrient status in pepper (Capsicum annuum L.) grown in recirculation nutrient solution as affected by salinity imposed to half of the root system.CrossRef | 1:CAS:528:DC%2BD2MXmt1WitLc%3D&md5=84e5348c2d79f4126a3cf472830173a3CAS |

Marschner H (1995) ‘Mineral nutrition of higher plants.’ 2nd ed. (Academic Press: San Diego)

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence. A practical guide. Journal of Experimental Botany 51, 659–668.
Chlorophyll fluorescence. A practical guide.CrossRef | 1:CAS:528:DC%2BD3cXjtF2js74%3D&md5=092bf5f89ae722b319a6295d4f24cbd4CAS |

Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and pepper. Plant Science 166, 525–530.
Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and pepper.CrossRef | 1:CAS:528:DC%2BD2cXntVyjsA%3D%3D&md5=39ccab87961e2528e5683232ea542377CAS |

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
Comparative physiology of salt and water stress.CrossRef | 1:CAS:528:DC%2BD38Xhslakurw%3D&md5=f51a15096130985e65701806a7266f1bCAS |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.CrossRef | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=4ff74227fb3898bf12208db44bd191acCAS |

Muthukumar T, Udaiyan K (2006) Growth of nursery-grown bamboo inoculated with arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria in two tropical soil types with and without fertilizer application. New Forests 31, 469–485.
Growth of nursery-grown bamboo inoculated with arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria in two tropical soil types with and without fertilizer application.CrossRef |

Navarro JM, Garrido C, Martínez V, Carvajal M (2003) Water relations and xylem transport of nutrients in pepper plants grown under two different salts stress regimes. Journal of Plant Growth Regulation 41, 237–245.
Water relations and xylem transport of nutrients in pepper plants grown under two different salts stress regimes.CrossRef | 1:CAS:528:DC%2BD3sXps1amsrY%3D&md5=d7745f10f166dbd10a4338c61fcd647cCAS |

Nayak DN, Ladha JK, Watanabe I (1986) The fate of marker Azospirillum lipoferum inoculated into rice and its effect on growth, yield, and N2 fixation of plants studied by acetylene reduction, 15N2 feeding and 15N dilution techniques. Biology and Fertility of Soils 2, 7–14.
The fate of marker Azospirillum lipoferum inoculated into rice and its effect on growth, yield, and N2 fixation of plants studied by acetylene reduction, 15N2 feeding and 15N dilution techniques.CrossRef |

Panwar JDS (1991) Effect of VAM and Azospirillum brasilense on photosynthesis nitrogen metabolism and grain yield in wheat. Indian Journal of Plant Physiology 34, 357–361.

Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassán FD, Luna MV (2007) Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. Applied Microbiology and Biotechnology 75, 1143–1150.
Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation.CrossRef | 1:CAS:528:DC%2BD2sXmsVKqtrw%3D&md5=8de32a23a3b771040823973de5a2fbb8CAS |

Pessarakli M (1991) Dry matter yield, nitrogen-15 absorption, and water uptake by green bean under sodium chloride stress. Crop Science 31, 1633–1640.
Dry matter yield, nitrogen-15 absorption, and water uptake by green bean under sodium chloride stress.CrossRef | 1:CAS:528:DyaK38XhtVGit7c%3D&md5=0c2f7d1339e4b6a11288caed3e6df9b5CAS |

Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83, 553–559.
Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate.CrossRef |

Shilev S, Sancho ED, Benlloch-González MB (2011) Rhizospheric bacteria alleviate salt-produced stress in sunflower. Journal of Environmental Management in press

Suhayda CG, Giannini JL, Briskin DP, Shannon MC (1990) Electrostatic changes in Lycopersicon esculentum root plasma membrane resulting from salt stress. Plant Physiology 93, 471–478.
Electrostatic changes in Lycopersicon esculentum root plasma membrane resulting from salt stress.CrossRef | 1:CAS:528:DyaK3cXkslGitLk%3D&md5=fd7ed4170958f8a4d515220eb8a46052CAS |

Sziderics AH, Rasche F, Trognitz F, Sessitsch A, Wilhelm E (2007) Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Canadian Journal of Microbiology 53, 1195–1202.
Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.).CrossRef | 1:CAS:528:DC%2BD2sXhtl2jtrzI&md5=dcef354d4c48eae62aba25f1dae40063CAS |

Torres Netto A, Campostrini E, Gonçalves de Oliveira J, Bressan-Smith RE (2005) Photosynthetic pigments, nitrogen, chlorophyll a fluorescence and SPAD-502 readings in coffee leaves. Scientia Horticulturae 104, 199–209.
Photosynthetic pigments, nitrogen, chlorophyll a fluorescence and SPAD-502 readings in coffee leaves.CrossRef | 1:CAS:528:DC%2BD2MXhslCiurY%3D&md5=c7e865b2b49aa14d860139b5b97e74a3CAS |

Véry AA, Robinson MF, Mansfield TA, Sanders D (1998) Guard cell cation channels are involved in Na+-induced stomatal closure in a halophyte. The Plant Journal 14, 509–521.
Guard cell cation channels are involved in Na+-induced stomatal closure in a halophyte.CrossRef |

Wignarajah K (1990) Growth response of Phaseolus vulgaris to varying salinity regimes. Environmental and Experimental Botany 30, 141–147.
Growth response of Phaseolus vulgaris to varying salinity regimes.CrossRef |

Yokoi S, Bressan RA, Hasegawa PM (2002) ‘Salt stress tolerance of plants. JIRCAS Working Report 25–33. (Japan International Research Center for Agricultural Sciences: Ohwashi, Japan)



Rent Article (via Deepdyve) Export Citation Cited By (32)

View Altmetrics