Abstract
Mistletoes are epiphytic hemiparasitic plants that are known to negatively affect the growth of their hosts, increase tree mortality, and as a consequence change the community dynamics. Mistletoe alters the mineral nutrition of the host and the nutrient cycle in the soil. In the present study, the elemental nutrient status is described for Acacia asak, A. ehrenbergiana, A. gerrardii, and A. tortilis that were infected with the mistletoe Plicosepalus curviflorus, at three levels of infection (no infection, low and high infection). The nutrients of the mistletoe and the soil under the studied acacias were also determined. The elemental contents of the infected Acacia species were significantly reduced compared to non-infected trees, particularly for potassium and sodium. The reduction in the elemental composition was also species-specific and dependent on infection density. Elemental contents of the mistletoe were significantly higher than their Acacia hosts, particularly for nitrogen, phosphorus, and potassium, and the concentrations of minerals in mistletoe tissues were host- and density-dependent. This study revealed a significant increase in nutrients in the soil beneath the canopy of infected Acacia compared to the non-infected trees. Overall, it appears that mistletoe infection has a dual effect. It threatens the health of the Acacia, potentially killing its host tree due to absorption of host nutrients particularly when the infection intense. It also has a positive effect in that it improves the availability of the micro-habitat of nutrients under the canopy, which in turn may contribute to the maintenance of biodiversity.
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References
Abdullah M, Al-Mazroui M (1998) Climatological study of the southwestern region of Saudi Arabia. I. Rainfall analysis. Clim Res 9:213–223
Ameloot E, Verlinden G, Boeckx P, Verheyen K, Hermy M (2008) Impact of hemiparasitic Rhinanthus angustifolius and R. minor on nitrogen availability in grasslands. Plant Soil 311:255–268
Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686
Arruda R, Carvalho LN, Del-Claro K (2006) Host specificity of a Brazilian mistletoe, Struthanthus aff. polyanthus (Loranthaceae), in cerrado tropical savanna. Flora 201:127–134
Aukema JE (2003) Vectors, viscin, and Viscaceae: mistletoes as parasites, mutualists, and resources. Front Ecol Environ 1:212–219
Bardgett R (2005) The biology of soil: a community and ecosystem approach. Oxford University Press, Oxford
Bickford CP, Kolb TE, Geils BW (2005) Host physiological condition regulates parasitic plant performance: Arceuthobium vaginatum subsp. cryptopodum on Pinus ponderosa. Oecologia 146:179–189
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. J Arid Environ 56:487–508
Bremner J, Mulvaney C (1982) Nitrogen-total. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis: Part 2. American Society of Agronomy, Inc., Madison, pp 595–624
Chaudhary SA, Le Houérou HN (2006) The rangelands of the Arabian Peninsula Science et changements planétaires. Sécheresse 17:179–194
Cuevas-Reyes P, Pérez-López G, Maldonado-López Y, González-Rodríguez A (2017) Effects of herbivory and mistletoe infection by Psittacanthus calyculatus on nutritional quality and chemical defense of Quercus deserticola along Mexican forest fragments. Plant Ecol 218:687–697
Dean W, Midgley J, Stock W (1994) The distribution of mistletoes in South Africa: patterns of species richness and host choice. J Biogeogr 21:503–510
Dobbertin M, Rigling A (2006) Pine mistletoe (Viscum album ssp. austriacum) contributes to Scots pine (Pinus sylvestris) mortality in the Rhone valley of Switzerland. For Pathol 36:309–322
Fisher JP, Phoenix GK, Childs DZ, Press MC, Smith SW, Pilkington MG, Cameron DD (2013) Parasitic plant litter input: a novel indirect mechanism influencing plant community structure. New Phytol 198:222–231
Glatzel G, Geils B (2008) Mistletoe ecophysiology: host–parasite interactions. Botany 87:10–15
Griebel A, Watson D, Pendall E (2017) Mistletoe, friend and foe: synthesizing ecosystem implications of mistletoe infection. Environ Res Lett 12:115012
Hall M, Scholte P, Al-Khulaidi A, Miller A, Al-Qadasi A, Al-Farhan A, Al-Abbasi T (2009) Arabia's last forests under threat II: remaining fragments of unique valley forest in southwest Arabia. Edinb J Bot 66:263–281
He M, Dijkstra FA, Zhang K, Li X, Tan H, Gao Y, Li G (2014) Leaf nitrogen and phosphorus of temperate desert plants in response to climate and soil nutrient availability. Sci Rep 4:6932
Hódar JA, Lázaro-González A, Zamora R (2018) Beneath the mistletoe: parasitized trees host a more diverse herbaceous vegetation and are more visited by rabbits. Ann For Sci 75:75–77
Karunaichamy K, Paliwal K, Arp P (1999) Biomass and nutrient dynamics of mistletoe (Dendrophthoe falcata) and neem (Azadirachta indica) seedlings. Curr Sci 76:840–842
Kim C-W, An C-H, Lee H-S, Yi J-S, Cheong EJ, Lim S-H, Kim H-Y (2019) Proximate and mineral components of Viscum album var. coloratum grown on eight different host tree species. J For Res 30:1245–1253
Kuijt J, Hansen B (2015) Loranthaceae. In: Kubitzki K (ed) Flowering plants Eudicots. Springer, Berlin, pp 73–119
Lo Gullo M, Glatzel G, Devkota M, Raimondo F, Trifilò P, Richter H (2012) Mistletoes and mutant albino shoots on woody plants as mineral nutrient traps. Ann Bot 109:1101–1109
March WA, Watson DM (2007) Parasites boost productivity: effects of mistletoe on litterfall dynamics in a temperate Australian forest. Oecologia 154:339–347
March WA, Watson DM (2010) The contribution of mistletoes to nutrient returns: evidence for a critical role in nutrient cycling. Austral Ecol 35:713–721
Marshall J, Ehleringer J, Schulze E-D, Farquhar G (1994) Carbon isotope composition, gas exchange and heterotrophy in Australian mistletoes. Funct Ecol 8:237–241
Mathiasen RL, Nickrent DL, Shaw DC, Watson DM (2008) Mistletoes: pathology, systematics, ecology, and management. Plant Dis 92:988–1006
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 Environ 27:937–946
Mellado A, Morillas L, Gallardo A, Zamora R (2016) Temporal dynamic of parasite-mediated linkages between the forest canopy and soil processes and the microbial community. New Phytol 211:1382–1392
Muvengwi J, Ndagurwa HG, Nyenda T (2015) Enhanced soil nutrient concentrations beneath-canopy of savanna trees infected by mistletoes in a southern African savanna. J Arid Environ 116:25–28
Ndagurwa HG, Dube JS, Mlambo D (2013) The influence of mistletoes on nitrogen cycling in a semi-arid savanna, south-west Zimbabwe. J Trop Ecol 29:147–159
Ndagurwa HG, Dube JS, Mlambo D (2014) The influence of mistletoes on nutrient cycling in a semi-arid savanna, southwest Zimbabwe. Plant Ecol 215:15–26
Ndagurwa HG, Dube JS, Mlambo D (2015) Decomposition and nutrient release patterns of mistletoe litters in a semi-arid savanna, southwest Zimbabwe. Austral Ecol 40:178–185
Ndagurwa HG, Mundy PJ, Dube JS, Mlambo D (2012) Patterns of mistletoe infection in four Acacia species in a semi-arid southern African savanna. J Tropical Ecol 28:523–526
Okubamichael D, Griffiths M, Ward D (2011) Host specificity, nutrient and water dynamics of the mistletoe Viscum rotundifolium and its potential host species in the Kalahari of South Africa. J Arid Environ 75:898–902
Okubamichael DY, Griffiths ME, Ward D (2016) Host specificity in parasitic plants-perspectives from mistletoes. AoB Plants 8:plw069
Olsen S, Sommers L (1982) Phosphorus. In: Weaver EA (ed) Methods of soil analysis: Part 2, 2nd edn. Soil Science Society of America Inc., Madison, pp 403–430
Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytol 166:737–751
Quested HM, Press MC, Callaghan TV (2003) Litter of the hemiparasite Bartsia alpina enhances plant growth: evidence for a functional role in nutrient cycling. Oecologia 135:606–614
Reblin JS, Logan BA (2015) Impacts of eastern dwarf mistletoe on the stem hydraulics of red spruce and white spruce, two host species with different drought tolerances and responses to infection. Trees 29:475–486
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. Funct Ecol 29:1114–1124
Spasojevic MJ, Suding KN (2011) Contrasting effects of hemiparasites on ecosystem processes: can positive litter effects offset the negative effects of parasitism? Oecologia 165:193–200
Stinca A, Chirico GB, Incerti G, Bonanomi G (2015) Regime shift by an exotic nitrogen-fixing shrub mediates plant facilitation in primary succession. PLoS ONE 10:e0123128f
Tobias PA, Guest DI (2014) Tree immunity: growing old without antibodies. Trends Plant Sci 19:367–370
Urban J, Gebauer R, Nadezhdina N, Čermák J (2012) Transpiration and stomatal conductance of mistletoe (Loranthus europaeus) and its host plant, downy oak (Quercus pubescens). Biologia 67:917–926
Vincent P (2008) Saudi Arabia: an environmental overview. CRC Press, New York
Waly N, Jrais R (2013) Comparative morphology of haustoria and endophytic systems in Loranthaceae species in Saudi Arabia. Egypt J Bot 53:1–10
Waly NM, Emad HM (2012) Taxonomical studies of some Acacia spp. growing in Saudi Arabia. Bull Environ Pharmacol Life Sci 1:55–62
Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University Press, Princeton
Watson DM (2002) Effects of mistletoe on diversity: a case-study from southern New South Wales. Emu 102:275–281
Watson DM (2009) Parasitic plants as facilitators: more Dryad than Dracula? J Ecol 97:1151–1159
Acknowledgements
The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for supporting this work through the research group No (RG-1441-302). The authors thank the Deanship of Scientific Research and RSSU at King Saud University for their technical support.
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Communicated by Lori Biederman.
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Al-Rowaily, S.L., Al-Nomari, G.S.S., Assaeed, A.M. et al. Infection by Plicosepalus curviflorus mistletoe affects the nutritional elements of Acacia species and soil nutrient recycling in an arid rangeland. Plant Ecol 221, 1017–1028 (2020). https://doi.org/10.1007/s11258-020-01058-5
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DOI: https://doi.org/10.1007/s11258-020-01058-5