Skip to main content
Log in

Recovery from Severe Mistletoe Infection After Heat- and Drought-Induced Mistletoe Death

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Mistletoes are emerging as important co-contributors to tree mortality across terrestrial ecosystems, particularly when infected trees are stressed by water limitations during drought. While the mechanistic effects of mistletoe infection on host physiology are reasonably well understood, quantifying the effects of mistletoe infection on stand productivity, canopy turnover and ecosystem structure remains challenging. Moreover, the potential devastating effect of mistletoe infection on host survival has distracted from the challenges that mistletoe populations are facing when increasing drought and heat stress threaten their survival in healthy populations. We coupled intensive observations of mistletoe population dynamics with measurements of host tree stem growth, canopy turnover and stand structure in a severely infected temperate eucalypt woodland to monitor how mistletoe infection alters aboveground biomass distribution and to assess ecosystem recovery from severe mistletoe infection during and after a three-year drought. We show that severe mistletoe infection reduces live standing biomass and canopy volume, with mistletoe leaves contributing up to 43% to total stand litter fall. We further identified that a mistletoe:host leaf area ratio above 60% significantly reduced basal area growth, which provides a threshold for productivity losses due to mistletoe infection in eucalypts. Yet, concurrent increases in basal area and the thickening of canopy volume indicate that host trees recover rapidly after the three-year drought combined with record summer heat nearly extinguished the mistletoe population. How common, or how widespread such dynamic changes in mistletoe population dynamics are within Australian or global ecosystems remains subject to further exploration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  • Al-Rowaily SL, et al. 2020. Infection by Plicosepalus curviflorus mistletoe affects the nutritional elements of Acacia species and soil nutrient recycling in an arid rangeland. Plant Ecology 1–12.

  • Bach CE, Kelly D, Hazlett BA. 2005. Forest edges benefit adults, but not seedlings, of the mistletoe Alepis flavida (Loranthaceae). Journal of Ecology 93(1), 79–86.

    Article  Google Scholar 

  • Baik J, Liaqat UW, Choi M. 2018. Assessment of satellite-and reanalysis-based evapotranspiration products with two blending approaches over the complex landscapes and climates of Australia. Agricultural and Forest Meteorology 263:388–398.

    Article  Google Scholar 

  • Bell DM, Pabst RJ, Shaw DC. 2020. Tree growth declines and mortality were asso521 ciated with a parasitic plant during warm and dry climatic conditions in a temperate coniferous forest ecosystem. Global Change Biology 26(3), 1714–1724.

    Article  PubMed  Google Scholar 

  • Bell TL, Adams MA. 2011. Attack on all fronts: functional relationships between aerial and root parasitic plants and their woody hosts and consequences for ecosystems. Tree Physiology 31(1), 3–15.

    Article  CAS  PubMed  Google Scholar 

  • Beringer J, et al. 2016. An introduction to the Australian and New Zealand flux tower network-OzFlux. Biogeosciences 13(21), 5895–5916.

    Article  CAS  Google Scholar 

  • Bowen ME, McAlpine CA, House APN, Smith GC. 2009. Agricultural landscape modification increases the abundance of an important food resource: Mistletoes, birds and brigalow. Biological Conservation 142(1), 122–133.

    Article  Google Scholar 

  • Carnegie AJ, Bi HQ, Arnold S, Li Y, Binns D. 2009. Distribution, host preference, and impact of parasitic mistletoes (Loranthaceae) in young eucalypt plantations in New South Wales, Australia. Botany-Botanique 87(1), 49–63.

    Article  Google Scholar 

  • Cernusak LA, Pate JS, Farquhar GD. 2004. Oxygen and carbon isotope composition of parasitic plants and their hosts in southwestern Australia. Oecologia 139(2), 199–213.

    Article  PubMed  Google Scholar 

  • Cooney SJN, Watson DM. 2008. An experimental approach to understanding the use of mistletoe as a nest substrate for birds: nest predation. Wildlife Research 35(1), 65–71.

    Article  Google Scholar 

  • de Buen LL, Ornelas JF, Garcia-Franco JG. 2002. Mistletoe infection of trees located at fragmented forest edges in the cloud forests of Central Veracruz, Mexico. Forest Ecology and Management 164(1–3), 293–302.

    Article  Google Scholar 

  • De Schepper V, Van Dusschoten D, Copini P, Jahnke S, Steppe K. 2012. MRI links stem water content to stem diameter variations in transpiring trees. Journal of Experimental Botany 63(7), 2645–2653.

    Article  PubMed  Google Scholar 

  • Diaz-Limon MP, Cano-Santana Z, Queijeiro-Bolanos ME. 2016. Mistletoe infection in an urban forest in Mexico City. Urban Forestry & Urban Greening 17:126–134.

    Article  Google Scholar 

  • Dobbertin M, Rigling A. 2006. Pine mistletoe (Viscum album ssp austriacum) contributes to Scots pine (Pinus sylvestris) mortality in the Rhone valley of Switzerland. Forest Pathology 36(5), 309–322.

    Article  Google Scholar 

  • Eamus D, Boulain N, Cleverly J, Breshears DD. 2013. Global change-type drought551 induced tree mortality: vapor pressure deficit is more important than temperature per se in causing decline in tree health. Ecology and Evolution 3(8), 2711–2729.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ehleringer JR, Schulze ED, Ziegler H, Lange OL, Farquhar GD, Cowar IR. 1985. Xylem-tapping mistletoes-water and nutrient parasites. Science 227(4693), 1479–1481.

    Article  CAS  PubMed  Google Scholar 

  • Fonturbel FE, Lara A, Lobos D, Little C. 2018. The cascade impacts of climate change could threaten key ecological interactions. Ecosphere 9(12).

  • Fox J, Weisberg S. 2019. An R Companion to Applied Regression, 3rd. Thousand Oaks CA: Sage.

    Google Scholar 

  • Frost A, Ramchurn A, Smith A. 2018. The Australian landscape water balance model (AWRA-L v6). Technical description of the Australian Water Resources Assessment Landscape model version 6.

  • Gea-Izquierdo G, et al. 2019. Synergistic abiotic and biotic stressors explain widespread decline of Pinus pinaster in a mixed forest. Science of the Total Environment 685, 963–975.

    Article  CAS  Google Scholar 

  • Gevaert AI, Renzullo LJ, Van Dijk AI, Van Der Woerd HJ, Weerts AH, De Jeu RA. 2018. Joint assimilation of soil moisture retrieved from multiple passive microwave frequencies increases robustness of soil moisture state estimation. Hydrology and Earth System Sciences 22(9), 4605–4619.

    Article  Google Scholar 

  • Godfree RC, Tinnin RO, Forbes RB. 2003. Relationships between dwarf mistletoe and the canopy structure of an old-growth lodgepole pine forest in central Oregon. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 33(6), 997–1009.

    Article  Google Scholar 

  • Griebel A, Bennett LT, Metzen D, Cleverly J, Burba G, Arndt SK. 2016. Effects of inhomogeneities within the flux footprint on the interpretation of seasonal, annual, and interannual ecosystem carbon exchange. Agricultural and Forest Meteorology 221:50–60.

    Article  Google Scholar 

  • Griebel A, Bennett LT, Arndt SK. 2017a. Evergreen and ever growing-stem and canopy growth dynamics of a temperate eucalypt forest. Forest Ecology and Management 389:417–426.

    Article  Google Scholar 

  • Griebel A, Watson D, Pendall E. 2017b. Mistletoe, friend and foe: synthesizing ecosystem implications of mistletoe infection. Environmental Research Letters 12(11):115012.

    Article  Google Scholar 

  • Griebel, A and others. 2020. Using a paired tower approach and remote sensing to assess carbon sequestration and energy distribution in a heterogeneous sclerophyll forest. Science of the Total Environment 699, 133918.

    Article  CAS  Google Scholar 

  • Hu B, et al. 2017. Mistletoe infestation mediates alteration of the phytohormone profile and anti-oxidative metabolism in bark and wood of its host Pinus sylvestris. Tree Physiology 37(5), 676–691.

    Article  CAS  PubMed  Google Scholar 

  • Jones DA, Wang W, Fawcett R. 2009. High-quality spatial climate data-sets for Australia. Australian Meteorological and Oceanographic Journal 58(4):233.

    Article  Google Scholar 

  • Jurskis V. 2005. Eucalypt decline in Australia, and a general concept of tree decline and dieback. Forest Ecology and Management 215(1–3), 1–20.

    Article  Google Scholar 

  • Jurskis V, Turner R, Jurskis D. 2005. Mistletoes increasing in ‘undisturbed’ forest: a symptom of forest decline caused by unnatural exclusion of fire? Australian Forestry 68(3), 221–226.

    Article  Google Scholar 

  • Karan M, et al. 2016. The Australian SuperSite Network: a continental, long-term terrestrial ecosystem observatory. Science of the Total Environment 568, 1263–1274.

    Article  CAS  Google Scholar 

  • Kolb TE, et al. 2016. Observed and anticipated impacts of drought on forest insects and diseases in the United States. Forest Ecology and Management 380, 321–334.

    Article  Google Scholar 

  • Kuppers M, Kuppers BIL, Neales TF, Swan AG. 1992. Leaf gas-exchange characteristics, daily carbon and water balances of the host mistletoe pair Eucalyptus-behriana F-Muell and Amyema-miquelii (Lehm Ex Mio) Tigh at permanently low plant water status in the field. Trees-Structure and Function 7(1), 1–7.

    Google Scholar 

  • Logan BA, et al. 2013. Impact of eastern dwarf mistletoe (Arceuthobium pusillum) on host white spruce (Picea glauca) development, growth and performance across multiple scales. Physiologia Plantarum 147(4), 502–513.

    Article  CAS  PubMed  Google Scholar 

  • Macfarlane C, Ryu Y, Ogden GN, Sonnentag O. 2014. Digital canopy photography: Exposed and in the raw. Agricultural and Forest Meteorology 197:244–253.

    Article  Google Scholar 

  • Maes W, et al. 2018. Can UAV-based infrared thermography be used to study plant-parasite interactions between mistletoe and eucalypt trees? Remote Sensing 10 (12), 2062.

    Article  Google Scholar 

  • March WA, Watson DM. 2007. Parasites boost productivity: effects of mistletoe on litterfall dynamics in a temperate Australian forest. Oecologia 154(2), 339–347.

    Article  PubMed  Google Scholar 

  • March WA, Watson DM. 2010. The contribution of mistletoes to nutrient returns: evidence for a critical role in nutrient cycling. Austral Ecology 35(7), 713–721.

    Article  Google Scholar 

  • Mathiasen RL, Nickrent DL, Shaw DC, Watson DM. 2008. Mistletoes: pathology, systematics, ecology, and management. Plant disease 92(7):988–1006.

    Article  PubMed  Google Scholar 

  • Meinzer FC, Woodruff DR, Shaw DC. 2004. Integrated responses of hydraulic architecture, water and carbon relations of western hemlock to dwarf mistletoe infection. Plant Cell and Environment 27(7), 937–946.

    Article  Google Scholar 

  • Mellado A, Morillas L, Gallardo A, Zamora R. 2016. Temporal dynamic of parasitemediated linkages between the forest canopy and soil processes and the microbial community. New Phytologist 211(4), 1382–1392.

    Article  Google Scholar 

  • Mellado A, Zamora R. 2017. Parasites structuring ecological communities: the mistletoe footprint in Mediterranean pine forests. Functional Ecology 31(11), 2167–2176.

  • Miller AC, Watling JR, Overton IC, Sinclair R. 2003. Does water status of Eucalyptus largiflorens (Myrtaceae) affect infection by the mistletoe Amyema miquelii (Loranthaceae)? Functional Plant Biology 30(12), 1239–1247.

    Article  PubMed  Google Scholar 

  • Monteith J, Unsworth M. 1990. Principles of Environmental Physics, 2nd edn. London: Edward Arnold. p 291.

    Google Scholar 

  • Mutlu S, Osma E, Ilhan V, Turkoglu HI, Atici O. 2016. Mistletoe (Viscum album) reduces the growth of the Scots pine by accumulating essential nutrient elements in its structure as a trap. Trees-Structure and Function 30(3), 815–824.

    Article  Google Scholar 

  • Ndagurwa HG, Dube JS, Mlambo D, Mawanza M. 2014. The influence of mistletoes on the litter-layer arthropod abundance and diversity in a semi-arid savanna, Southwest Zimbabwe. Plant and Soil 383(1–2):291–299.

    Article  CAS  Google Scholar 

  • Nguyen H, Wheeler MC, Otkin JA, Cowan T, Frost A, Stone R. 2019. Using the evaporative stress index to monitor flash drought in Australia. Environmental Research Letters 14(6):064016.

    Article  Google Scholar 

  • Novick KA, et al. 2016. The increasing importance of atmospheric demand for ecosystem water and carbon fluxes. Nature Climate Change 6(11), 1023–1027.

    Article  CAS  Google Scholar 

  • Parker TJ, Mathiasen RL. 2004. A comparison of rating systems for dwarf mistletoe induced witches’ brooms in ponderosa pine. Western Journal of Applied Forestry 19(1), 54–59.

    Article  Google Scholar 

  • R Core Team. 2019. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.

    Google Scholar 

  • Raftoyannis Y, Radoglou K, Bredemeier M. 2015. Effects of mistletoe infestation on the decline and mortality of Abies cephalonica in Greece. Annals of Forest Research 58(1), 55–65.

    Article  Google Scholar 

  • Reid N, Lange R. 1988. Host specificity, dispersion and persistence through drought of two arid zone mistletoes. Australian Journal of Botany 36(3):299–313.

    Article  Google Scholar 

  • Smith MS, Reid N. 2000. Population dynamics of an arid zone mistletoe (Amyema preissii, Loranthaceae) and its host Acacia victoriae (Mimosaceae). Australian Journal of Botany 48(1), 45–58.

    Article  Google Scholar 

  • Reid N, Yan Z, Fittler J. 1994. Impact of mistletoes (Amyema miquelii) on host (Eucalyptus blakelyi and Eucalyptus melliodora) survival and growth in temperate Australia. Forest Ecology and Management 70(1–3), 55–65.

    Article  Google Scholar 

  • Renchon AA et al. 2018. Upside-down fluxes Down Under: CO2 net sink in winter and net source in summer in a temperate evergreen broadleaf forest. Biogeosciences 15(12), 3703–3716.

    Article  CAS  Google Scholar 

  • Rigling A, Eilmann B, Koechli R, Dobbertin M. 2010. Mistletoe-induced crown degradation in Scots pine in a xeric environment. Tree Physiology 30(7), 845–52.

    Article  PubMed  Google Scholar 

  • Roussel J-R, Auty D. 2020. lidR: Airborne LiDAR Data Manipulation and Visualization for Forestry Applications. R package version 3:3.

  • Sangüesa-Barreda G, Linares JC, Camarero JJ. 2012. Mistletoe effects on Scots pine decline following drought events: insights from within-tree spatial patterns, growth and carbohydrates. Tree Physiology 32(5), 585–598.

    Article  PubMed  Google Scholar 

  • Shaw DC, Watson DM, Mathiasen RL. 2004. Comparison of dwarf mistletoes (Arceuthobium spp., Viscaceae) in the western United States with mistletoes (Amyema spp., Loranthaceae) in Australia-ecological analogs and reciprocal models for ecosystem management. Australian Journal of Botany 52(4), 481–498.

  • Strong GL, Bannister P. 2002. Water relations of temperate mistletoes on various hosts. Functional Plant Biology 29(1), 89–96.

    Article  PubMed  Google Scholar 

  • Szmidla H, Tkaczyk M, Plewa R, Tarwacki G, Sierota Z. 2019. Impact of common mistletoe (Viscum album L.) on scots pine forests—a call for action. Forests 10(10).

  • Turner RJ, Smith P. 2016. Mistletoes increasing in eucalypt forest near Eden, New South Wales. Australian Journal of Botany 64(2), 171–179.

    Article  Google Scholar 

  • Ward MJ. 2005. Patterns of box mistletoe Amyema miquelii infection and pink gum Eucalyptus fasciculosa condition in the Mount Lofty Ranges, South Australia. Forest Ecology and Management 213(1–3), 1–14.

    Article  Google Scholar 

  • Watson DM. 2001. Mistletoe—a keystone resource in forests and woodlands worldwide. Annual Review of Ecology and Systematics 32:219–249.

    Article  Google Scholar 

  • Watson DM. 2009. Parasitic plants as facilitators: more Dryad than Dracula? Journal of Ecology 97(6), 1151–1159.

    Article  Google Scholar 

  • Watson DM. 2015. Disproportionate declines in ground-foraging insectivorous birds after mistletoe removal. Plos One 10(12).

  • Watson DM. 2016. Fleshing out facilitation-reframing interaction networks beyond top-down versus bottom-up. New Phytologist 211(3), 803–808.

    Article  Google Scholar 

  • Watson DM, McGregor HW, Spooner PG. 2011. Hemiparasitic shrubs increase resource availability and multi-trophic diversity of eucalypt forest birds. Functional Ecology 25(4), 889–899.

    Article  Google Scholar 

  • Watson DM, Herring M. 2012. Mistletoe as a keystone resource: an experimental test. Proceedings of the Royal Society B-Biological Sciences 279(1743), 3853–3860.

    Article  PubMed Central  Google Scholar 

  • Wickham H. 2016. ggplot2: Elegant Graphics for Data Analysis. New York: Springer.

    Book  Google Scholar 

  • Wickham H. 2019. stringr: Simple, Consistent Wrappers for Common String Operations. R package version 1(4).

  • Wickham H et al. 2019. Welcome to the tidyverse. Journal of Open Source Software 4(43), 1686.

    Article  Google Scholar 

  • Yang D, et al. 2017. Microenvironment in the canopy rivals the host tree water status in controlling sap flow of a mistletoe species. Tree Physiology 37(4), 1–10.

    Article  Google Scholar 

  • Zeppel MJ, et al. 2015. Drought and resprouting plants. New Phytologist 206(2), 583–589.

    Article  Google Scholar 

  • Zscheischler J, et al. 2016. Short-term favorable weather conditions are an important control of interannual variability in carbon and water fluxes. Journal of Geophysical Research-Biogeosciences 121(8), 2186–2198.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zweifel R, Bangerter S, Rigling A, Sterck FJ. 2012. Pine and mistletoes: how to live with a leak in the water flow and storage system? Journal of Experimental Botany 63(7), 2565–2578.

    Article  CAS  PubMed  Google Scholar 

  • Zweifel R, Häsler R. 2000. Stem radius changes and their relation to stored water in stems of young Norway spruce trees. Trees 15(1), 50–57.

    Article  Google Scholar 

Download references

Acknowledgements

Thanks to Peter Mumford and Jason Middleton of the School of Aviation at UNSW Sydney for the provision of the airborne LiDAR data which appears in Figure 6. We further thank Craig McNamara for his assistance with the collection of the 2020 UAV-based LiDAR data, Norbert Klause, Charitha Gunasekara and Inna Ljungblom for their assistance with collecting monthly PAI images and sorting the litter fall data, and David Tissue and Victor Resco de Dios for their assistance with initial site establishment. HC, RHN and MMB acknowledge financial support from the NSW Bushfire Risk Management Research Hub. This study was supported by Western Sydney University and used research infrastructure provided to OzFlux and Ecosystem Processes by Terrestrial Ecosystem Research Network (TERN), an Australian Government NCRIS-enabled project. The data from the TERN core hectare are available at the TERN data portal (https://portal.tern.org.au).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anne Griebel.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Author contributions

AG designed the study with input from EP, MB and DM. DM acquired the LiDAR data in 2020 and processed the LiDAR data from all flights; RN and HC calculated the soil moisture and vapor pressure deficit anomalies. AG analyzed the data and drafted the manuscript, and all authors contributed to the final version.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 267 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Griebel, A., Metzen, D., Pendall, E. et al. Recovery from Severe Mistletoe Infection After Heat- and Drought-Induced Mistletoe Death. Ecosystems 25, 1–16 (2022). https://doi.org/10.1007/s10021-021-00635-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-021-00635-7

Keywords

Navigation