Shifting from acquisitive to conservative: the effects of Phoradendron affine (Santalaceae) infection in leaf morpho-physiological traits of a Neotropical tree species
Marina Corrêa Scalon A , Sabrina Alves dos Reis B and Davi Rodrigo Rossatto B CA Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade de Brasília, Caixa Postal 04457, 70904-970, Brasília, DF, Brasil.
B Departamento de Biologia, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista, Via de Acesso Professor Paulo Donatto Castellane S/N, Vila Industrial, 14884-900, Jaboticabal, SP, Brasil.
C Corresponding author. Email: drrossatto@gmail.com
Australian Journal of Botany 65(1) 31-37 https://doi.org/10.1071/BT16177
Submitted: 1 September 2016 Accepted: 24 November 2016 Published: 10 January 2017
Abstract
Mistletoes are parasitic plants that penetrate the host branches through a modified root and connect to their xylem to acquire nutrients and water. Under mistletoe infection, resources that would otherwise be used by the host are stolen by the parasite. Our aim was to compare leaf morpho-physiological traits between healthy uninfected branches and mistletoe-infected branches of a Neotropical tree species (Handroanthus chrysotrichus (Mart. ex DC.) Mattos – Bignoniaceae). We also investigated differences between mistletoe and host leaf traits. Morphological (petiole length and thickness, leaf area and thickness, and specific leaf area) and physiological leaf traits (pre-dawn and midday water potential) were measured in 10 individuals infected with the mistletoe Phoradendron affine (Pohl ex DC.) Engl. & K.Krause (Santalaceae). Mistletoes showed smaller and thicker leaves with lower pre-dawn and midday water potential, suggesting that mistletoes are more profligate water users than the host. Host leaves from infected branches were scleromorphic and showed stronger water-use control (less negative water potential) than host leaves from uninfected branches. Our results indicated that leaves from infected branches shifted to a more conservative resource-use strategy as a response to a water and nutrient imbalance caused by mistletoe infection.
Additional keywords: hemiparasite, leaf morphology, leaf traits, leaf water potential, resource use.
References
Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics international 11, 36–43.Arruda R, Fadini RF, Carvalho LN, Del-Claro K, Mourão FA, Jacobi CM, Teodoro GS, van den Berg E, Caires CS, Dettke GA (2012) Ecology of neotropical mistletoes: an important canopy-dwelling component of Brazilian ecosystems. Acta Botanica Brasílica 26, 264–274.
Bannister P, Strong GL (2001) Carbon and nitrogen isotope ratios, nitrogen content and heterotrophy in New Zealand mistletoes. Oecologia 126, 10–20.
| Carbon and nitrogen isotope ratios, nitrogen content and heterotrophy in New Zealand mistletoes.Crossref | GoogleScholarGoogle Scholar |
Bowie M, Ward D (2004) Water and nutrient status of the mistletoe Plicosepalus acaciae parasitic on isolated Negev Desert populations of Acacia raddiana differing in level of mortality. Journal of Arid Environments 56, 487–508.
| Water and nutrient status of the mistletoe Plicosepalus acaciae parasitic on isolated Negev Desert populations of Acacia raddiana differing in level of mortality.Crossref | GoogleScholarGoogle Scholar |
Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Campanello P, Scholz FG (2005) Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plant water potential in Neotropical savanna trees. Trees 19, 296–304.
| Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plant water potential in Neotropical savanna trees.Crossref | GoogleScholarGoogle Scholar |
Calder M, Bernhardt P (1983) ‘The biology of mistletoes.’ (Academic Press: Sydney)
Capuzzo JP, Rossatto DR, Franco AC (2012) Differences in morphological and physiological leaf characteristics between Tabebuia aurea and T. impetiginosa is related to their typical habitats of occurrence. Acta Botanica Brasílica 26, 519–526.
| Differences in morphological and physiological leaf characteristics between Tabebuia aurea and T. impetiginosa is related to their typical habitats of occurrence.Crossref | GoogleScholarGoogle Scholar |
Chaves CJN, Dyonisio JC, Rossatto DR (2016) Host trait combinations drive abundance and canopy distribution of atmospheric bromeliad assemblages. AoB Plants 8, plw010
| Host trait combinations drive abundance and canopy distribution of atmospheric bromeliad assemblages.Crossref | GoogleScholarGoogle Scholar |
Der JP, Nickrent DL (2008) A molecular phylogeny of Santalaceae (Santalales). Systematic Botany 33, 107–116.
| A molecular phylogeny of Santalaceae (Santalales).Crossref | GoogleScholarGoogle Scholar |
Ehleringer JR, Cook CS, Tieszen LL (1986) Comparative water use and nitrogen relationships in a mistletoe and its host. Oecologia 68, 279–284.
| Comparative water use and nitrogen relationships in a mistletoe and its host.Crossref | GoogleScholarGoogle Scholar |
Escher P, Eiblmeier M, Hetzger I, Rennenberg H (2004) Seasonal and spatial variation of carbohydrates in mistletoes (Viscum album) and the xylem sap of its hosts (Populus × euamericana and Abies alba). Physiologia Plantarum 120, 212–219.
| Seasonal and spatial variation of carbohydrates in mistletoes (Viscum album) and the xylem sap of its hosts (Populus × euamericana and Abies alba).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFSltrs%3D&md5=c52ff9779686ea94925a028c751cf466CAS |
Escher P, Peuke AD, Bannister P, Fink S, Hartung W, Jiang F, Rennenberg H (2008) Transpiration, CO2 assimilation, WUE, and stomatal aperture in leaves of Viscum album (L.): effect of abscisic acid (ABA) in the xylem sap of its host (Populus euamericana). Plant Physiology and Biochemistry 46, 64–70.
| Transpiration, CO2 assimilation, WUE, and stomatal aperture in leaves of Viscum album (L.): effect of abscisic acid (ABA) in the xylem sap of its host (Populus euamericana).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtV2htbc%3D&md5=83960ee2ae7f558814f1e02e33cef5b4CAS |
Glatzel G (1983) Mineral nutrition and water relations of hemiparasitic mistletoes: a question of partitioning. Experiments with Loranthus europaeus on Quercus petraea and Quercus robur. Oecologia 56, 193–201.
| Mineral nutrition and water relations of hemiparasitic mistletoes: a question of partitioning. Experiments with Loranthus europaeus on Quercus petraea and Quercus robur.Crossref | GoogleScholarGoogle Scholar |
Glatzel G, Geils BW (2009) Mistletoe ecophysiology: host–parasite interactions. Botany 87, 10–15.
| Mistletoe ecophysiology: host–parasite interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsVChuw%3D%3D&md5=1db425d4f75040b9aa3e15b9e83a9524CAS |
Jarek S (2009) ‘Mvnormtest: normality test for multivariate variables. R package.’ Available at http://cran.r-project.org/web/packages/mvnormtest/index.html [verified 8 December 2016]
Judd WS, Campbell CS, Kellogg EA, Stevens PF (2016) ‘Plant systematics: a phylogenetic approach.’ 4th edn. (Sinauer Associates: Sunderland, MA)
Kuijt J (1969) ‘The biology of parasitic flowering plants.’ (University of California Press: Berkeley, CA)
Logan BA, Reblin JS, Zonana DM, Dunlavey RF, Hricko CR, Hall AW, Schmiege SC, Butschek RA, Duran KL, Emery RJN, Kurepin LV, Lewis JD, Pharis RP, Phillips NG, Tissue DT (2013) Impact of eastern dwarf mistletoe (Arceuthobium pusillum) on host white spruce (Picea glauca) development, growth and performance across multiple scales. Physiologia Plantarum 147, 502–513.
| Impact of eastern dwarf mistletoe (Arceuthobium pusillum) on host white spruce (Picea glauca) development, growth and performance across multiple scales.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsFWgsL0%3D&md5=25df36452e6eed3e0c55274a027781e6CAS |
Lohmann LG, Taylor CM (2014) A new generic classification of tribe Bignonieae (Bignoniaceae) 1. Annals of the Missouri Botanical Garden 99, 348–489.
| A new generic classification of tribe Bignonieae (Bignoniaceae) 1.Crossref | GoogleScholarGoogle Scholar |
Lüttge U, Haridasan M, Fernandes GW, de Mattos EA, Trimborn P, Franco AC, Caldas LS, Ziegler H (1998) Photosynthesis of mistletoes in relation to their hosts at various sites in tropical Brazil. Trees 12, 167–174.
| Photosynthesis of mistletoes in relation to their hosts at various sites in tropical Brazil.Crossref | GoogleScholarGoogle Scholar |
Maruyama PK, Mendes-Rodrigues C, Alves-Silva E, Cunha AF (2012) Parasites in the neighbourhood: interactions of the mistletoe Phoradendron affine (Viscaceae) with its dispersers and hosts in urban areas of Brazil. Flora 207, 768–773.
| Parasites in the neighbourhood: interactions of the mistletoe Phoradendron affine (Viscaceae) with its dispersers and hosts in urban areas of Brazil.Crossref | GoogleScholarGoogle Scholar |
Meinzer F, Woodruff D, Shaw D (2004) Integrated responses of hydraulic architecture, water and carbon relations of western hemlock to dwarf mistletoe infection. Plant, Cell & Environment 27, 937–946.
| Integrated responses of hydraulic architecture, water and carbon relations of western hemlock to dwarf mistletoe infection.Crossref | GoogleScholarGoogle Scholar |
Niinemets Ü (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82, 453–469.
| Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs.Crossref | GoogleScholarGoogle Scholar |
Noetzli KP, Müller B, Sieber TN (2003) Impact of population dynamics of white mistletoe (Viscum album ssp. abietis) on European silver fir (Abies alba). Annals of Forest Science 60, 773–779.
| Impact of population dynamics of white mistletoe (Viscum album ssp. abietis) on European silver fir (Abies alba).Crossref | GoogleScholarGoogle Scholar |
Orozco A, Rada F, Azocar A, Goldstein G (1990) How does a mistletoe affect the water, nitrogen and carbon balance of two mangrove ecosystem species? Plant, Cell & Environment 13, 941–947.
| How does a mistletoe affect the water, nitrogen and carbon balance of two mangrove ecosystem species?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsl2lsbs%3D&md5=b517ac8dab19825803c147a264157f98CAS |
Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61, 167–234.
| New handbook for standardised measurement of plant functional traits worldwide.Crossref | GoogleScholarGoogle Scholar |
Popp M, Mensen R, Richter A, Buschmann H, Willert DJ (1995) Solutes and succulence in southern African mistletoes. Trees 9, 303–310.
| Solutes and succulence in southern African mistletoes.Crossref | GoogleScholarGoogle Scholar |
Press MC, Graves JD (1995) ‘Parasitic plants.’ (Chapman & Hall: London)
Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytologist 166, 737–751.
| Impacts of parasitic plants on natural communities.Crossref | GoogleScholarGoogle Scholar |
Quinn GP, Keough MJ (2002) ‘Experimental design and data analysis for biologists.’ (Cambridge University Press: Cambridge, UK)
R Development Core Team (2015) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna)
Reblin JS, Logan BA, Tissue DT (2006) Impact of eastern dwarf mistletoe (Arceuthobium pusillum) infection on the needles of red spruce (Picea rubens) and white spruce (Picea glauca): oxygen exchange, morphology and composition. Tree Physiology 26, 1325–1332.
| Impact of eastern dwarf mistletoe (Arceuthobium pusillum) infection on the needles of red spruce (Picea rubens) and white spruce (Picea glauca): oxygen exchange, morphology and composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1SqsbrN&md5=986e71bcfcc9324c8797603725a6a9fbCAS |
Reich P, Ellsworth D, Walters M (1998) Leaf structure (specific leaf area) modulates photosynthesis–nitrogen relations: evidence from within and across species and functional groups. Functional Ecology 12, 948–958.
| Leaf structure (specific leaf area) modulates photosynthesis–nitrogen relations: evidence from within and across species and functional groups.Crossref | GoogleScholarGoogle Scholar |
Reid N, Smith D, Venables W (1992) Effect of mistletoes (Amyema preissii) on host (Acacia victoriae) survival. Australian Journal of Ecology 17, 219–222.
| Effect of mistletoes (Amyema preissii) on host (Acacia victoriae) survival.Crossref | GoogleScholarGoogle Scholar |
Richter A, Popp M (1992) The physiological importance of accumulation of cyclitols in Viscum album L. New Phytologist 121, 431–438.
| The physiological importance of accumulation of cyclitols in Viscum album L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmsVymtLY%3D&md5=701f29ea4db254e0549797b18a39bb3bCAS |
Rossatto DR, Kolb RM (2009) An evergreen neotropical savanna tree (Gochnatia polymorpha, Asteraceae) produces different dry-and wet-season leaf types. Australian Journal of Botany 57, 439–443.
| An evergreen neotropical savanna tree (Gochnatia polymorpha, Asteraceae) produces different dry-and wet-season leaf types.Crossref | GoogleScholarGoogle Scholar |
Rossatto DR, Hoffmann WA, Franco AC (2009) Differences in growth patterns between co‐occurring forest and savanna trees affect the forest–savanna boundary. Functional Ecology 23, 689–698.
| Differences in growth patterns between co‐occurring forest and savanna trees affect the forest–savanna boundary.Crossref | GoogleScholarGoogle Scholar |
Rossatto DR, Sternberg LSL, Franco AC (2013) The partitioning of water uptake between growth forms in a Neotropical savanna: do herbs exploit a third water source niche? Plant Biology 15, 84–92.
| The partitioning of water uptake between growth forms in a Neotropical savanna: do herbs exploit a third water source niche?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38npsVagsA%3D%3D&md5=72fd94f2b71cf5b24888fd3d70826d51CAS |
Scalon MC, Wright IJ (2015) A global analysis of water and nitrogen relationships between mistletoes and their hosts: broad‐scale tests of old and enduring hypotheses. Functional Ecology 29, 1114–1124.
| A global analysis of water and nitrogen relationships between mistletoes and their hosts: broad‐scale tests of old and enduring hypotheses.Crossref | GoogleScholarGoogle Scholar |
Scalon MC, Haridasan M, Franco AC (2013) A comparative study of aluminium and nutrient concentrations in mistletoes on aluminium‐accumulating and non‐accumulating hosts. Plant Biology 15, 851–857.
| A comparative study of aluminium and nutrient concentrations in mistletoes on aluminium‐accumulating and non‐accumulating hosts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFKlur7O&md5=f9311ae03b2239957d2775b2ad02cc9bCAS |
Scalon MC, Rossatto DR, Domingos FMCB, Franco AC (2016a) Leaf morphophysiology of a Neotropical mistletoe is shaped by seasonal patterns of host leaf phenology. Oecologia 180, 1103–1112.
| Leaf morphophysiology of a Neotropical mistletoe is shaped by seasonal patterns of host leaf phenology.Crossref | GoogleScholarGoogle Scholar |
Scalon MC, Wright IJ, Franco AC (2016b) To recycle or steal? Nutrient resorption in Australian and Brazilian mistletoes from three low‐phosphorus sites. Oikos
| To recycle or steal? Nutrient resorption in Australian and Brazilian mistletoes from three low‐phosphorus sites.Crossref | GoogleScholarGoogle Scholar | in press.
Schulze ED, Turner N, Glatzel G (1984) Carbon, water and nutrient relations of two mistletoes and their hosts: a hypothesis. Plant, Cell & Environment 7, 293–299.
Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT (2014) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, Cell & Environment 37, 153–161.
| How do trees die? A test of the hydraulic failure and carbon starvation hypotheses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVyjurbN&md5=9f28c2f82516cceb758b2ab43dbbf71bCAS |
Shaw DC, Chen J, Freeman EA, Braun DM (2005) Spatial and population characteristics of dwarf mistletoe infected trees in an old-growth Douglas-fir western hemlock forest. Canadian Journal of Forest Research 35, 990–1001.
| Spatial and population characteristics of dwarf mistletoe infected trees in an old-growth Douglas-fir western hemlock forest.Crossref | GoogleScholarGoogle Scholar |
Silva, AR (2014) ‘Biotools: tools for biometry and applied statistics in agricultural science.’ R package version 1.Available at: https://rdrr.io/cran/biotools/man/biotools-package.html [verified 8 December 2016]
Stewart GR, Press MC (1990) The physiology and biochemistry of parasitic angiosperms. Annual Review of Plant Biology 41, 127–151.
| The physiology and biochemistry of parasitic angiosperms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXksFGkurg%3D&md5=0176b7918d2dd1a8569253e364f4ea21CAS |
Turner IM (1994) Sclerophylly: primarily protective? Functional Ecology 8, 669–675.
| Sclerophylly: primarily protective?Crossref | GoogleScholarGoogle Scholar |
Ullmann I, Lange O, Ziegler H, Ehleringer J, Schulze ED, Cowan I (1985) Diurnal courses of leaf conductance and transpiration of mistletoes and their hosts in central Australia. Oecologia 67, 577–587.
| Diurnal courses of leaf conductance and transpiration of mistletoes and their hosts in central Australia.Crossref | GoogleScholarGoogle Scholar |
Warton DI, Duursma RA, Falster DS, Taskinen S (2012) smatr 3: an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution 3, 257–259.
| smatr 3: an R package for estimation and inference about allometric lines.Crossref | GoogleScholarGoogle Scholar |
Watling J, Press M (2001) Impacts of infection by parasitic angiosperms on host photosynthesis. Plant Biology 3, 244–250.
| Impacts of infection by parasitic angiosperms on host photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFGhsb8%3D&md5=b1fb917746935a101f922d9b62c59e44CAS |
Whittington J, Sinclair R (1988) Water relations of the mistletoe, Amyema miquelii, and its host Eucalyptus fasciculosa. Australian Journal of Botany 36, 239–255.
| Water relations of the mistletoe, Amyema miquelii, and its host Eucalyptus fasciculosa.Crossref | GoogleScholarGoogle Scholar |
Wright IJ, Reich PB, Westoby M (2001) Strategy shifts in leaf physiology, structure and nutrient content between species of high‐and low‐rainfall and high‐and low‐nutrient habitats. Functional Ecology 15, 423–434.
| Strategy shifts in leaf physiology, structure and nutrient content between species of high‐and low‐rainfall and high‐and low‐nutrient habitats.Crossref | GoogleScholarGoogle Scholar |
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
| The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1Crt74%3D&md5=65bdb98ffc4be2c488788c424bee9a19CAS |