DOI: 10.5061/dryad.76hdr7sxp
title: Mistletoes could moderate drought impacts on woodland birds, but are themselves susceptible to drought-induced dieback

description: Mistletoes are hemiparasitic plants and keystone species in many
 ecosystems globally. Given predicted increases in drought frequency and
 intensity, mistletoes may be crucial for moderating drought impacts on
 community structure. Dependent on host vascular flows, mistletoes can
 succumb to stress when water availability falls, making them susceptible
 to mortality during drought. We counted mistletoe across &gt;350,000
 km2 of south-eastern Australia and conducted standardised bird surveys
 between 2016 and 2021, spanning a major drought event in 2018-19. We aimed
 to identify predictors of mistletoe abundance and mortality and determine
 whether mistletoes might moderate drought impacts on woodland birds. Live
 mistletoe abundance varied with tree species composition, land use and
 presence of mistletoebirds. Mistletoe mortality was widespread, consistent
 with high 2018/19 summer temperatures, low 2019/20 summer rainfall and the
 interaction between summer temperatures and rainfall in 2019/20. The
 positive association between surviving mistletoes and woodland birds was
 greatest in the peak drought breeding seasons of 2018/19 and 2019/20,
 particularly for small residents and insectivores. Paradoxically,
 mistletoes could moderate drought impacts on birds, but are themselves
 vulnerable to drought-induced mortality. An improved understanding of the
 drivers and dynamics of mistletoe mortality is needed to address potential
 cascading trophic impacts associated with mistletoe die-off.
description: During 2019/20, we conducted habitat assessments at 2,111
 monitoring sites spanning over 300,000 km<sup>2</sup> of
 south-eastern Australia (Figure 1). We selected monitoring sites in areas
 of woodland habitat deemed suitable for two Critically Endangered bird
 species: the regent honeyeater and swift parrot <em>Lathamus
 discolor</em>. We used a combination of MaxEnt habitat suitability
 models (Figures S1 and S2), expert field searches and the location of
 previous sightings to inform site locations. Since both bird species are
 habitat specialists<sup>29</sup>, our sampling encompasses the
 highest quality remaining woodlands in south-eastern Australia.
 Each monitoring site was a 50m radius (0.79 hectares) around a
 fixed GPS location to two metres accuracy. During one visit to each site
 in 2019/20, we recorded the habitat fixed effects detailed in Table 1. Our
 mistletoe counts focussed on the three most abundant mistletoe species
 (Family Loranthaceae) in the study range: box, needle-leaf and
 long-flowered. We conducted a 360° search of the canopy from each site
 centroid, deviating from this point where necessary to count accurately
 the number of live and dead mistletoe clumps present.
 <strong>Table 1:</strong> Site-level and visit-level
 fixed effects obtained for identifying predictors of mistletoe abundance
 and health and to model the effect of mistletoe abundance on woodland bird
 abundance. For further information on the fixed effects, see Table
 S1. 
 
 <strong>Level</strong> 
 <strong>Fixed effect</strong>
 <strong> </strong> 
 <strong>Description</strong> 
 
 Site-level Spatial location 
 WGS84
 decimal latitude longitude to 2m accuracy. 
 Region 10-level factor
 defining regional clusters of monitoring sites. Included as a random term
 in mistletoe and bird models. 
 Land
 use 9-level factor: Primary land
 use. Canopy
 cover Percentage canopy cover to the nearest
 5%. Tree species PC1
 & PC2 Principal component axes 1 & 2
 of tree species composition (see Figure S3). 
 Tree age Proportion of
 trees present with a diameter at breast height &gt;80cm.
 Tree health 
 
 Proportion of trees in the site that are healthy or only mildly
 stressed per Briggs & Taws30. 
 
 Shrub cover Percentage shrub cover (vegetation 30cm
 to 2m) to the nearest 5%. 
 Live
 mistletoe Total number of clumps of live
 mistletoe across all three species. 
 
 Dead mistletoe Total number of
 clumps of dead mistletoe across all three species. 
   Distance to
 permanent or semi-permanent water source 5-level factor:
 1 = water present within site, 2 = water within 100m, 3 = water within
 300m, 4 = water &gt;300m away, 5 = distance to water
 unknown.  
 
 Mistletoebird presence Presence/absence
 of mistletoebirds detected during ≥ 1 bird survey per site.
   Noisy miner
 abundance Mean abundance of noisy miners (a
 hyperabundant and colonial native bird that excludes other songbirds from
 habitats they occupy) detected during repeat bird surveys at each site
 (mistletoe models), or abundance per site visit (bird models).
 
 Visit-level Breeding Season 
 Annual
 Austral breeding season August to January. 
 Hours since dawn/to dusk
 
 Hours from 6am (morning) or hours to 7pm (afternoon).
   
 Observer 7-level factor: bird surveyor / habitat
 assessor. Random effect in bird models. 
 
   Blossom 5- level factor:
 site-level blossom abundance (including both eucalypts and mistletoes): 0
 = no blossom; 1 = light blossom- few flowers in a small number of trees; 2
 = moderate blossom- few flowers in many trees or moderate flowering in a
 few trees; 3 = heavy blossom- profuse flowering in few trees or moderate
 flowering in multiple trees; 4 = very heavy blossom- multiple
 profusely-flowering canopies. 
 
   Max summer temperature
 
 Mean monthly maximum summer temperature November to
 Feb.  
 
 Max summer rain Mean maximum
 monthly summer rainfall November to Feb. 
 <strong>Bird
 surveys</strong> We conducted 9,012 point-count
 surveys at a total of 1,218 monitoring sites in the Austral spring/summer
 breeding season (August to January) between 2016 and 2021 (Table S2). Each
 survey was conducted by one of 15 professional ornithologists, with 86% of
 surveys completed by seven observers. Our rapid (5-minute) census,
 involving one minute of regent honeyeater song broadcast, was designed to
 maximise the detectability of such rare, nomadic habitat specialists by
 increasing the spatial extent of surveys without compromising
 detectability<sup>31</sup>. We recorded the maximum count of
 all bird species detected visually or aurally within a 50m radius of the
 fixed-point location during each site visit, along with a blossom score
 for each site. Observers remained at the site centroid as much as
 possible, but deviated where necessary to identify individual birds to
 species level or to obtain accurate counts of birds occupying heavily
 flowering trees near site boundaries. We did not include transient birds
 flying through or over study sites in the counts. The blossom score was a
 five-level factor (Table 1); a simple way of modelling variation in
 blossom abundance on nomadic species occupancy
 patterns<sup>32</sup>. To account for intra-seasonal variation
 in flowering phenology and associated changes in woodland bird
 distribution/abundance<sup>33</sup>, we surveyed as many sites
 as possible (77%) twice; once in spring between August and October and
 again in early summer between November and January.
 <strong>Climate data </strong> We
 sourced climate data from the Australian National University Climate
 surface database (ANUCLIM v6.1<sup>34</sup>). We obtained
 national monthly maximum temperature and rainfall measures between 2017
 and 2020, and derived these measures for each of our monitoring site
 locations from a 250m national raster. See Supplementary file S1 for
 further information on derivation of the climate data. For mistletoe
 analysis, we calculated annual mean maximum rainfall and temperature
 measures averaged across the summer months of November to February, when
 mistletoes are most susceptible to drought
 impacts<sup>35</sup>.
 <strong>Statistical analysis</strong>
 We used R v3.4.3<sup>36</sup> for all statistical
 analyses. We first checked for spatial autocorrelation in mistletoe
 abundance and mortality data using correlograms of Moran’s I via package
 <em>ncf </em>v1.2-5<sup>37</sup>. To check for
 cross-correlation between covariates, we used <em>GGally
 </em>v1.4.0<sup>38</sup>, but no covariates showed
 consistent strong positive or negative correlation with others.
 To account for interspecific variation in the suitability of tree
 species as mistletoe hosts<sup>39</sup>, we ran a centred and
 scaled Principal Component Analysis (PCA) of the proportional contribution
 of each tree species to canopy cover across sites using <em>stats
 </em>v3.6.2 in base R. The first two Principal Component axes, which
 we included in subsequent mistletoe and bird models (Tree species PC1
 & PC2), together explained 9% of the total variation in tree
 species composition. Because the proportion of total variation explained
 by the PCA was relatively low, we also conducted a separate analysis of
 the association between individual tree species and live mistletoe
 abundance (Supplementary file S2). To account for
 spatial autocorrelation in the mistletoe and bird data, we fitted a series
 of Integrated Nested Laplace Approximation (INLA) Generalised Linear Mixed
 Models (GLMMs) via package <em>INLA
 </em>v21.02-23<sup>40</sup>. The INLA models included a
 Stochastic Partial Differentiation Equation (SPDE) random term that
 calculates the distances between the spatial location of monitoring sites
 using Matern covariance<sup>41,42</sup>. We selected the best
 models as those with the lowest Deviance Information Criterion (DIC) value
 and assessed their goodness of fit based on conditional R2
 values43. To answer question 1 <em>What are the
 predictors of mistletoe abundance and the drivers of mistletoe mortality?
 </em>we first used live mistletoe counts as the response in a GLMM
 with a negative binomial error structure. The model included as fixed
 effects: Land use, canopy cover, tree species composition, tree health,
 tree age and distance to standing water, with region included as a random
 term (Table 1). To assess the association between mistletoebird presence
 (the key disperser of mistletoe fruits<sup>15</sup>) and noisy
 miner abundance (a key driver of mistletoebird
 distribution<sup>44</sup>) on mistletoe abundance, we re-ran
 the model on the subset of sites where we conducted bird surveys (Figure
 1) and included mistletoebird presence and noisy miner abundance as fixed
 effects in the saturated model. We replaced live
 mistletoe abundance with dead mistletoe abundance as the response measure
 to identify the predictors of mistletoe mortality. To the fixed effects
 included in the live mistletoe model described above, we added live
 mistletoe abundance, mean maximum monthly summer (Nov-Feb) temperature and
 summer rainfall for 2017/18, 2018/19 and 2019/20, as well as the annual
 interaction between these temperature and rainfall measures.
 To answer question two <em>What is the relationship between
 live mistletoe abundance and woodland bird abundance, and how does this
 relationship change during drought?</em> we calculated four woodland
 bird abundance response measures, based on overall bird abundance, body
 size, residency status and feeding guild (Tables 2 and S2). We excluded
 noisy miners from bird abundance measures due to their impacts on woodland
 bird abundance<sup>44</sup>, and instead included noisy miner
 abundance as a fixed effect in the woodland bird models (Table 1). The
 response measures were counts of birds described in Table 2. Fixed effects
 included overall blossom score, breeding season, noisy miner abundance,
 canopy and shrub cover extent, tree species composition, land use,
 distance to standing water, survey time, and live mistletoe abundance (log
 + 1 transformed). We included observer and region as random terms. To
 examine how the relationship between woodland birds and mistletoes changed
 during drought, we included in the woodland bird models the interaction
 term<em> live mistletoe abundance</em> × <em>breeding
 season</em>. We also conducted supplementary analyses to further
 explore the relative importance of mistletoe and eucalypt blossom during
 the drought for woodland birds (Supplementary file S3). For all bird
 models we used a Poisson error structure.
 <strong>Table 2:</strong> Bird response measures used
 in models to answer question 2: What is the relationship between live
 mistletoe abundance and woodland bird abundance, and how does this
 relationship change during drought? Note the species composition of bird
 response measures are not mutually exclusive. See table S3 and the raw
 dataset available via the Dryad digital repository. Bird
 response   
 Description   
 Justification Total bird
 abundance Total abundance of all bird species
 detected, excluding noisy miners.  
 
 Overall bird abundance is the ultimate measure of bird community
 response to mistletoe health and
 abundance<sup>45</sup>.  
 Small resident bird abundance
 
 Abundance of all birds with mean body mass less than 60g
 considered not to be migratory or nomadic.  
 
 60g is the mean mass of noisy miners, which exclude smaller birds
 from habitats they occupy. Excluding migratory and nomadic species
 accounts for high spatio-temporal variability of such species, independent
 of any effects of mistletoe abundance on bird
 abundance<sup>27,44</sup>.  
 Nectarivores
      
   Insectivores Total abundance
 of all nectarivorous birds.  
     Total abundance of all
 insectivorous birds. Feeding guilds will differ in the
 extent to which they depend on mistletoe abundance. Nectarivores predicted
 to be most dependent on mistletoes as a direct feeding
 substrate<sup>46</sup>.  
 Insectivores predicted to be less dependent on mistletoes than
 nectarivores, but through potential impacts of mistletoe on insectivore
 abundance, insectivores may be more dependent on mistletoe than
 granivores<sup>14,15</sup>.
description: The files contained in this sumbmission are excel.csv files and
 can be opened and run with the accompanying R-script