Nutritional and isotopic relationships of selected Bornean tropical mistletoe–host associations in Brunei Darussalam
Kushan U. Tennakoon A C , Wang H. Chak A and Jay F. Bolin B
+ Author Affiliations
- Author Affiliations
A Biology Program, Faculty of Science, University of Brunei Darussalam, Tungku Link, Gadong, BE 1410, Brunei Darussalam.
B Department of Botany, Smithsonian Institution, PO Box 37012, NMNH MRC-166, Washington, DC 20013, USA.
C Corresponding author. Email: kushan.tennakoon@ubd.edu.bn
Functional Plant Biology 38(6) 505-513 https://doi.org/10.1071/FP10211
Submitted: 8 November 2010 Accepted: 29 March 2011 Published: 3 June 2011
Abstract
Our understanding of mineral nutrition and carbon heterotrophy in mistletoes is derived largely from arid and temperate plant communities. Sharp differences between the tropical, temperate and arid communities, such as seasonality, water availability and mean temperature may influence basic assumptions regarding mistletoe physiology. Thus, we present mineral nutrition profiles and natural abundance carbon and nitrogen stable isotope data for tropical mistletoes and their hosts. Parasite–host mineral nutrition profiles were estimated for three Loranthaceous mistletoes: Scurrula ferruginea Danser, Macrosolen cochinchinensis Blume, and Dendrophthoe curvata Blume and 12 unique mistletoe–host associations. δ13C and δ15N values were estimated for 12 parasite–host associations. Differences between host and parasite δ13C values were small but showed significant depletion in mistletoe leaves compared with the distal branch and proximal branch host leaves. Host and mistletoe δ13C values were uncorrelated whereas δ15N values were significantly correlated, demonstrating mistletoe N dependence. Concentrations of K were higher in mistletoes relative to hosts and significantly higher for Dendrophthoe host associations. For Scurrula and Macrosolen, mean mistletoe–host concentrations of major and minor elements did not differ significantly.
Additional keywords: Dendrophthoe, Macrosolen, mineral nutrition, mistletoe–host interactions, Scurrula, δ13C, δ15N.
References
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 |
Bannister P, King WM, Strong GL (1999) Aspects of the water relations of Ileostylus micranthus (Hook f.) Tieghem, a New Zealand mistletoe. Annals of Botany 84, 79–86.
| Aspects of the water relations of Ileostylus micranthus (Hook f.) Tieghem, a New Zealand mistletoe.Crossref | GoogleScholarGoogle Scholar |
Bolin JF, Tennakoon KU, Maass E (2010) Mineral nutrition and heterotrophy in the water conservative holoparasites Hydnora Thunb. (Hydnoraceae). Flora 205, 802–810.
Calder DM (1983) Mistletoes in focus: an introduction. In ‘The biology of mistletoes’. (Eds M Calder, P Berhard) pp. 1–17. (Academic Press: Sydney, Australia)
Cernusak LA, Pate JS, Farquhar GD (2004) Oxygen and carbon isotope composition of parasitic plants and theirs hosts in southwestern Australia. Oecologia 139, 199–213.
| Oxygen and carbon isotope composition of parasitic plants and theirs hosts in southwestern Australia.Crossref | GoogleScholarGoogle Scholar | 14991394PubMed |
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annual Review of Ecology and Systematics 33, 507–559.
| Stable isotopes in plant ecology.Crossref | GoogleScholarGoogle Scholar |
Deliu C (1974) Mineral nutrition in semi parasitic plants. Part 3: potassium content in certain semi parasitic and caulineplants. StudiaUniversitatis Babes-Bolyai Biologia 19, 89–94.
Dykes AP (1997) Rainfall interception from a lowland tropical rainforest in Brunei. Journal of Hydrology 200, 260–279.
| Rainfall interception from a lowland tropical rainforest in Brunei.Crossref | GoogleScholarGoogle Scholar |
Ehleringer JR, Schulze ED, Ziegler H, Lange OL, Farquhar GD, Cowar IR (1985) Xylem-tapping mistletoes: water or nutrient parasites? Science 227, 1479–1481.
| Xylem-tapping mistletoes: water or nutrient parasites?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvivFKjtA%3D%3D&md5=97425dfcbf76b4ffa8f26cceb0c31a71CAS | 17777782PubMed |
Ehleringer JR, Cook CS, Tieszen LL (1986) Comparative water use and nitrogen relationships in a mistletoe Phoradendron juniperinum and its host. Oecologia 68, 279–284.
| Comparative water use and nitrogen relationships in a mistletoe Phoradendron juniperinum and its host.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
| Carbon isotope discrimination and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktlKmu70%3D&md5=782f1c1e0af45e5dab51601bdfed4f0eCAS |
Field CB, Mooney HA (1985) The photosynthesis-nitrogen relationship in wild plants. In ‘On the economy of plant form and function’. (Ed. TJ Givnish) pp. 25–55. (Cambridge University Press: Cambridge)
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 (1987) Haustorial resistance, foliage development and mineral nutrition in the hemiparasitic mistletoe Loranthus europaeus Jacq. (Loranthaceae). In ‘Parasitic flowering plants. Proceedings of 4th International symposium on parasitic flowering plants’. (Eds HW Weber, W Forstreuter) pp. 253–262. (Philipps-Universitat: Marburg, Germany)
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=21d4eccf05d4b4e5b9cb97c1deb930bcCAS |
Goldstein G, Rada F, Sternberg L, Burguera JL, Burguera M, Orozco A, Montilla M, Zabala O, Azocar A, Canales MJ, Celis A (1989) Gas exchange and water balance of a mistletoe species and its mangrove hosts. Oecologia 78, 176–183.
| Gas exchange and water balance of a mistletoe species and its mangrove hosts.Crossref | GoogleScholarGoogle Scholar |
Hull RJ, Leonard OA (1964) Physiological aspects of parasitism in mistletoes (Arceuthobium and Phoradendron) 1. The carbohydrate nutrition of mistletoes. Plant Physiology 39, 996–1007.
| Physiological aspects of parasitism in mistletoes (Arceuthobium and Phoradendron) 1. The carbohydrate nutrition of mistletoes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2MXhs1yktw%3D%3D&md5=4b90b42f94d50102b7a89549c5a65af3CAS | 16656050PubMed |
Humphries EC (1956) Mineral components and ash analysis. In ‘Modern methods of plant analysis’. (Eds K Park, WM Tracey) pp. 468–502. (Springer-Verlag: Berlin)
Jones LHP (1978) Mineral components of plant cell walls. American Journal of Clinical Nutrition 31, 94–98.
Kumar NC (1975) Eco-physiological studies on Dendrophthoe falcata infection. Bulletin of the Botanical Society of Bengal 29, 33–38.
Kumar NC, Mukherjee KL (1973) Host–parasite relation in Dendrophthoe falcata infection. Indian Phytopathology 26, 148–152.
Kuo J, Pate JS (1990) Anatomy and ultrastructure of haustoria in selected West Australian parasitic angiosperms. In ‘Proceedings of the XIIth International congress for electron microscopy’. pp. 690–691. (San Francisco Press: San Francisco)
Lamont BB (1983) Mineral nutrition of mistletoes. In ‘The biology of mistletoes’. (Eds M Calder, P Berhard) pp. 129–143. (Academic Press: Sydney, Australia)
Lamont BB, Southall KJ (1982) Distribution of mineral nutrients between the mistletoe Amyema presii and its host, Acacia acuminata. Annals of Botany 49, 721–725.
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 |
Marschner H (1986) ‘Mineral nutrition of higher plants.’ (Academic Press: London)
Marshall JD, Ehleringer JR (1990) Are xylem-tapping mistletoes partially heterotrophic? Oecologia 84, 244–248.
Marshall JD, Ehleringer JR, Schulze ED, Farquhar G (1994) Carbon isotope composition, gas exchange and heterotrophy in Australian mistletoes. Functional Ecology 8, 237–241.
| Carbon isotope composition, gas exchange and heterotrophy in Australian mistletoes.Crossref | GoogleScholarGoogle Scholar |
Mengel K, Kirkby EA (1987) ‘Principles of plant nutrition.’ (4th edn) (International Potash Institute: Bern, Switzerland)
Misra PC, Saxena YR (1971) Nitrogen metabolism in angiosperm parasites: total nitrogen and its forms. Indian Journal of Experimental Biology 9, 72–74.
Murphy J, Riley J (1962) A modified single solution for the determination of phosphate in natural waters. Analytica Chimica Acta 27, 31–36.
| A modified single solution for the determination of phosphate in natural waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF38XksVyntr8%3D&md5=5af6c72dbb34afeb0425d69536a675b9CAS |
Nickrent DL, Malécot V, Vidal-Russel R, Der JP (2010) A revised classification of Santalales. Taxon 59, 538–558.
Nicoloff T (1923) Contribution a la physiologie de la nutrition des parasites végétaux supérieurs. Revue général de Botanique 35, 545–552.
Pate JS (2001) Haustoria in action: case studies of nitrogen acquisition by woody xylem-tapping hemiparasites from their hosts. Protoplasma 215, 204–217.
| Haustoria in action: case studies of nitrogen acquisition by woody xylem-tapping hemiparasites from their hosts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mnos1OgtQ%3D%3D&md5=a39e078754107217f91c06fd2b9e03ddCAS | 11732059PubMed |
Pate JS, True KC, Kuo J (1991) Partitioning of dry matter and mineral nutrients during a reproductive cycle of the mistletoe Amyema linophyllum (Fenzl.) Tieghem parasitizing Casuarina obese Miq. Journal of Experimental Botany 42, 427–439.
| Partitioning of dry matter and mineral nutrients during a reproductive cycle of the mistletoe Amyema linophyllum (Fenzl.) Tieghem parasitizing Casuarina obese Miq.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkt1KjtbY%3D&md5=4a4f858c16f5c439a2e3acad24d91b1eCAS |
Popp M, Mensen R, Richter A, Bushmann H, Willert DJV (1995) Solutes and succulence in Southern African mistletoes. Trees 9, 303–310.
| Solutes and succulence in Southern African mistletoes.Crossref | GoogleScholarGoogle Scholar |
Prakash S, Krishnam PS, Tewari KK (1967) Biochemical aspects of parasitism by the angiosperm parasites 1. Phosphate fractions in the leaves of Loranthus and hosts. Plant Physiology 42, 347–351.
| Biochemical aspects of parasitism by the angiosperm parasites 1. Phosphate fractions in the leaves of Loranthus and hosts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXktVyktbc%3D&md5=158be3a43967a27f6b8683012bdb1281CAS | 16656513PubMed |
Press MC, Shaw N, Tuohy JM, Stewart GR (1987) Carbon isotope ratios demonstrate carbon flux from C4 host to C3 parasite. Plant Physiology 85, 1143–1145.
| Carbon isotope ratios demonstrate carbon flux from C4 host to C3 parasite.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXptFOqtg%3D%3D&md5=3baff2e3053d6710813ca7b1ed16b5f3CAS | 16665818PubMed |
Richter A, Popp M, Mensen R, Stewart GR, Willert DJV (1995) Heterotrophic carbon gain of the parasitic angiosperm Tapinanthus oleifolius. Australian Journal of Plant Physiology 22, 537–544.
| Heterotrophic carbon gain of the parasitic angiosperm Tapinanthus oleifolius.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXos1erur4%3D&md5=a9a329c63fdf0135a32b1171ff86299cCAS |
Schulze ED, Ehleringer J (1984) The effect of nitrogen supply on growth and water use efficiency of xylem mistletoes. Planta 162, 268–275.
| The effect of nitrogen supply on growth and water use efficiency of xylem mistletoes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlvFSms78%3D&md5=5d347d83e8ea03d845941cc181ec657eCAS |
Schulze ED, Turner NC, Glatzel G (1984) Carbon, water and nutrient relations of two mistletoes and their hosts: a hypothesis. Plant, Cell & Environment 7, 293–299.
Schulze ED, Lange OL, Ziegler H, Gebauer G (1991) Carbon and nitrogen isotope ratios of mistletoes growing on nitrogen and non-nitrogen fixing hosts and on CAM plants in the Namib desert confirm partial heterotrophy. Oecologia 88, 457–462.
St Clair SB, Lynch JP (2005) Element accumulation patterns of deciduous and evergreen tree seedlings on acid soils: implications for sensitivity to manganese toxicity. Tree Physiology 25, 85–92.
Stewart GR, Orebamjo TO (1980) Nitrogen status and nitrate reductase activity of the parasitic angiosperm Tapinanthus bangwensis (Engl. & Krause) Danser growing on different hosts. Annals of Botany 45, 587–589.
Stewart GR, Press MC (1990) The physiology and biochemistry of parasitic angiosperms. Annual Review of Plant Physiology and Plant Molecular Biology 41, 127–151.
| The physiology and biochemistry of parasitic angiosperms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXksFGkurg%3D&md5=09fdd6cb945db5bb63647a9cdd1ced7cCAS |
Tennakoon KU, Pate JS (1996) Effects of parasitism by a mistletoe on the structure and functioning of branches of its host. Plant, Cell & Environment 19, 517–528.
| Effects of parasitism by a mistletoe on the structure and functioning of branches of its host.Crossref | GoogleScholarGoogle Scholar |
Urness PJ (1969) Nutritional analyses and in vitro digestibility of mistletoes browsed by deer in Arizona. Journal of Wildlife Management 33, 499–505.
| Nutritional analyses and in vitro digestibility of mistletoes browsed by deer in Arizona.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXlt1Wis70%3D&md5=55982da29f3e41f145924040339b1bacCAS |
Wang L, Kgope B, D’Odorico P, Macko SA (2008) Carbon and nitrogen parasitism by a xylem-tapping mistletoe (Tapinanthus oleifolius) along the Kalahari transect: a stable isotope study. African Journal of Ecology 46, 540–546.
| Carbon and nitrogen parasitism by a xylem-tapping mistletoe (Tapinanthus oleifolius) along the Kalahari transect: a stable isotope study.Crossref | GoogleScholarGoogle Scholar |
