DOI: 10.5061/dryad.qjq2bvqqv
title: Ecosystem engineers show variable impacts on habitat availability for cavity nesters in South American temperate forests

description: Ecosystem engineers are organisms that impact their environment and
 co-existing species by creating or modifying habitats, and thus they play
 important roles as drivers of community assembly. We examined whether
 cavity characteristics and/or habitat attributes associated with cavities
 provided by four ecosystem engineers, influence the presence of nests of
 three secondary cavity-nesting birds [Aphrastura spinicauda (Thorn-tailed
 Rayadito), Tachycineta leucopyga (Chilean Swallow), and Troglodytes aedon
 (Southern House Wren)], and whether these variations influence their
 reproductive success. We tested this by: i) assessing nest presence in
 cavities supplied by ecosystem engineers and ii) quantifying the
 reproductive success of secondary cavity nesters as a function of cavity
 characteristics and habitat attributes supplied by ecosystem engineers.
 Between 2009 and 2022, we recorded 757 cavities in 546 trees in old-growth
 and second-growth forests in a Global Biodiversity Hotspot in the Andes of
 southern Chile. Insect/fungi and Pygarrhichas albogularis (White-throated
 Treerunner) play a key role as the primary producers of cavities.
 Insect/fungi generated the cavities for 82% of A. spinicauda nests and 95%
 of T. aedon nests; in contrast, 57% of T. leucopyga nests were cavities
 excavated by P. albogularis. Characteristics of cavities (size of cavity
 entrance, volume, and height above ground) were associated with nest
 presence of secondary cavity nesters and with reproductive success of A.
 spinicauda and T. aedon. Habitat attributes such as tree density and
 canopy cover influenced nest presence for A. spinicauda and T. leucopyga,
 but did not correlate with the reproductive success of any secondary
 cavity nester. Bamboo density and forest type were related to reproductive
 success of A. spinicauda and T. aedon. Diameter at Breast Height of trees
 was related to the reproductive success of T. leucopyga. This study
 contributes to understanding the importance of various ecosystem engineers
 for the conservation of secondary cavity-nesting birds in temperate
 forests and beyond.
description: <em>Study area and focal species</em>
 We conducted our study in Andean temperate rainforests of South
 America in the La Araucanía Region, Chile (39°16’S-71°48’W). The main
 weather characteristics of the area are cool summers and average annual
 precipitation &gt;2000 mm distributed throughout the year. The
 surveyed sites included eight old-growth forests (&gt;200 years)
 within public and private protected areas and seven second-growth forest
 sites (40-100 years) on private land (Ibarra et al. 2012, Caviedes and
 Ibarra 2017), each with a mean area of 40 ha (Fig. 1). Old-growth forest
 sites were mixed conifer-broadleaf forests dominated by
 <em>Saxegothaea conspicua</em>, <em>Laureliopsis
 philippiana</em>, and <em>Nothofagus dombeyi</em>
 (500-1000 masl) or by the conifer <em>Araucaria araucana</em>
 and <em>Nothofagus pumilio </em>(1000-1400 masl).
 Second-growth forest sites were dominated by broadleaf species including
 <em>Nothofagus obliqua</em>, <em>N. dombeyi</em>,
 and <em>Laurelia sempervirens </em>(Díaz et al. 2005,
 Altamirano et al. 2017). The understory in both old-growth and
 second-growth forest sites was mostly dominated by bamboo species
 (<em>Chusquea</em> spp.), <em>Rhaphithamnus
 spinosus</em>, different species of <em>Azara</em> and
 <em>Berberis</em>, and tree saplings of species found in both
 types of forest (Díaz et al. 2006, Altamirano et al. 2017).
 <em>Aphrastura spinicauda</em>, <em>Tachycineta
 leucopyga,</em> and <em>Troglodytes aedon</em> are
 strictly dependent on cavities for nesting, and they are among the most
 abundant secondary cavity nesters in the temperate forests of South
 America (Ridgely and Guy 2009, Altamirano et al. 2017). <em>A.
 spinicauda</em> and <em>T. leucopyga</em> are forest
 specialists and typically prefer to use large trees for nesting, while
 <em>T. aedon</em> is considered a generalist and can be found
 in both forests and shrublands (Díaz et al. 2005, Cornelius et al. 2000).
 The diet of all three species consists mainly of insects (Arayo and
 Chester 1993, Altamirano et al. 2012). Nests of these species are
 typically located at heights ranging from 0 to 29 meters above the ground
 (Cornelius 2008, Altamirano et al. 2012). These species exhibit the
 highest degrees of habitat specialization among the avian community in
 southern temperate rainforests, and they are known to be strongly affected
 by habitat loss and degradation in this region (Ibarra and Martin
 2015).   <em>Nest searching,
 monitoring and cavity characteristics</em>
 Between 2009 and 2022, we conducted systematic nest monitoring
 from October to February throughout the breeding season. We worked 6 hours
 per day and 6 days per week in 15 stands encompassing both old-growth and
 second-growth forests. We found and monitored as many active cavity-nests
 as possible (Fig. 1). The authors and field assistants searched for nests
 mostly from pre-existing trails in each stand. We located active bird
 nests by stopping frequently to observe the behaviour of adult birds using
 binoculars. We were alerted to potential nests if adults visited the same
 tree or flew out of a tree suddenly, by evidence of recent wear at the
 entrance of the cavity, or if adults perched near or entered/exited
 cavities (Martin et al. 2004, Cockle et al. 2011b, Altamirano et al.
 2017). Nest-searching was alternated between stand and days. We checked
 lower cavities (&lt;2 m in height) directly using a flashlight with a
 mirror. For higher cavities (&gt;2 m in height), we checked the
 interior using a wireless monitoring system with a telescopic pole
 reaching up to 15 m high (Martin et al 2004, Huebner and Hurteau 2007,
 Cockle et al 2011b). We considered a cavity as active when at least one
 egg or nestling was present inside. We identified nests &gt;15 m high
 as active by observing adult nesting behaviour (e.g., active feeding
 nestling or removing fecal sacs). We assigned a unique number code for
 each nest, cavity, and nest-tree and recorded the nesting bird species,
 origin of the cavity (excavated or produced by fungal/insect decay) and
 excavator species (in the case the cavity was excavated). We monitored
 each occupied cavity every 3-4 days to determine nest fate (number of
 hatched eggs, number of fledglings) and to record when cavities were
 available again for additional nesting attempts. For all surveyed cavities
 that were accessible, we recorded cavity characteristics: cavity volume
 (cm<sup>3</sup>), size of cavity entrance (cm) and cavity
 height above ground (m). As a proxy to assess the cavity volume, we use a
 cylindrical-shape volume formula: V = pr<sup>2</sup>d, where r
 is half of cavity width and d is cavity depth (Koch et al. 2012, Robles
 and Martin 2013).   
 <em>Habitat attributes </em> At
 the end of each nesting season, we quantified habitat attributes through
 vegetation plots (0.04 ha, radius = 11.2 m) around each nest-tree found in
 old-growth and second-growth forests (Ibarra et al. 2014, Caviedes and
 Ibarra 2017). We established 0.04 hectare plots with a radius of 11.2
 meters around each nest tree, under the assumption that secondary nesters
 would concentrate their activities, such as foraging and territory
 defence, within this area (Ibarra et al. 2014, Altamirano et al. 2015).
 Within each plot, we measured both site-level and tree-level attributes.
 Site-level attributes included: 1) tree density: the density of all trees
 with a diameter at breast height (DBH) greater than 12.5 centimeters; 2)
 Tree diameter at breast height (DBH): the diameter of trees measured at
 breast height; 3) Canopy cover: the proportion of the sky covered by
 canopy, estimated from the center of the plot; and 4) density of bamboo
 understory: the density of bamboo vegetation up to 3 meters in height. For
 tree-level attributes, trees were assigned to one of five decay classes:
 Class 1, live healthy trees; Class 2, live unhealthy trees; Class 3,
 recently dead trees; Class 4, long-dead trees; and Class 5, naturally
 fallen trees (modified from Edworthy et al., 2012).
description: # Ecosystem engineers show variable impacts on habitat availability for
 cavity nesters in South American temperate forests
 [https://doi.org/10.5061/dryad.qjq2bvqqv](https://doi.org/10.5061/dryad.qjq2bvqqv) ## Description of the data and file structure *Nest presence and cavity selection* To assess the relationships between the nest presence of *A. spinicauda,* T. leucopyga, or *T. aedon* and the cavities supplied by ecosystem engineers, we first assigned a “1” to cavities with nest presence of any of these three secondary cavity nesters and “0” for cavities found empty or with the presence other nesting birds. For all analyses, we excluded years 2010 and 2022 because of a lack of data. We used generalized linear mixed models (GLMMs) with binomial error distributions and logit link functions. The identity of the ecosystem engineer, along with forest type (old-growth and second-growth forests), cavity volume (cm3), size of cavity entrance (cm), cavity height above ground (m), tree density, average DBH, canopy cover (%), and bamboo density, were incorporated as fixed terms in our analysis. Year and site identity were fitted as a random term to control for variability among years and sites (Bates 2010). We tested all possible combinations of variables, excluding interactions. We used an information-theory approach to assess which characteristics better describe cavity selection; such an approach allows consideration of non-exclusive candidate models, which is particularly relevant when many factors may influence the dependent variable (Burnham and Anderson, 2002). For each species we ranked all candidate models based on AIC, averaged all models within ∆AIC ≤ 2, and we calculated model-averaged parameter estimates and standard errors. *Reproductive success of secondary cavity nesters* We used the logistic exposure method (Shaffer 2004) to assess the influence of habitat on daily nest survival rate for each of the three focal species. Similar to the analyses conducted for nest presence, we tested all possible combinations of variables, excluding interactions. In this model, the identity of the ecosystem engineer, along with forest type (old-growth and second-growth forests), cavity volume (cm3), size of cavity entrance (cm), cavity height above ground (m), tree density, average DBH, canopy cover (%), and bamboo density, were included as fixed terms. For each species we ranked all candidate models based on AIC, averaged all models within ∆AIC ≤ 2, and we calculated model-averaged parameter estimates and standard errors. This approach allowed us to assess the relative importance of each variable on the reproductive success and provided insights into the cavity and habitat preferences and requirements of avian species within the study area. We used GLMMs ( package lme4 v1.1.3, Bates et al. 2015, R software version 4.0.3) using Year and Site as random term and nest fate (successful = 1, failed = 0) as the response variable. We had to exclude, from the analysis, the nests in cavities excavated by *D. lignarius* for both *T. leucopyga* and *T. aedon*. We also excluded the nests of *T. aedon* in the cavities excavated by *C. pitius*, because there was no variability in the response (these nests were all successful) preventing the assessment of how external variables may affect their survival (i.e., quasi-complete separation of data points). For all analyses we standardized all continuous variables to a mean of zero with one unit of standard deviation (Schielzeth 2010). ### Files and variables **Description:**   ##### Variables N° = From 1 to infinity TREE ID = Unique code CAV. ID = Unique code NEST ID = Unique code (e.g. 1415001) SP CODE = Species code (e.g. APHSPI) CAV. ORIGEN = 1 = Natural, 2 = Excavated TREE SP. = Species code. DBH = Diameter at Breast Height DECAY= Class 1, live healthy trees; Class 2, live unhealthy trees; Class 3, recently dead trees; Class 4, long-dead trees; and Class 5, naturally fallen trees EXPOSURE = Days Fixed terms: ENGINEER =  ROTFUNGI = Insects/fungi, COLPIT = *Colaptes pitius*, VENLIG* = Dryobates lignarius, *PYGALB* = Pygarrhichas albogularis* FOREST = OG = Old-growth forest, SEC = Second-growth forest *Cavity characteristics* HEIGHT = cavity height above ground (m) ENTR = size of cavity entrance (cm) VOL = cavity volume (cm3) *Habitat attributes* HC = Highest canopy, the proportion of the sky covered by canopy estimated from the center of the plot (%) TA = Tree around, all trees with a diameter at breast height (DBH) greater than 12.5 centimeters around nest tree (0.04 ha, radius = 11.2 m). DP = Average of all trees with a diameter at breast height (DBH) greater than 12.5 centimeters around nest tree (0.04 ha, radius = 11.2 m). BP = average of density of bamboo vegetation up to 3 meters in height around nest tree (0.04 ha, radius = 11.2 m). Blank cells = NA Random term: YEAR SITE = KAW = Kawellucó, HUE = Huelemolle, PIC = Pichares, LLA = Llancalil,  TRA = Trancura,  FUT = Fundo Futuro, CAÑ = Cañi, PNH = Parque Nacional Huerquehue Response variables: **A) Nest presence and cavity selection** USE = Absence of nest = 0, Presence of nest = 1 **B) Reproductive success of secondary cavity nesters** FATE = successful (At least one fledglings) = 1, failed (Not fledglings) = 0 #### File: Nest\_presence\_2\_Cuatianquiz\_Lima\_et\_al.xlsx Each page corresponding to one species studied. The variables in each sheet is the same for all species. ## Code/software We used GLMMs (package lme4 v1.1.3, Bates et al. 2015, R software version 4.0.3) **A) NEST PRESENCE:** *Sheet in excel: APHSPI = Aphrastura spinicauda, TACMEY = Tachycineta leucopyga,  TROMUS* = *Troglodytes aedon* aphNest.R #### library(readxl) aph &lt;- read_excel("Nest presence_2_Cuatianquiz Lima eta.xlsx", sheet = "APHSPI") **B) REPRODUCTIVE SUCCESS:** *Sheet in excel: REP-APHSPI = Aphrastura spinicauda, REP-TACMEY = Tachycineta leucopyga,  REP-TROMUS* = *Troglodytes aedon* aph_fate.R library(readxl) aph_fa &lt;- read_excel("Nest presence_2_Cuatianquiz Lima eta.xlsx", sheet = "REP-APHSPI")