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Synthesizing Ecosystem Implications of Mistletoe Infection

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Synthesizing Ecosystem Implications of Mistletoe Infection Environmental Research Letters LETTER • OPEN ACCESS Related content - Networks on Networks: Water transport in Mistletoe, friend and foe: synthesizing ecosystem plants A G Hunt and S Manzoni implications of mistletoe infection - Networks on Networks: Edaphic constraints: the role of the soil in vegetation growth To cite this article: Anne Griebel et al 2017 Environ. Res. Lett. 12 115012 A G Hunt and S Manzoni - Impact of mountain pine beetle induced mortality on forest carbon and water fluxes David E Reed, Brent E Ewers and Elise Pendall View the article online for updates and enhancements. This content was downloaded from IP address 137.154.212.215 on 17/12/2017 at 21:57 Environ. Res. Lett. 12 (2017) 115012 https://doi.org/10.1088/1748-9326/aa8fff LETTER Mistletoe, friend and foe: synthesizing ecosystem OPEN ACCESS implications of mistletoe infection RECEIVED 28 June 2017 Anne Griebel1,3 ,DavidWatson2 and Elise Pendall1 REVISED 1 Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith, NSW, Australia 12 September 2017 2 Institute for Land, Water and Society, Charles Sturt University, PO box 789, Albury, NSW, Australia ACCEPTED FOR PUBLICATION 3 Author to whom any correspondence should be addressed. 29 September 2017 PUBLISHED E-mail: [email protected] 16 November 2017 Keywords: mistletoe, climate change, biodiversity, parasitic plants, tree mortality, forest disturbance Original content from this work may be used Abstract under the terms of the Creative Commons Biotic disturbances are affecting a wide range of tree species in all climates, and their occurrence is Attribution 3.0 licence. contributing to increasing rates of tree mortality globally. Mistletoe is a widespread group of parasitic Any further distribution of this work must plants that establishes long-lasting relationships with a diverse range of host tree species. With climate maintain attribution to change, ecophysiological stress is increasing, potentially making trees more susceptible to mistletoe the author(s) and the title of the work, journal infection, which in turn leads to higher forest mortality rates. citation and DOI. The perception of mistletoe presence in individual trees and forest stands is divided within the scientific community, leading to an ongoing debate regarding its impacts. Forest managers concerned about stand health and carbon sequestration may view mistletoe as a foe that leads to reduced productivity. In contrast, ecologists may see mistletoe as a friend, in light of the wildlife habitat, biodiversity and nutrient cycling it promotes. However, individual studies typically focus on isolated effects of mistletoe presence within their respective research area and lack a balanced, interdisciplinary perspective of mistletoe disturbance. With this conceptual paper we aim to bring togetherthepositiveandnegative impacts of mistletoe presence on tree physiology, soil nutrient cycling as well as stand health and stand dynamics. We focus on the role of mistletoe-induced tree mortality in ecosystem succession and biodiversity. In addition, we present potential modifications of mistletoe presence on the energy budget and on forest vulnerability to climate change, which could feed back into stand dynamics and disturbance patterns. Lastly, we will identify the most pressing remaining knowledge gaps and highlight priorities for future research on this widespread agent of biotic disturbance. 1. Introduction and increasing wildfires as the climate changes (Hut- ley et al 2013, Schoennagel et al 2017). Furthermore, 1.1. Disturbance impacts on forest ecosystems such climate induced disturbances can weaken ecosys- Forest ecosystems contain 80% of aboveground car- tem resilience and alter the occurrence and life-cycle bon and 40% of belowground carbon stocks globally of biotic disturbances (Dukes et al 2009, Johnson (Watson et al 2000) along with the capacity of storing et al 2010, Allen et al 2010, Scott and Mathiasen 2012), carbon over centuries. Disturbances have the poten- such as the recent bark beetle outbreaks that affected tial to alter ecosystem processes and functioning, yet vast areas across western North America (Edburg they are part of the natural cycle of any ecosystem et al 2012). Beetle-induced stand mortality can (Kulakowski et al 2017). Climate induced disturbances, compromise atmospheric carbon sequestration rates such as heatwaves and droughts, can significantly lower (Brown et al 2010), but this has not been found in all carbon sequestration rates in forests (Reichstein et al cases (Reed et al 2014), indicating uncertainty in effects 2013,Yiet al 2015,Yuanet al 2016)andcausewide- of biotic disturbance on carbon cycling. ranging tree mortality (McDowell et al 2011,Karaet al While insect outbreaks and abiotic disturbances 2017). Similarly detrimental effects were reported from like drought, storm and fire often cause wide-spread excessive wind-throw following storms and cyclones stand mortality, the presence of parasitic plants is more © 2017 The Author(s). Published by IOP Publishing Ltd Environ. Res. Lett. 12 (2017) 115012 Figure 1. Mistletoe being friend or foe lies in the eye of the beholder. Left: Areal view of a eucalypt stand that is infected with mistletoe (Amyema miquelii; mistletoe brooms are easily distinguished by their red colored leaves); center: Dead infected trees with the typical establishment of mistletoe brooms expanding from the club-shaped haustoria at the terminal branches; right: An immature boobook owl (Ninox novaeseelandiae) roosting in a mistletoe-infected Acacia on a hot (45 ◦C) day in southern Australia. With their high water content and densely-branched habit, mistletoe clumps represent a more moderate microclimate used by many animals seeking shelter. (Photographs left and center by Anne Griebel, right by Skye Wassens; used with permission). subtle in modifying ecosystem processes and stand is projected to increase the likelihood, frequency and dynamics. Unlike cyclones and wildfires, which are duration of droughts in many ecosystems (Collins et al not necessarily a threat in every climate region, par- 2013), so we must understand the physiological causes, asitic plants are globally distributed and an integral the amplifying role of biotic agents on ecosystem pro- component of most ecosystems (Mathiasen et al 2008). cesses and the resulting consequences of this trend The relationship between the parasite and the host may (McDowell et al 2011). This is increasingly complex reflect mutualism, e.g. vascular epiphytes rely on the as parasitic infection on its own is rarely lethal; rather, structural support of a host plant and in return enhance a combination of multiple stress factors exaggerates nutrient cycling by fertilizing the soil with nutrient- stand mortality rates. enriched litter (March and Watson 2010, Bartels and Tree mortality after extreme droughts typically Chen 2012). The largest group of aerial parasitic plants indicates that cavitation is the predominant process are mistletoes, which are widespread sap-feeding hemi- causing mortality, but native trees in hot and arid cli- parasites (i.e. capable of photosynthesis) that portray mates (such as Australia) are more adapted to drought epiphytic behavior and belong to the order Santalales so that carbon starvation following stomatal regula- (Bell and Adams 2011). Over 1600 species of mistle- tion might contribute to tree death during prolonged toes world-wide have developed a remarkable range droughts.Thisisalong-standingdebate(McDowell of adaptations for mimicking various morphological et al 2008,Salaet al 2010,Sevantoet al 2014), and the traits specific to their local hosts; at least 20 species parasitic and unregulated water use of mistletoes will are listed as endangered. Because mistletoes are long likely contribute to both processes at its host: exaggerat- lived (exceeding 30 years) it can take decades to notice ing vessel cavitation might ultimately result in failure of their damaging effect on the host (figure 1). The poten- the hydraulic transport system, as well as induce carbon tial positive effects of mistletoe infection arise at the starvation by limiting carbon availability (see section ecosystem scale, such as their ability to boost bio- 2). Carbon limitation can be provoked on multiple diversity, which has sparked a debate about the role pathways, such as (i) the acquisition of heterotrophic of mistletoes as keystone species and ecosystem engi- carbon from the host, (ii) the restriction of photosyn- neers (Press and Phoenix 2005,Hatcheret al 2012, thetic carbon gain through inducing increased stomatal Watson and Herring 2012). regulation and (iii) through failures in the hydraulic system which might impair carbon transport from stor- 1.2. Mistletoe amplifies tree mortality age reserves. However, process-based research focused Mistletoe abundance has been increasing within exist- predominantly on the functional understanding of ing distributions (Dobbertin and Rigling 2006,Bowen parasite infection on the leaf-level scale (e.g. Mathi- et al 2009, Turner and Smith 2016), and exacerbation asen et al 2008,BellandAdams2011), and we are of climatic stress in the form of prolonged droughts increasingly recognizing the multifunctional role of has amplified tree mortality rates in mistletoe infected mistletoe in communities and ecosystems (e.g. Wat- forests (Mathiasen et al 1990, Dobbertin and Rigling son 2001,PressandPhoenix2005,Hatcheret al 2012). 2006,Way2011,Sanguesa-Barreda¨ et al 2012,Kolb A holistic
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