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Trophic behavior of specialist predators from a macroecological approach: the

case of the Magellanic woodpecker in South American temperate forests

Article  in  Global Ecology and Conservation · September 2020

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 1 Trophic behavior of specialist predators from a macroecological approach: the case of

2 the Magellanic woodpecker in South American temperate forests

3 Alberto J. Alaniz,1,2,3* Mario A. Carvajal2,3,4, Pablo M. Vergara4, Andrés Fierro4, Darío

4 Moreira-Arce4, Alejandro Rojas-Osorio3, Gerardo E. Soto5 and Amanda D. Rodewald5

1
5 Departamento de Ingeniería Geográfica, Facultad de Ingeniería, Universidad de Santiago

6 de Chile.

2
7 Centro de Estudios en Ecología Espacial y Medio Ambiente, Ecogeografía, Santiago,

8 Chile.

3
9 Departamento de Ecología, Facultad de Biológicas, Pontificia Universidad Católica de

10 Chile, Santiago, Chile

4
11 Departamento de Gestión Agraria, Facultad Tecnológica, Universidad de Santiago de

12 Chile, Chile.

5
13 Cornell Lab of Ornithology and Department of Natural Resources, Cornell University,

14 Ithaca, USA

15 *Corresponding author: Alberto J. Alaniz (Address: Enrique Kirberg Baltiansky nº 03 |

16 Universidad de Santiago de Chile, Estación Central, Santiago, Chile; ORCID: 0000-0003-

17 4878-8848; Email alberto.alaniz@usach.cl

18
19 ABSTRACT

20 Theoretical and empirical studies have addressed predator-prey relationships, but the

21 relevance of individual prey species, prey species richness and environment on the niche and

22 the distribution of specialist predators have been scarcely tested with a macroecological

23 approach. Here we aim to analyze the niche and spatial distribution of the Magellanic

24 woodpecker (MWP; Campephilus magellanicus), a specialist predator, analyzing the relative

25 importance of its individual prey species, prey species richness and environmental factors.

26 We modeled the niches of the MWP and its five most important long-horned beetle prey

27 species, quantifying their similarity in spatial distribution and niche. Then we evaluated the

28 relative importance of single prey species and prey species richness on the potential

29 distribution of the MWP, which showed a high degree of overlap with the niche and spatial

30 distribution of three prey species. MWP models with each of these three prey species had a

31 better fit than the model with prey species richness, and contributed more than environmental

32 variables. These results suggest that MWP responds to particular prey items rather than prey

33 species richness. These findings highlight the usefulness of ecological niche models to

34 identify behavioral traits, being potentially replicable in other types of interactions such as

35 competition, mutualism, parasitism, and pollination.

36 Keywords: Niche overlap, Predator-prey, Potential spatial interaction, Niche modelling,

37 Ecological interactions, Biogeographic analysis.

38
39 HIGHLIGHTS

40 • The influence of prey on niche and distribution of a specialist predator was tested

41 • The Magellanic woodpecker responded to single prey items rather than prey species

42 richness.

43 • Prey species were more important than environmental variables for niche.

44 • Ecological niche models may be useful to assess prey species behavioral traits.

45 INTRODUCTION

46 Trophic interactions are shaped by evolutionary history and environmental pressure (Pianka,

47 2011), and have the potential to affect the behavior and ecology of species profoundly.

48 Interactions between consumers and their prey and resources, are among those widely

49 recognized to influence both the niche space and geographic distribution of species (Colwell

50 and Rangel, 2009; Dietl, 2003; Fleischer et al., 2018). Theoretical and empirical models have

51 addressed how interactions can be strongly mediated by environmental variables, as well as

52 the extent to which predators tend to adjust their space use in response to the distribution of

53 prey and other resources (Flaxman and Lou, 2009; Hammond et al., 2007).

54 At a local scale, the dynamics of predator–prey populations emerge from the two-way

55 behavioral and demographic responses of prey and predators (Courbin et al., 2014; Lima,

56 2002; Williams and Flaxman, 2012), while at broad spatial scales the coexistence of predators

57 and their prey spans wide gradients of prey resources and environmental conditions (Holt

58 and Barfield, 2009; Shurin and Allen, 2001). Predator-prey interactions are influenced by the

59 level of specialization of predators, and tend to increase when their niches overlap as

60 predators become more specialized on a single prey species (Case et al., 2015; Colwell and
61 Rangel, 2009; Dietl, 2003; Fleischer et al., 2018). Conversely, the habitat preference and

62 range extent of generalist predators is influenced by the richness of available prey species

63 (Emin et al., 2018; Gherghel et al., 2018; Holt and Barfield, 2009; Shurin and Allen, 2001).

64 However, resource-rich and competition-free conditions may cause a single prey species to

65 be more abundant, inducing predators to be more efficient at feeding upon this prey item, as

66 expected for generalist predators with dietary plasticity and local adaptation (Peers et al.,

67 2014). Such a pattern of prey availability will influence the predator to couple its niche and

68 distribution as a function of the prey on which it has specialized over the evolutionary time

69 scale (Holt and Barfield, 2009).

70 Ecological Niche Models (ENMs) can be useful to test hypotheses about the geographic

71 extent in which predator and prey are predicted to coexist, and to assess their levels of

72 similarity in niche requirements (Alaniz et al., 2018b; Alt et al., 2019; Aryal et al., 2016)

73 This method has been applied to compare the spatial distribution and ecological niches of

74 specialist (Aryal et al., 2016; Peers et al., 2014; Trainor et al., 2014) and generalist (Alaniz

75 et al., 2018b; Gherghel et al., 2018; Hof et al., 2012) predators in relation to their prey. It is

76 important to note that the uncertainty in the prediction of these predator-prey interactions

77 tends to increase as the spatial scale becomes coarser (Peterson and Soberón, 2012; Sandom

78 et al., 2013; Soberón, 2007; Soberon and Nakamura, 2009), and reduces when biotic

79 predictors are included in ENMs (Araújo and Rozenfeld, 2014; Atauchi et al., 2018; Gherghel

80 et al., 2018; Holt et al., 2018; Simões and Peterson, 2018). Previous studies have used abiotic

81 variables combined with ecological and biological knowledge of the species to sharpen the

82 estimation of native species distribution in the Southern South American Temperate

83 Rainforest (SSATR) biome (Alaniz et al., 2018a; Carvajal et al., 2018; Gutiérrez-Tapia and
 84 Palma, 2016; Uribe-Rivera et al., 2017). These models have included biological data such as

85 i) phylogenetic information to reconstruct the distribution of species under past climate

86 changes (Gutiérrez-Tapia and Palma, 2016); ii) dispersal capacity of species to predict future

87 distribution considering climate change scenarios (Uribe-Rivera et al., 2017); iii) population

88 traits to estimate source-sink metapopulation dynamics for focal species (Carvajal et al.,

89 2018); and iv) floral resource requirements of a pollinator hoverfly to estimate its habitat loss

90 during the last 15 years (Alaniz et al., 2018a). However, prey-predator interactions have not

91 been studied with a macroecological approach in the SSATR, while in the rest of the world

92 the studies that include this approach are scarce (Gherghel et al., 2018; Hof et al., 2012;

93 Trainor et al., 2014).

94 An important species of the SSATR is the Magellanic woodpecker (MWP, Campephilus

95 magellanicus), a large-sized bird (35-40 cm height) considered an essential seed dispersal

96 agent and ecological engineer that creates cavities in dead trees, providing habitat for many

97 species in the SSATR (Soto et al., 2018; Vergara et al., 2017). MWP have been documented

98 feeding on a diverse group of trophic resources, including tree sap, fruits and small

99 vertebrates (e.g. small bird broods, lizards; Ojeda, 2003). In spite of this relatively flexible

100 trophic behavior, their fledglings require to be fed with large-sized wood-boring larvae of

101 saproxylic long-horned beetles (Cerambycidae), which may provide a good nutritional

102 source (Winkler et al., 1995). Five long-horned beetle species have been documented to be

103 the main preferred prey items of the MWP due to their large size (> 4 cm) and relatively high

104 abundance in old-growth Nothofagus forest (e.g. Ojeda and Chazarreta, 2014; Vergara et al.,

105 2016; 2017). Thus the survival rate and viability of fledglings, as well as their capacity to

106 reach the adult stage, are strongly influenced by the availability of these prey items (Ojeda
107 and Chazarreta, 2014; Vergara et al., 2017b, 2016). This suggests that prey species play an

108 essential role in determining the niche and distribution of the MWP, however this relationship

109 has not been evaluated. The study of this relationship may be important to unravel the

110 influence of prey species on this ecological engineer species, which could be essential to

111 maintain the health of the complete ecological network that depends on cavities. Testing the

112 specialism and dependence of the MWP in terms of its niche in relation to its prey is essential

113 to prevent its extinction in the face of a global decline of insect populations. We hypothesize

114 that MWP could adjust their niche requirements and distribution in response to large-sized

115 larvae of long-horned beetles, which have relatively low abundance in temperate forests

116 (Cerda and Angulo, 2000). The low abundance of the long-horned beetles in addition to the

117 highly specialist behavior of the MWP threaten the long-term survival of an important

118 ecological engineer in the cavity-nesting network of SSATR.

119 Here we address the relationship between a specialist predator and its prey species across the

120 complete SSATR biome from 33 °S to 56 °S, characterized by high amounts of precipitation

121 and the presence of several caducifolious and evergreen tree species. In particular we address

122 the following questions: i) how important are particular prey species to the niche and

123 distribution of this specialist species in comparison to bioclimatic variables and prey species

124 richness? ii) Which prey species have the greatest environmental niche overlap with and best

125 explain the distribution of Magellanic woodpeckers?

126 MATERIALS AND METHODS

127 Analytical framework overview

128 Maximum Entropy-based ENM were computed in Maxent 3.3.3k (Phillips et al., 2017) and

129 used to estimate the environmental suitability and characterize ecological niche from a set of

130 predictor variables. ENM analysis involved the following methodological steps detailed in

131 Figure 1: A) First we fitted “abiotic” ENMs for woodpeckers and their prey species using

132 only environmental variables as predictors, aiming to generate suitability maps for both. Then

133 we estimated species richness from the outputs of prey ENMs. Finally, we applied a series

134 of metrics to measure spatial overlap of the MWP with each prey species, as well as prey

135 species richness. B) We fitted univariate ENMs for the MWP, using individual prey species

136 and richness as predictors, evaluating the performance of each model. Then we fitted ENMs

137 for the MWP adding each prey species and richness to the set of environmental variables,

138 comparing their contributions to the model. C) We evaluated the environmental niche

139 similarity between the MWP and each prey species using principal component analysis

140 (PCA-env).

141 Species inputs

142 Species occurrences are required as input for ENM, so we compiled a database of MWP (n

143 = 910) from different sources considering only non-duplicated occurrences with specific

144 geographic coordinates recorded after 1980: 1) eBird (Sullivan et al., 2009); 2) Global

145 Biodiversity Information Facility (GBIF.org, 2019); 3) published studies; and 4) our own

146 field records (Table S1). We used occurrence data of saproxylic long-horned beetles

147 (Cerambycidae) from GBIF (GBIF.org, 2019), ten entomological collections and our own

148 field samples, including records in different sites from south-central Chile (35 - 42°S) to

149 south Patagonia (42 - 55°S, Fig. S1). We used only geographically specific locations from

150 eBird and GBIF, excluding occurrences without explicit latitude and longitude information.
151 We reduced the spatial autocorrelation of occurrences by applying a spatial rarefying

152 function which select points considering a minimum distance of 3 km, maintaining only the

153 non-autocorrelated selected occurrences (Brown, 2014). We considered this distance based

154 on the home range of a MWP pair (1 km; Vergara et al., 2017a) and the pixel size used (500

155 m), aiming to avoid overfitting and spatial bias in the ENM. To ensure the quality of the

156 ENM in relation to the minimum number of occurrences, we followed the methodology of

157 van Proosdij et al. (2015), where the minimum number of occurrences depends on the species

158 prevalence (percentage of area occupied by the species in relation to the total modeled area).

159 We considered data of five long-horned beetle species: Calydon globithorax (n = 58),

160 Calydon submetallicum (n = 45), Cheloderus childreni (n = 59), Lautarus concinnus (n = 79)

161 and Microplophorus magellanicus (n = 169). We based the analysis on the above five species

162 because they have large-sized larvae (usually > 4 cm) known to be locally abundant and are

163 preyed upon by MWP, as reported by many studies (Baldini and Alvarado, 2008; Cameron

164 and Real, 1974; Espinosa et al., 2016; Rageot and Gedda, 2011; Soto et al., 2017; Vergara

165 and Schlatter, 2004) and our own observations of woodpecker nests (Supplementary File 1).

166 Environmental variable inputs

167 Another important input for ENM are environmental predictor layers, so we compiled a

168 dataset of bioclimate, site, vegetation and human influence variables (Table S2): A)

169 bioclimate variables, composed of 19 bioclimatic layers plus solar radiation, wind speed and

170 water vapor pressure from the WorldClim 2 project (Fick and Hijmans, 2017); B) site

171 variables, which included elevation, slope, aspect and topographic diversity index, Soil

172 Organic Carbon (SOC) at 0-30 cm and 30-100 cm depth (Hengl et al., 2017; Theobald et al.,

173 2015), obtained from published studies and active radar sensors, downloaded from the
174 Google Earth Engine platform (GEE; Gorelick et al. 2017) and processed; C) vegetation

175 variables consisting of Evenness Vegetation Index (EVI), Normalized Difference Water

176 Index (NDWI), Net Primary Production (NPP), Vegetation Continuous Fields (VCF), and

177 Plant Senescence Reflectance Index (PSRI); and D) human influence variables, including

178 Burned Area Index (BAI) and human footprint (Venter et al., 2016). The initial full predictor

179 dataset included 32 environmental variables (Table S2), all at a spatial resolution of 1000 m

180 (the largest pixel). The spatial extent or background of the variables was the complete range

181 of SSATR biomes (evergreen and deciduous forest) excluding the Patagonia steppe biome

182 (Fig. S1), as applied in previous modelling studies in this same region (Alaniz et al., 2018a;

183 Carvajal et al., 2018).

184 Environmental niche modelling procedure

185 We generated an exploratory environmental ENM in MaxEnt v3.4.1, using all the predictor

186 variables and the datasets of non-autocorrelated occurrences of MWP and their five prey

187 species (Phillips et al., 2017). These exploratory ENMs use a cross-validation technique for

188 evaluation, where the number of replicates varies in each species depending on the number

189 of available occurrences, considering 70% of data for training and 30% for testing. From

190 those models we calculated two metrics of the relevance of each species model for each

191 environmental variable: percentage contribution (PC) and permutation importance (PI). To

192 estimate collinearity we calculated a non-parametric correlation index between predictor

193 variables at the pixel level. Then in order to reduce the overfitting and collinearity between

194 variables, we selected the predictors with the highest contribution to the exploratory model

195 and lowest correlation index (< |0.7|). When two predictors had a high correlation index, we

196 maintained the variable with the highest contribution. Finally, we generated a final model
197 using the non-autocorrelated dataset occurrences and the selected variables from the

198 exploratory ENM (Tables S3 and S4) (Alaniz et al., 2020b, 2020a; Carvajal et al., 2019,

199 2018).

200 Prey species richness

201 We estimated prey species richness as the number of species present in each pixel, as

202 predicted by abiotic ENMs (Gherghel et al., 2018). We estimated the number of prey species

203 as a continuous variable (“continuous richness”) by adding the suitability values predicted

204 from abiotic ENMs, obtaining a raster of continuous numeric value, ranging between 0 (cells

205 with no species present) and 5 (cells with all species present) (Calabrese et al., 2014). We

206 also reclassified the continuous probabilistic predictions for each prey species into a binary

207 model (presence-absence) by considering as presence all the suitability values above the 10th

208 percentile. Then we added all the prey species binary maps, obtaining a single map of

209 potential species richness (“categorical richness”). This was done in order to make our results

210 comparable to previous studies which used binary ENMs to construct species richness maps

211 (e.g. Gherghel et al., 2018; Kershaw et al., 2013; Radosavljevic and Anderson, 2014), as well

212 as to include alternative ways to evaluate the potential spatial interaction.

213 Spatial overlap

214 We used the geographic distributions predicted by the previously generated final ENMs to

215 assess the overlap between the spatial distribution of woodpeckers and each individual prey

216 species (Fig. 1A). First we estimated the Potential Spatial Interaction (PSI) of woodpeckers

217 with each prey species to identify zones where both predator and prey are predicted to coexist

218 locally, as proposed by (Alaniz et al., 2018b). We reclassified each ENM into four levels of
219 suitability: null, low, medium, and high. Values under the 10th percentile threshold of

220 suitability were considered statistically not significant and classified as the null level, while

221 the other three levels (low, medium and high) were classified in equal intervals. Then we

222 multiplied the reclassified suitability map of woodpeckers by that of each prey species, based

223 on Alaniz et al. (2018b), assuming that the potential predator-prey interaction is proportional

224 to the product of predator and prey raster multiplication. This process generated PSI maps

225 with five potential interaction levels (labeled very low, low, medium, high, very high).

226 Finally, we quantified the area (km2) assigned to each PSI level relative to the distribution of

227 MWP.

228 Second, we applied two widely used indices to assess niche overlap between species,

229 Schoener´s “D” and Hellinger´s “I” niche similarity statistics, ranging from 0 (no overlap) to

230 1 (complete overlap) (Warren et al., 2008). Schoener´s “D” is simple and linked to biological

231 characteristics of the species, while Hellinger´s “I” does not involve any biological

232 assumptions (Warren et al., 2008). We used the “dismo” R package (Hijmans and Elith,

233 2017) to calculate those indices for the MWP and each of the prey species (Broennimann et

234 al., 2012b).

235 Third, we fitted a linear regression (LM) and estimated the Spearman correlation (rho)

236 between the maps of predicted suitability for woodpeckers and each prey species, trying to

237 identify spatial correlation between the suitability values of predator and prey. We then

238 evaluated the association between woodpecker habitat suitability and prey species richness

239 using: 1) ANOVA with multiple comparisons for categorical richness; and 2) LM and the

240 Spearman correlation for continuous richness.

241 Biotic model performance

242 We assessed the contribution of single prey species (n = 5 species) and species richness to

243 the occurrence of woodpeckers using three approaches (Fig. 1B):

244 First, we fitted univariate-biotic ENMs comparing the area under the receiver operating curve

245 (AUC) of these models. AUC provides an overall measure of model goodness of fit, ranging

246 between 0 and 1, with values > 0.8 being interpreted as good model performance (Phillips et

247 al., 2017). Single prey species and species richness were specified as single predictor

248 variables in univariate-biotic ENMs, and then as a reference (control) value we generated an

249 ANOVA to compare the AUC of those models including the AUC of the environmental

250 model of woodpeckers.

251 Second, we fitted an ENM for the MWP using all the biotic variables together, aiming to

252 identify which reached the highest percent contribution (PC).

253 Third, we developed a series of ENMs including environmental and prey variables (biotic),

254 aiming to assess the contribution of prey to the suitability model for the woodpecker in

255 comparison to environmental variables. We generated six ENMs of the MWP considering

256 the selected environmental variables (from the final model), adding: i) one prey species

257 suitability map per model as an additional predictor variable (five ENMs, one per prey); and

258 ii) an additional model considering the prey species richness map as a predictor variable (only

259 one model for prey species richness). Finally, we evaluated the PC of each variable per

260 model, comparing the biotic variable (individual prey species or prey species richness) to

261 bioclimatic, human influence and habitat variables.

262 Environmental niche overlap

263 Overlap in environmental niche space (n-dimensional hypervolume) between the MWP and

264 each of its prey species was analyzed using a Principal Components Analysis (PCA) of the

265 environmental conditions at sites with a given species present (Broennimann et al., 2012b).

266 To generate the PCA, all the species should have the same predictor dataset to allow

267 comparison, so we included the full set of predictor environmental variables in this analysis.

268 Each PCA was performed using the “ecospat” package in the R environment (Di Cola et al.,

269 2017).

270 RESULTS

271 Spatial overlap

272 Abiotic variables used in ENMs predicted well the occurrence of MWP across the Coast and

273 Andes Ranges of central Chile and north Patagonia (35° to 42°S) to the southernmost part of

274 the continent at 55°S (Fig. S2). Abiotic models also indicated that distributions of five long-

275 horned beetle species are suitable in forests between 35° to 42° S, although the ranges of only

276 three species, C. submetallicum, L. concinnus and M. magellanicus, extended to the

277 southernmost forests at 55°S (Fig. S3). These abiotic ENMs for woodpeckers and their five

278 potential prey species performed quite well (AUC > 0.89 for all models; Fig. S3 and Table

279 S4).

280 Distribution overlap between woodpeckers was greatest with three prey species, C.

281 submetallicum (48.5%), L. concinnus (41.4%) and M. magellanicus (39.8%), as estimated

282 from the PSI procedure (Table 1). The prey species with the least potential to interact with

283 woodpeckers was C. childreni, which overlapped only 17.3% of the woodpecker’s range

284 (Table 1). PSI values had a heterogeneous distribution, with higher values concentrated
285 between 35°S and 42°S for all prey species (Fig. 2). However, C. submetallicum, L.

286 conccinus and M. magellanicus also presented high levels of PSI in some southernmost parts

287 (52 ºS to 55ºS) of their respective distribution range (Fig. 2).

288 The environmental niche of the MWP showed high similarity (estimated “D” and “I” ≥ 0.50)

289 with those of prey, especially for C. submetallicum, L. conccinus and M. magellanicus (“D”

290 = 0.70, 0.66 and 0.64, respectively; “I” estimates 0.91, 0.91 and 0.89, respectively; Table 1).

291 Among prey species, C. globithorax was the least similar to woodpeckers with a “D” estimate

292 of 0.50 and an “I” estimate of 0.77. Finally, habitat suitability predicted for three prey species

293 (C. submetallicum, L. conccinus and M. magellanicus) had the highest correlation

294 coefficients with the woodpecker’s suitability (rho= 0.80, 0.79 and 0.73, respectively) and

295 explained variance of the LM with the woodpecker’s suitability (R 2= 0.54, 0.60 and 0.52,

296 respectively; Table 1). In contrast, the distribution of C. globithorax explained the smallest

297 proportion of variance in habitat suitability for woodpeckers (R 2=0.3; Table 1).

298 The number of prey species co-occurring with MWP varied spatially but peaked at mid-

299 latitudes (37 to 42°S), and the southernmost part of the range (52 to 55°S; Fig. 3A). Only

300 one-third (32%) of the woodpecker’s range was predicted to support more than three prey

301 species, whereas roughly the same (37%) was predicted to have only one or two (Fig. 3A).

302 Continuous richness exhibited a pattern similar to that of categorical richness, with high

303 values (>2.5) concentrated from central Chile to north Patagonia (35 to 42°S) as well as the

304 southernmost zone (52°S to 55°S; Fig. 3B); low values (<2.5) occurred between 45 and 50°S.

305 Habitat suitability for woodpeckers increased significantly as prey species richness increased

306 (RSE = 0.16, df = 5, SS = 48.3, p < 0.001), with suitability values doubling when prey species

307 richness increased from one to five (Fig. 3C and S4). The predicted prey species richness
308 was significantly correlated with woodpecker suitability (r = 0.94, p < 0.001), and accounted

309 for 65% of the variance (Fig. 3D).

310 Biotic model performance

311 Univariate biotic ENMs varied significantly in their performance in the estimation of

312 woodpecker occurrence (Fig. 4 and S5). The reference abiotic ENM for woodpeckers (the

313 “Environment” model) had the best model performance (AUC= 0.89 ± 0.01, Fig. 4).

314 However, the univariate biotic ENMs of three prey species (C. submetallicum, L. concinus

315 and M. magellanicus) had good fits, with AUC > 0.8 (AUC= 0.84 ±0.01, 0.86 ±0.02 and 0.86

316 ±0.02, respectively). Although the biotic ENM of prey species richness had good

317 performance (AUC = 0.83 ±0.02), its overall performance was lower than that of the three

318 species with the highest AUC (Fig. 4). Finally, the biotic ENMs for C. childreni and C.

319 globithorax had lower performance in estimating woodpecker occurrence (mean AUC= 0.80

320 ±0.02 and 0.78 ±0.02, respectively; Fig. 4).

321 M. magellanicus reached the highest PC with 29.6% when all the biotic variables were

322 included in the same ENM of the MWP, followed by L concinnus and prey species richness

323 with 29% and 25.4%, respectively (Table S5). When each specific prey ENM was added as

324 a biotic variable together with the environmental predictor set, the prey was the most

325 significant in three of the five prey ENMs, contributing 67.9, 65.8 and 60.8% to the cases of

326 L. concinnus, M. magellanicus and C. submetallicun, respectively. Prey species richness

327 reached 63.5% of PC, while C. globithorax and C. childreni did not have a PC significantly

328 higher than that of the environmental variables (Fig. 5). In the control model (with

329 environmental variables only) bioclimatic and vegetation variables reached the highest PC

330 values, with 40.8 and 36.2%, respectively.

331 Environmental niche overlap

332 All prey species had environmental niches that overlapped with that of MWP (Fig. 6 and S6).

333 However, except for L. conccinus, the environmental niches of other beetles were smaller

334 than and nested within the niche of woodpeckers (Fig. 6). The niche of L. conccinus was the

335 most similar to the MWP, having an almost complete overlap in both axes of the PCA (Fig.

336 6). The niche of M. magellanicus was the second most similar, differing in axis 2 where M.

337 magellanicus is mainly distributed in the negative values, associated with higher values of

338 temperature seasonality (Bio 4), temperature annual range (Bio 7) and mean diurnal range

339 (Bio 2) (Fig. 6 and S6). The niche of C. childreni is nested within the MWP niche, and is

340 distributed mainly in positive values of axis 1, which is associated with highest values of

341 coldest quarter temperature (Bio 11), precipitation of wettest quarter (Bio 16) and

342 precipitation of coldest quarter (Bio 19) (Fig. 6 and S6). The niche of C. globithorax was

343 partially nested within the MWP niche, and is distributed mainly in positive values of axis 2

344 of the PCA, which is determined by the mean diurnal range (Bio 2), max temperature of

345 warmest month (Bio 5) and precipitation seasonality (Bio 15) (Fig. 6 and S6). Finally, the

346 niche of C. submetallicum is also nested within the MWP niche, and is distributed mainly in

347 negative values of axis 1 in the PCA which, is associated with the highest values of mean

348 temperature of driest quarter (Bio 9) and mean temperature of warmest quarter (Bio 10) (Fig.

349 6 and S6).

350 Discussion

351 Predator–prey relationship

352 The geographic distribution and environmental woodpecker niche space was more consistent

353 with large-sized long-horned beetle species, known to be the most important and preferred

354 prey items, than with general prey species richness (Espinosa et al., 2016; Ojeda and

355 Chazarreta, 2006; Vergara et al., 2016; Winkler et al., 1995). This finding supports the

356 specialist behavior of this predator, highlighting the role of some prey items mainly in the

357 south of their geographic distribution. Since prey item larvae are similar in size, the specialist

358 behavior of the predator and its niche overlap with prey should be determined by the

359 geographic distribution of the prey rather than the morphological traits of larvae.

360 Fine-scale studies support the role of M. magellanicus as the main prey of the MWP in the

361 southernmost sub-Antarctic forests (Vergara et al., 2017b, 2017a; Vergara and Schlatter,

362 2004). M. magellanicus and the MWP share their preferences for habitat features (e.g. tree

363 decay); the MWP uses those features to guide movements and foraging decisions within its

364 home range (Soto et al., 2017; Vergara et al., 2016). The close trophic relationship suggests

365 that MWP have specialized locally in the search and capture of larvae of M. magellanicus on

366 their primary host (Nothofagus trees) (Cerda and Angulo, 2000; Vergara et al., 2017a;

367 Vergara and Schlatter, 2004). This trophic behavior reported by field studies of the MWP

368 and supported here contrasts with other woodpecker species worldwide and in Chile, which

369 have more flexible and generalist foraging behavior (e.g. the Chilean flicker forages on ants,

370 coleopterans and a wide variety of other small insects). Askins (1983) reported that

371 woodpeckers tend to have a wider trophic breadth in tropical biomes than in temperate ones.

372 Our results suggest that the broad-scale geographic distribution and niche overlap between

373 predator and prey are consistent with previous studies supporting close, fine-scale

374 specialization of MWP on particular prey items (Cerda and Angulo, 2000; Vergara et al.,
375 2017a; Vergara and Schlatter, 2004). The higher AUC reached by the woodpecker niche

376 model when particular prey species were used as the only predictor variable (univariate biotic

377 ENM) compared to prey species richness is also consistent with a specialist behavior

378 (Gherghel et al., 2018; Holt and Barfield, 2009). Our results also showed that each of the

379 biotic predictors (prey) alone could reach significant accuracy in predicting the predator

380 niche and its spatial distribution, presenting very high values of AUC (>0.85). Our finding

381 that a single biotic variable could reach similar accuracy to a complete environmental dataset

382 reinforces the hypothesis presented in this study. Also, the contribution of particular prey

383 species as biotic variables was twice as high as bioclimatic or vegetation variables,

384 highlighting the importance of these prey species in the niche of a specialist predator. The

385 relationship between the MWP and its prey may respond to habitat variables (e.g. forest),

386 affecting predator and prey species at the same time. However, our findings support the key

387 role of prey species in the niche and distribution of the MWP, due to the highest AUC reached

388 by prey species as predictors and the high relative contribution of prey species in comparison

389 with habitat variables.

390 Biogeographical predator-prey factors

391 We found that the ENM overlap between the MWP and its prey could be influenced by the

392 climatic configuration of Chile. We found that some prey species are more associated with

393 the Mediterranean climate of central-south Chile (30° to 40°S latitude; C. globithorax, C.

394 submetallicum and C. childreni), determined by their link with high seasonality, wide annual

395 temperature range and the distribution of precipitation and temperature (dry, hot summer;

396 wet, cold winter) (Fig. 3 and S6). L. conccinus and M. magellanicus presented a wider niche

397 and spatial distribution (south of 40°S), being present in the southernmost MWP distribution.
398 South of 40°S biodiversity has been historically determined by glaciations and postglacial

399 recolonization, resulting in a contraction and expansion of forest habitat (Gutiérrez-Tapia

400 and Palma, 2016; Segovia et al., 2013). This phenomenon produces a latitudinal decrease in

401 species diversity which has been described for many groups, as shown here for long-horned

402 beetle species (Gutiérrez-Tapia and Palma, 2016; Segovia et al., 2013). This determines that

403 the woodpecker´s distribution in southern Patagonia (42 to 55°S) is more closely related to

404 the distribution of certain prey species (L. concinus and M. magellanicus). Long-horned

405 beetles are highly specialized in host tree species (Saint-Germain et al., 2004), thus it is

406 highly probable that they colonized south of 40°S after the last glacial maximum (LGM

407 17,000 ybp), following the expansion of their host trees (Segovia et al. 2013). This forest

408 expansion south of 40°S after the LGM offered the MWP the opportunity to expand and

409 adjust its geographical distribution (Hammond et al., 2007; Flaxman & Lou, 2009).

410 Conservation implications

411 Our findings generate a series of implications for conservation. First, usually species threat

412 level assessments based on ENM consider different phenomena such as habitat loss,

413 fragmentation and climate change directly effecting the target species (Carvajal et al., 2018;

414 Hill et al., 2017). However, the threat level of highly specialist species could be determined

415 by other species that have a close relationship with them, which requires integrating these

416 “essential species” into the assessments and strategies for conservation. Second, species

417 survival across its geographical range could rely on the preservation of other species, which

418 means that by preserving the prey we may preserve predators. However, this relationship

419 needs to be tested at local and biogeographical scales, which can justify the inclusion of other

420 species in the conservation actions for some main target species. Third, several studies have
421 addressed future shifts in species distribution ranges due to climate change, projecting

422 massive migrations searching for suitable habitat conditions (Hill et al., 2017; Pecl et al.,

423 2017). However, this approach based mainly on environmental factors does not consider the

424 complexity of ecological networks (e.g. predator-prey, mutualism, parasitism), which makes

425 the projection of other ecological impacts difficult at wider scales.

426 Using ENM to study trophic interactions

427 Here we combined multiple methodological approaches to test prey-predator interactions

428 from an ENM approach, highlighting the high potentiality of this methodological framework

429 to study ecological interactions. However, some methodological and theoretical assumptions

430 need to be discussed.

431 One methodological assumption is related to occurrence for ENM. Taxonomic bias in species

432 sampling is usually an important limitation in the development of ENM for particular groups

433 of species, where insects have remained neglected compared to other groups (e.g. birds,

434 mammals, plants) (Troudet et al., 2017). Our models reached good fits, which could be

435 produced by the homogeneous distribution of occurrences across the geographical range of

436 the modeled species (Fig. S1). This was possible by including data from multiple

437 entomological collections across different zones of Chile, and reduction of the spatial

438 autocorrelation (see methods). It is necessary to develop spatially systematic monitoring

439 programs of insect species, increasing the availability of data for future modelling studies.

440 The use of different methodologies to determine if ecological interactions are more likely to

441 take place or not may help to reduce biases and spurious findings derived from the application

442 of only one method (PCA, similarity indices, univariate biotic ENM, correlations between
443 suitability maps and potential spatial interaction PSI, among those used here; e.g. Warren et

444 al. 2008; Broennimann et al. 2012; Anderson 2017; Alaniz et al. 2018b). Previous

445 methodologies have been used to estimate the spatial interaction or the overlap in the

446 distribution of species (Alaniz et al., 2018b; Warren et al., 2008) based on the potential co-

447 occurrence of the organisms. However, this co-occurrence may not be equivalent to the

448 effective interaction, because species could differ in the use of habitat, activity times or

449 exploited resources (Araújo and Rozenfeld, 2014; Pollock et al., 2014). The ecological

450 knowledge of the species is essential to understand better and confirm the existence of an

451 effective interaction, which if true can be extrapolated to wider geographical scales

452 (Anderson, 2017). The link between ecological knowledge and this type of analysis could be

453 useful to study other type of interactions such as: A) future shifts in the geographic patterns

454 of biological control of herbivorous insects on weeds due to climate change (Alaniz et al.,

455 2020a); B) the negative effects of invasive species on local ecological assemblages (Alaniz

456 et al., 2018b); and C) the spatial representativeness of protected areas preserving ecological

457 interactions such as pollination, seed dispersal, predation.

458 Niche overlap analyses are commonly applied with two different approaches, A) to evaluate

459 the niche share or partitioning of two species that use the same resource (Scheffer and van

460 Nes, 2006), and B) to evaluate the environmental niche similarity or dissimilarity between

461 two or more species at biogeographic scales (PCA-env; Broennimann et al., 2012a). The

462 latter approach has been used to evaluate the level of environmental niche similarity for

463 species of different trophic levels that interact in the same ecological network (e.g. parasite-

464 host, predator-prey, mutualist and commensal species; Aryal et al., 2016; Gherghel et al.,

465 2018; Vasconcelos et al., 2017). Here we considered the second approach (B) to evaluate the
466 similarity between MWP and its preferred prey. However, this analysis is usually based only

467 on abiotic variables under a Grinnellian niche approach (Soberon and Nakamura, 2009),

468 which does not fully address the biotic components of the niche (Eltonian niche; Soberón,

469 2007). We incorporated variables as proxies of biotic components of the habitat linked to

470 forest (productivity, senescence, canopy cover and canopy humidity), soil organic carbon

471 and disturbances (human footprint index, burned area index), aiming to expand the focus of

472 this type of analysis.

473 We found that ENMs can be useful to infer trophic relationships and ethological traits of

474 species. Finally, we believe that the methodological framework may be useful to understand

475 potential prey-predator interaction in other biomes, and can be applied to estimate other types

476 of interspecific interactions such as parasitism, competence, mutualism, pollination, etc.

477 Acknowledgments: This work received support from FONDECYT 1180978 and Fondo

478 Fortalecimiento USA1799-28 (USACH), the Rufford Foundation, the Andrew W. Mellon

479 Foundation, Advanced Human Capital Program – CONICYT, and the Athena Grant from the

480 Cornell Lab of Ornithology. We are grateful to W. Hochachka and M. Nazar for advice and

481 technical support. Alberto J. Alaniz and Mario A. Carvajal were supported by CONICYT-

482 PFCHA/ Doctorado Nacional 2020-21201496 and 2020-21201494, respectively.

483 Author contribution statement: AJA designed the idea, developed all the analyses and

484 wrote the manuscript. MAC and PMV contributed with the writing process and analysis; AF,

485 ARO, GES and ADR reviewed the manuscript and contributed to the discussion section.

486 Data availability Statement: All data are available by e-mail request to the corresponding

487 author.
488

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750

751
752 Table 1. Potential spatial interaction (PSI), niche similarity indexes and suitability
753 correlations between MWP and its prey species. Potential spatial interaction of each is
754 expressed as the percentage of the total distribution of the MWP (total area = 145906 km2*).

Niche Suitability
Potential spatial interaction (%)
similarity correlations

Very Very
Model Low Medium High Total “D” “I” R2 rho
low High

C. lobithorax 5.12 9.01 8.18 6.16 3.42 31.89 0.50 0.77 0.30 0.74

C. submetallicum 10.10 13.10 12.81 8.50 3.96 48.48 0.70 0.91 0.54 0.80

C. childreni 2.73 4.64 5.19 3.35 1.36 17.26 0.56 0.82 0.46 0.80

L. concinnus 10.15 10.65 9.37 6.28 4.97 41.42 0.66 0.91 0.60 0.79

M. magellanicus 9.26 11.83 8.99 5.75 3.54 39.37 0.64 0.89 0.52 0.73

755
756
757
758 Figure 1. Methodological framework used in the study showing sequentially the following
759 steps: A) Spatial overlap analysis between MWP (in red) and prey species (individually in
760 blue and richness in green), showing the analysis applied. B) Biotic model performance
761 showing the three methodological approaches to evaluate the contribution of prey species to
762 the ENM of MWP. C) Environmental niche overlap analysis.
763
764 Figure 2. Potential spatial iteration (PSI) levels between predator MWP (Campephilus
765 magellanicus) and five prey species (long-horned beetles), from null to very high.
766
767 Figure 3. A) Map of the categorical prey species richness, B) Map of continuous prey species
768 richness, C) Boxplot of woodpecker suitability values per prey species richness level
769 (significant differences between levels are shown with different letters; Appendix Figure S2)
770 D) Scatterplot of woodpecker suitability and relative prey abundance, including a regression
771 line and confidence intervals.
772
773 Figure 4. PCA plots of environmental niche requirements of MWP (red) and each prey
774 species (long-horned beetles; blue); this figure shows the overlapping of environmental
775 niches considering the two first components (axes 1 and 2) of both interacting species.
776 Additionally, the Z axis shows the predicted suitability scaled from 0 to 1 in each component,
777 axis 1 (upper graph) and axis 2 (right graph). The contribution of each environmental variable
778 in each component for each pair of species appears in Appendix Figure S6.
779
780 Figure 5. Box-plot comparing the AUC of each model generated. AUC differences between
781 models were compared using ANOVA and the Tukey test for multiple comparisons. *Prey
782 species richness corresponded to the “continuous richness”.

783
784 Figure 6. Mean percent contribution of each variable within ENMs of MWP, integrating
785 prey species as predictor.

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