1 Old-growth structural attributes associated conservation giant subtropical conifers

2 Marcelo Callegari Scipioni1*, Pedro Higuchi2, Guilherme Diego Fockink3,

3 Craig D. Allen4

5 1
Federal University of Santa Catarina, Department of Agriculture, Biodiversity and

6 Forestry, C.P. 101, 89520-000, Curitibanos, SC – Brazil

7 *Corresponding author: marcelo.scipioni@ufsc.br

8 2
State University of Santa Catarina, Departament of Forestry, 88.520-000, Lages, SC –

9 Brazil. higuchip@gmail.com

10 3
State University of Santa Catarina, Master´s Program in Forest Engineering, 88.520-

11 000, Lages, SC – Brazil. guilhermefockink@gmail.com

12 4
Department of Geography and Environmental Studies, University of New Mexico,

13 Albuquerque, NM 87131 USA. craigdallen@unm.edu

14

15 Abstract

16 Giant Araucaria trees in Brazilian Atlantic forests today are rare but remain critically

17 important for structuring these ecosystems, providing unique and rare habitat elements

18 that can serve as points of reference for their management. Old-growth Araucaria trees,

19 with their complex crowns and big trunk cavities, supply more important ecological

20 services than smaller or even comparable-sized trees with simple crowns. Forest

21 ecology managers lack information on the old-growth structures of Brazilian Araucaria

22 forest, their ecological importance, and their potential societal values and uses. In this

23 study we investigated the old-growth attributes of Araucaria angustifolia and relate

24 their wide structural variability to ecological management goals. In this study we used

25 currently available data on the last giant Araucaria trees and compared with young and

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26 mature trees, as well as our own new records, from large trees of 1.6 to 3.2 m diameter

27 in the Araucaria forests in southern Brazil. In order to quantify the structural attributes

28 of these remnant trees, their main trunks, any reiterated canopy trunks, and trunk

29 cavities were measured for diameters, heights, and volumes. These old-growth trees had

30 an average height of 38.4 m, and total tree volumes ranged from 21.5 to 106.6 m3, with

31 the wood volume of reiterated trunks averaging 4.4% of the total volume in giant trees.

32 The biggest reiterated trunk was 1.1 m in diameter and 17 m long, which is larger than

33 most mature Araucaria trees. Number of cavities and number of reiterated trunks were

34 all significantly related to the diameters of these large remnant Araucaria trees; both

35 features are absent in Araucaria <50 cm in diameter. The maximum diameter and

36 average length of reiterated trunks were correlated with the number and size of trunk

37 cavities. Commercial wood values and uses are limited for all trees with main trunk

38 diameters exceeding 1.5 m due to large internal cavities – however, these rare, relictual

39 old-growth structures are of high ecological value for the local fauna and flora. Old-

40 growth giant Araucaria also have unrealized potential for multiple societal uses and

41 benefits.

42 Keywords: Tree size; Giant trees; Ancient trees; Tree cavities; Reiterated trunks;

43 Araucaria forest

44

45 Introduction

46 Giant trees of the gymnosperm species Araucaria angustifolia were once

47 common in southern Brazil, but large trees and old-growth forests of this species are

48 under critical threat of extinction (Thomas 2013) due to drastic reduction of their

49 populations through deforestation and logging that have greatly altered their stand

50 diameter structures (Souza 2007; Souza et al. 2012) and massively reduced the numbers

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51 of large individuals in the Araucaria forests, with modern records for only 21 giant trees

52 (Scipioni et al. 2019a; Scipioni 2019). The majority of these remaining giant trees are in

53 small forest fragments that do not represent functioning old-growth forests.

54 A. angustifolia, commonly known as Parana pine, occurs in the southern and

55 southeastern plateaus of Brazil, in the southeast of Paraguay, and the northwest of

56 Argentina, at elevations between 400 to 1800 m a.s.l. Mature individuals are from 20 to

57 45 m in height with a single, erect, and cylindrical trunk measuring from 0.5 to 3.2 m in

58 diameter (Backes and Nilson 1983; Scipioni et al. 2019a), and able to exceed 400 years

59 of age (Carvalho 2003; Oliveira et al. 2010). The Araucaria tree has a chalice-shaped

60 crown, with at least two thirds of it normally lacking lateral branching, a structural form

61 unique among the conifers (Seitz 1986; Eckenwalder 2009; Farjon and Filer 2013).

62 Large Araucaria trees often have reiterated trunks that are popularly called

63 “double-crowned araucaria trees”, although old-growth Araucaria actually may have

64 multiple reiterated trunks, where each one has its own separate crown. Van Pelt and

65 Sillett (2008) provide this precise definition of “reiterated trunks” for tall old-growth

66 conifers from western North America: “The reiterated trunk is any trunk within a tree

67 other than the main trunk. As the term ‘‘reiterate’’ means ‘‘to repeat,’’ it is referring to

68 the primary architectural model of tree growth. Hence, a reiterated trunk is a repeat of

69 the tree growth form within a tree crown. In many conifers, reiterated trunks retain the

70 appearance of young trees growing within the crown of a larger tree, although their

71 branches are asymmetrically (mostly away from the main trunk) oriented and usually

72 extend to their base. Old-growth Araucaria in southern Brazil share these distinctive

73 architectural structures with such well-known giant conifers as Picea sitchensis (Kramer

74 et al. 2019), Pseudotsuga menziesii (Van Pelt and Sillett 2008), Sequoia sempervirens

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75 and Sequoiadendron giganteum (Sillett et al. 2015), with the last two reaching heights

76 of >90 m and ages of >2000 years.

77 Other characteristics of tall and old conifers are distinctive cavities at the main

78 trunk's base and along its length. Giant Araucaria trees have very large trunk cavities,

79 with openings between 1 to 2 m wide and of up to 4.4 m in height. The internal areas of

80 these cavities range from 3 m2 to 6 m2. The ceiling height in the largest Araucaria tree

81 cavities measures 14 meters along the central main trunk axis (Scipioni et al. 2019a).

82 The resulting loss of tree biomass or carbon mass from these cavities, however has

83 ecological benefits from the increased habitat value for big animals and

84 microenvironments for nesting and sheltering habitat of numerous animal species and

85 epiphytes (Remm and Lõhmus 2011; Lindenmayer et al. 2012a; Pinho et al. 2020).

86 Trunk cavities in giant trees represent keystone vegetation structures for

87 biodiversity (Remm and Lõhmus 2011) and also for forest management, with the risk of

88 their economic depreciation increasing due to the emergence of wood imperfections.

89 The traditional forestry practices of cutting large-diameter trees, with or without

90 cavities, for timber and regularly replacing them with younger trees (Percel et al. 2018;

91 Wu et al. 2020), does not take into account their high maximum growth and carbon

92 sequestration potentials (Sillett et al. 2010), resulting in forests without or with few

93 large trees, and thus also missing their distinctive and ecologically important old-growth

94 structures.

95 The rapid and increasing loss of large-diameter trees is a global phenomenon

96 (Lindenmayer et al. 2012b; Wu et al. 2020), often accompanied by our lack of

97 knowledge about their old-growth attributes (Scipioni et al. 2019b). In several areas not

98 yet intensively explored by scientists, such as some forests of the Amazon (Gorgens et

99 al. 2019) and Borneo (Shenkin et al. 2019), recent discoveries of surprisingly-tall trees

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100 over 60 m in height have been made. For some threatened tropical tree species, e.g.,

101 Araucaria angustifolia and Ocotea porosa for the Brazilian Atlantic forest, traces of

102 preserved trunks of monumentally large specimens have been found but at present there

103 are only a few records of the last standing giant trees (Scipioni 2019; Scipioni et al.

104 2019a).

105 Giant Araucaria trees show a great plasticity of crowns and reiterated trunks.

106 They look quite different from younger Araucaria trees that lack reiterated trunks or

107 well-developed crowns. In addition, huge old Araucaria trees have several other unique

108 structural attributes such as extensive buttressing, large and numerous trunk cavities of

109 a considerable internal volume, much lateral branching, and deeply fissured bark

110 (Lindenmayer and Laurance 2016; Scipioni et al. 2019a). The above characteristics may

111 assist in the identification and classification of old-growth forest patches and old trees in

112 the Brazilian Atlantic forest (Van Pelt 2001; Van Pelt 2007; Chiavetta et al. 2014). The

113 frequency and horizontal spatial proximity (e.g., 10 to 20 m) between giant trees were

114 both previously much greater in old-growth Araucaria forest, being important elements

115 to identify and characterize such old-growth forests (Scipioni et al. 2019a). But the

116 definition of old-growth forest is not simple and precise in Araucaria forest. It is

117 necessary to use a variety of characteristics or criteria because there is wide variability

118 in values for a given characteristic. Some key, objective characteristics of old-growth

119 forest, according Franklin and Spies (1984), are: two or (commonly) more tree species

120 with a wide range in size and age and often including a long-lived seral dominant and

121 shade-tolerant associate; a multilayered canopy with individual live trees that are either

122 old (>200 years) or have become large (1.0 m diameter at breast height – DBH); and

123 significant coarse woody debris, including snags and downed logs; and snags and logs

124 of large dimension.

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125 Recent silvicultural research is beginning to show how natural Araucaria forests

126 in southern Brazil can be managed for sustainable harvests and provide some

127 environmental services (Longhi et al. 2018; Costa et al. 2020; Curto et al. 2021);

128 however, without knowledge and consideration of the old-growth attributes of rare

129 relictual Araucaria trees, this work could threaten the permanent loss of the few

130 remaining large trees in Araucaria forest types, along with their economic, ecological,

131 and social potential.

132 Recognition of old-growth tree attributes becomes especially important in

133 fragmented landscapes (Chiavetta et al. 2014). Little is known about the crown and

134 trunk cavity structures of giant Araucaria tree, as well their size and form. The

135 development of such information will increase understanding of the physiognomic,

136 biomass (carbon sequestration), and biodiversity values and potentials of these large

137 ancient trees, as well as improve the identification of remaining old-growth forests

138 patches within largely human-dominated landscapes (Franklin and Spies 1984; Lutz et

139 al. 2018). The objective of our study is thus to establish old-growth attributes from

140 ground-based measurements, including: 1) quantitatively distinguish the remnant young

141 trees from the last giant Araucaria trees; 2) determines particular measures of tree size

142 that can be used as predictors for old-growth attributes to the conservation of big trees,

143 e.g., reiterated trunks and cavities in the base of the main trunk; and 3) infer when the

144 attributes of old-growth develop relative to the growth in diameter in Araucaria trees.

145

146 Materials and methods

147

148 Selection of trees

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149 Following Scipioni et al. (2019a), a diameter at breast height (DBH, 1.3 m) of

150 greater than or equal to 1.50 m was the selection criterion for giant Araucaria trees.

151 Based on forest inventory sampling efforts to find the last giant Araucaria trees over the

152 past five years, in all 16 trees were studied (Table 1, Fig. 1). Three new records of large

153 trees also were included in this study, in addition to those previously found by Scipioni

154 et al. (2019a). Eight large trees with overlapping canopies that were visually obscured

155 and thus difficult to measure were not included in this study. Only state and locality

156 names and geographic coordinates are provided, rather than the individual tree names.

157 For additional information on Brazilian giant trees see Scipioni et al. (2019a) and the

158 online platform www.arvoresgigantes.org. Young and mature trees with diameters less

159 than 1.5 m in diameter were selected at different sites. Four sites in Araucaria tree

160 plantations, three sites in natural forest (Table 2, Fig. 1) and isolated large Araucaria

161 trees in different sites too were also sampled (Appendix A), totalling 1,247 Araucaria

162 trees.

163

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165 Fig. 1. Study sites and the giant Araucaria trees found in Araucaria forests of southern

166 Brazil.

167

168 Table 1. Location of the giant Araucaria trees found in southern Brazil (Scipioni et al.

169 2019a).

Locality/State Tree code Latitude Longitude Altitude

Castro/PR Castro 25° 1'14.85"S 49°56'25.80"W 986 m

Chopinzinho/PR Chonp 25°55'42.96"S 52°22'3.54"W 828 m

Canela/RS Canel 29°21'4.75"S 50°50'2.52"W 781 m

Nova Petrópolis/RS NovaP 29°21'6.69"S 51° 3'7.06"W 731 m

Campo Belo do Sul/SC* CamBS 27°58'0.07"S 50°49'20.41"W 845 m

Caçador/SC Caca1 26°51'51.15"S 50°56'31.40"W 1050 m

Caçador/SC Caca2 26°51'51.15"S 50°56'31.40"W 1050 m

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 Caçador/SC Caca3 26°51'51.15"S 50°56'31.40"W 1050 m

Fraiburgo/SC* Fraib1 27° 1'2.98"S 50°55'36.42"W 1056 m

Fraiburgo/SC* Fraib2 27° 1'2.98"S 50°55'36.42"W 1056 m

Fraiburgo/SC Fraib3 27° 1'2.98"S 50°55'36.42"W 1056 m

São José do Cerrito/SC* SaoJC 27°36'57.10"S 50°42'58.44"W 902 m

Santa Terezinha/SC SantT 26°47'48.39"S 50° 0'19.84"W 627 m

São Joaquim/SC SaoJ1 28°9'29.87"S 49°47'50.46"W 1345 m

São Joaquim/SC SaoJ2 28°22'51.72"S 49°59'22.08"W 1240 m

São Joaquim/SC SaoJ3 28°18'48.40"S 49°57'4.21"W 1250 m

170 *New records.

171

172 Table 2. Location of the young and mature trees in plantation (P) and natural forest

173 (NF) Araucaria.

Locality/Site name/Land use n Latitude Longitude Altitude

CS/Chata/P 43 27°56’59’’S 50°48’59’’W 920 m

CS/Fundo das Canoas/P 73 28°01’49’’S 50°51’16’’W  850 m 

CS/São Judas/P 44 50°47’21’’W 870 m

28°01’51’’S
CS/Gateados Florestal/NF 35 27°59'25"S 50°48’41’’W 967 m

CT/Forest Experimental/UFSC/P 928 27°19'08.3’’S 50°42’36.7’’W 832 m

CT/SC Trilha ecológica 67 27°17’22’’S 50°32’09’’W 1050 m

UFSC/NF

PERF/Parque Ecológico René 34 27° 1'5.83"S 50°55'36.07"O 1048 m

Frey/NF

174 Legend: Campo Belo do Sul (CS), Curitibanos (CT) and Fraiburgo (PERF).

175
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176 Dendrometry

177 The circumference of tree main trunks at breast height (1.30 m), the total height,

178 and the volume were measured following the methodologies in Van Pelt (2001), Van

179 Pelt et al. (2004), and Scipioni et al. (2019a). Measuring tape and dendrometers were

180 used. Tree volumes were determined by measuring diameters at various heights using a

181 laser dendrometer (Criterion RD 1000; Laser Technology, Inc.) installed on a leveled

182 tripod. Reiterated trunks in Araucaria considered how lateral or vertical these structures

183 were relative parallel to the main trunk (Fig. 2), and had to exceed 0.2 m of vertical

184 height,  10 cm in basal diameter, and insertion points greater than 2 m in height up the

185 main trunk. Total heights and the heights of the insertion points of reiterated trunks

186 were also measured. Trunk volumes that included diameters of extremities in each

187 section were calculated using the Smalian method (Van Pelt 2001). For reiterated trunks

188 only, a single diameter reading was taken in the centre of the section, using the Huber

189 method (Van Pelt 2001). The total tree volume was a sum of the main trunk and the

190 reiterated trunk volumes. Total tree heights were measured using a TruPulse 200B

191 (Laser Technology, Inc.) range finder that was positioned at ground level, creating a

192 90° angle (vertical distance) and targeting the tops of the highest branches. This

193 methodology was used for verification of measurements when a horizontal viewing

194 distance for an accurate measurement was not sufficient (Scipioni et al. 2019a).

195 The surface areas of the cavities at the base of the main trunks were measured,

196 localized on base ground of the trunk up to a height of 6 m. Cavity surface areas were

197 measured using metric tapes and TruPulse 200B rangefinder. Only cavities of natural

198 origin formed by scar wounds and stub wounds were considered – these normally

199 originate from damage by agents of wounding (treefall, lightning, fire, animals, etc.)

200 that allows entry of a fungal or bacterial infection near the damage site, which then

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201 spreads multiple directions into the heartwood (Shortle and Dudzik 2012). Trees with

202 man-made cavities were not considered, including damage that caused cavities for

203 assessing the viability of logging by means of straight cuts by axes or chainsaws

204 (Scipioni et al. 2019a). Photographs of the trunk bases and crowns trees were taken to

205 create scale drawings, as in Fig.2. The illustrations of the tree bases also included a

206 profile of a person 1.8 m tall to show scale (Van Pelt 2001). The images were handled

207 in Photoshop and drawn using CorelDraw X6 software.

208 The following four variables in giant trees were used for the main trunks:

209 diameter - DBH (m), height - H (m), volume - Vol. (m 3), and form factor - f1,3. We used

210 two variables to describe the tree cavities: number of cavities – NCav, and open area of

211 the cavities at the base of the main trunk (m 2) - BACav. For the reiterated trunks, we

212 used twelve variables: number of reiterated trunks - NTR, total volume of the

213 reiterated trunks - VolTR (m3), average diameter - ADRT (m), maximum diameter -

214 MaxDRT (m), average height at the insertion to the base reiteration trunks to the main

215 trunk - AHRT (m), maximum height at the insertion base of the reiterated trunk at main

216 trunk - MaxHRT (m), minimum length of the reiterated trunk - MinLRT (m),

217 maximum length of the reitrated trunk - MaxLRT(m), basal diameter of each reiterated

218 trunk - RTDn (m2), top height of each reiterated trunk in relation to the main trunk -

219 HfRTn (m), and length of each reiterated trunk (m) - LRTn for the reiterated trunks.

220 Further details of the positions and measurements of the variables are found in Fig. 2.

221 Young and mature trees with diameters less than 1.5 m in diameter had the following

222 variables measured: diameter at breast height; total tree height; and the variables related

223 to cavities and reiterated trunks, when these were present.

224

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226 Fig. 2. Measurement positions of the variables for giant Araucaria trees and images of

227 different basal cavities in trunk, as examples of Caçador (Caca1, Caca3) and São

228 Joaquim (SaoJ3) trees, SC.

229

230 Data analysis

231 Comparisons between young, mature, and giant trees (n= 1,247) were made

232 using diameter at breast height (DBH) as an independent variable, versus the size and

233 quantity of cavities at the base of the main trunk and reiterated trunks as dependent

234 variables. The polynomial models and their plots were performed using PAST software

235 (Hammer et al. 2001). The models were aimed to identify the diameter of the increment

236 of these old growth attributes: number and size of cavities and reiterated trunks.

237 Giant Araucaria trees (DBH >1.5 m) are visually apparent in the forest canopy,

238 allowing initial identification of these large trees in the landscape. The mean values and

239 standard deviations of giant tree attributes were calculated for the following variables:

240 diameter, length, volume, and height of insertion of the reiterated trunks. Data on tree

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241 diameters, heights, and cavities were used to assess the relationships between tree size

242 and the number and sizes of old-growth structures. The variables tested for correlations

243 were DBH, H, Ncav, BACav, NTR, AHRT, MaxHRT, MinLRT, MaxDRT, and the

244 average length of the reiterated trunk (ALRT). Pearson correlations were computed in

245 Excel at a 5% significance level. To understand the ordering of old-growth attributes, a

246 single data matrix was formed for the 16 trees with their 18 biometric attributes

247 described above. After removing multi-collinear variables based on the Variance

248 Inflation Factor (VIF > 10), we performed a Principal Components Analysis (PCA). For

249 this, all variables were scaled to zero mean and unit variance. The multivariate analysis

250 was performed using R software (R Development Core Team 2020) along with ade4

251 (Dray and Dufour 2007), corrplot (Wei and Simko 2017), factorextra (Kassambara and

252 Mundt 2020), and usdm (Naimi et al. 2014).

253 Results

254 Dendrometry of Araucaria trees

255 Araucaria trees have a growth potential that can exceed 3 m in diameter and 40

256 m in height (Fig.3 A and B). Despite this growth potential, few trees were registered

257 with dimensions from 1.5 m in diameter and heights greater than 30 m (Table 3). The

258 reiterated trunks were recorded from 0.78 cm in DBH. The number and size of the

259 reiterated trunks increases with the size of the tree in diameter (Fig. 3 C, D), although

260 some giant Araucaria do not have reiterated trunks, demonstrating that they maintained

261 the apical growth of the crown. However, a history of structural damage favors the

262 formation of reiterated trunks in large Araucaria individuals, and most of the largest

263 Araucaria trees are characterized by multiple reiterated trunks.

264

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265 Table 3. Dendrometric measurements of the young and mature Araucaria trees in

266 plantation (P) and natural forest (NF), Campo Belo do Sul (CS), Curitibanos (CT) and

267 Fraiburgo. *Standard error.

Locality/Site name/Land use
CS/Chata/P
CS/Fundo das Canoas/P
CS/São Judas/P
CS/Gateados Florestal/NF
CT/Forest Experimental/UFSC/P 0.19±0.42 9.8±1.8
CT/SC Trilha ecológica
UFSC/NF
PERF/NF
Natural Forest (n= 143)
Plantation trees (n= 1088)
Giant trees (n= 16)
268
DBH Total height Min. Max Min. – Max
(m)* (m) * DBH (m) Total height (m)
0.23±0.6 13.7±2.6 0.10 – 0.31 7.8 – 16.9
0.28±0.11 15.4±4.9 0.03 – 0.47 4.8 – 27.6
0.34±0.12 17.4±3.3 0.09 – 0.60 7.6 – 21.5
0.89±0.33 24.9±4.2 0.26 – 1.57 15.7 – 35.0
4.2 – 28.9 2.5 – 14.9
0.26±0.14 10.9±4.2 0.04 – 0.51 3.5 – 27.0
0.96±0.29 29.4±3.1 0.79 – 1.49 21.0 – 35.0
0.63±0.42 19.4±9.9 4.6 – 1.49 3.5 – 35.0
0.19±6.4 10.6±3.1 0.03 – 0.60 2.5 – 27.6
2.07±0.43 37.7±4.8 1.57 – 3.25 25.1 – 44.6

269 Basal cavities are absent in most young and mature Araucaria trees <1.20 m

270 DBH (Fig 3. E). All documented trees >1.50 m in DBH have large internal cavities and

271 most have small openings near the soil level – only four giant Araucaria trees in this

272 study showed large openings at the base of the trunk between 0.4 - 5.5 m 2 (Fig 3. F).

273 The presence of large basal cavities in these rare giant Araucaria trees greatly

274 compromises the timber values of their lower trunks; on the other hand, the internal

275 access of the tree by bees, bats, and many other animals make these trees important

276 habitats with high ecological value in the Araucaria Forest.

277

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279 Fig. 3. Dendrometric variables in young Araucaria trees to giant Araucaria trees:

280 diameter x height (A), physiognomy of trees in relation to size (B), diameter x reiterated

281 trunks (C, D) and diameter x cavities (E, F).

282

283 Giant Araucaria trees

284 A total of 53 reiterated trunks and 31 cavities were measured for the 16 giant

285 Araucaria trees. Tree diameters, with bark, ranged from 1.61 to 3.25 m (Table 4). These

286 trees had an average height of 38.4 ± 4.6 m. The whole-tree volumes with the main

287 trunk, reiterated trunks, and bark ranged, from 21.5 to 106.6 m3; reiterated trunk

288 volumes represented 4.4%±3.6 of this total. Nine of the trees had at least 4 reiterated

289 trunks within their crowns (Table 5), and two trees did not have reiterated trunks and

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290 open cavities (Caca2; Fraib3). Nevertheless, all the trees had big internal cavities, with

291 the thickness of wood and bark along the radial axes ranged from 15 to 25 cm.

292

293 Table 4. Dendrometric measurements of the giant Araucaria trees ranked by DBH.

Tree code DBH (m) Total height (m) Volume (m3)

SaoJ1 3.25 39.2 106.6
Canel 2.68 39.0 72.1
Caca1 2.38 44.0 62.04
SaoJ2 2.25 39.3 63.3
Fraib1 2.09 40,0 38.7
SaoJ3 2.08 25.1 34.1
NovaP 2.07 35.1 44.3
Castro 2.01 44.6 61.0
SaoJC 1.95 40.4 51.7
Caca2 1.93 42.0 58.1
SantT 1.88 38.7 33.5
Chonp 1.87 37.0 47.5
Fraib2 1.85 37.0 38.2
Fraib3 1.72 35.8 35.5
CamBS 1.64 33.0 21.5
Caca3 1.61 40.0 55.8
294

295 The mean diameter and length of the reiterated trunks were 0.45±0.19 m and

296 5.0±4.25 m, respectively. The largest recorded diameter of a reiterated trunk was 1.1 m,

297 with a length of 17 m. The mean length of the reiterated trunks was 6.47±4.12 m. The

298 average insertion height of the reiterated trunks was 19.1±4.7 m, with the lowest

299 formation base at 5.5 m and the highest at 31 m (Table 5). Our measurements revealed

300 extreme structural variation among giant Araucaria trees. The largest-diameter trees

301 (SaoJ1, Canel, Caca1) had complex crowns with multiple reiterated trunks and were

302 roughly double or triple as massive volumetrically as trees with a 1.6 - 1.9 m in

303 diameter (Table 5), due to the large reiterated trunks and cylindric form of main trunk.

304 The first two main components of the multivariate analysis of nine attributes

305 (form factor (f 1.3); basal diameter of the reiterated trunk (RTD3), top height of each

306 reiterated trunk in relation to the main trunks (HfRT 1, 4 and 6); and length of the
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307 reiterated trunks (LRT 2, 3, 4 and 7) retained 61.1% of the information, with dimension

308 1 expressing the variation in the complexity of the crown by variables of the third

309 (RTD3, LRT3) and fourth (HfRT4, LRT4) orders that represented the number of

310 reiterated trunks. Dimension 1 favored the grouping of trees with 3 to 5 reiterated trunks

311 and represented a majority of the specimens in the study. Dimension 2 expressed

312 apparent variation in the variables of the first (HfRT1) and last order (LRT7) by a

313 greater and lesser number of reiterated trunks, ordering them on the one hand from 0 to

314 2 reiterated trunks (Caca 2, Fraib3, SaoJ3, Caca3, SantT and Fraib2) and on the other,

315 from 6 to 7 reiterated trunks (Canel, SaoJ1 and CamBS) (Fig. 4; Fig. 5). The variation

316 between these groups had a strong influence on the height of the reiterated trunks in

317 relation to the ground (HfRT1).

318 Ncav, NTR, BAcav and MaxDRT were positively correlated with DBH,

319 indicating that quantity and size of old-growth attributes were more prevalent in large-

320 diameter trees (Table 6). Old-growth attributes, quantity and size of cavities and

321 reiterated trunks, are positively correlated with larger diameter trees. Larger-diameter

322 trees have reiterated trunks of larger diameters and different lengths. The largest-

323 diameter reiterated trunks originate at higher positions along the main trunk. Greater

324 numbers and sizes of tree cavities are favored by larger diameters and longer lengths of

325 reiterated trunks. On the other hand, no significant correlations were found with the

326 number of reiterated trunks. The reiterated trunks of greater length have the largest

327 diameters, with their insertion bases at the highest positions on the main trunk and their

328 crowns close to the height of the main trunk crown.

329

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330

331 Fig. 4. Principal component analysis (PCA) of dendrometric variables in giant

332 Araucaria trees: (A) scree plot with a percentage of explained variances by dimensions;

333 (B) correlation plot between variables and PCA dimensions; (C) variables indicated as

334 vectors; and (D) ordination of giant Araucaria trees.

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335 Table 5 Structures of the reiterated trunks and basal cavities in Araucaria trees ranked by the number of reiterated trunks.

Tree code NR VolRT Average Average Max AHRT (m)* MaxHR Average MinLRT MaxLRT NCav BACav
T (m3) volume*/Max. diameter (m) DRT T (m) length RT (m) (m) (m2)
(m3) (ADRT)* (m) (m)*
Canel 7 6.06 0.87±0.52/1.50 0.52±0.29 1.11 17.30±4.24 26.60 7.80±5.02 4.70 17.00 3 0.015
CamBS 6 2.01 0.34±0.16/0.55 0.34±0.17 0.46 18.40±4.10 24.60 5.37±1.18 4.70 7.20 2 1.007
SaoJ1 6 6.06 1.01±0.69/1.99 0.54±0.28 0.85 15.00±6.34 20.00 7.03±2.65 1.90 9.00 6 5.503
Chonp 5 4.96 0.99±0.75/1.75 0.66±0.17 0.90 18.78±0.89 20.00 2.60±1.69 1.00 5.00 2 0.125
Castro 4 1.46 0.37±0.43/1.00 0.26±0.08 0.36 22.53±1.30 23.50 7.98±6.27 2.50 17.00 1 0.100
NovaP 4 0.77 0.19±0.27/0.59 0.37±0.12 0.55 17.23±1.93 19.20 3.00±1.63 1.00 5.00 0 0.000
Caca1 4 3.93 0.98±0.81/1.93 0.48±0.05 0.53 22.55±3.08 26.00 8.95±5.65 4.00 16.00 2 0.960
Fraib1 4 1.34 0.34±0.22/0.66 0.35±0.13 0.47 22.75±6.95 31.00 5.25±4.03 0.00 11.00 4 0.254
SaoJC 4 4.43 1.11±1.12/2.20 0.47±0.12 0.57 20.75±10.70 30.50 6.78±5.86 0.60 12.50 0 0.000
SaoJ2 3 3.54 1.18±0.56/1.74 0.52±0.10 0.58 19.80±2.33 22.30 8.40±1.80 6.40 9.90 3 0.138
Fraib2 2 2.38 1.19±1.25/2.08 0.50±0.08 0.56 18.50±2.12 20.00 5.20±4.53 2.00 8.40 5 0.401
SantT 2 0.34 0.17±0.15/0.28 0.32±0.08 0.38 19.05±0.21 19.20 5.50±2.55 3.70 7.30 1 0.063
Caca3 1 0.62 0.62 0.30 0.30 24.40 24.40 15.60 0.00 15.60 1 0.180
SaoJ3 1 0.16 0.16 0.39 0.39 13.60 13.60 4.90 0.00 4.90 1 2.745
Caca2 0 - - - - - - - - - 0 0.000
Fraib3 0 - - - - - - - - - 0 0.000
336 Legend: NTR: number of reiterated trunks; VolTR: total volume of the reiterated trunks; ADRT: average diameter; MaxDRT: maximum

337 diameter; AHRT: average height of the insertion base reiteration trunks at the main trunk; MaxHRT: maximum height at the insertion base of the

338 reiteration trunk at main trunk; MinLRT: minimum length of the reiterated trunks; MaxLRT: maximum length of the reiterated trunks; NCav:

339 numbers of cavities; and BACav: open area of the cavities at the base of the main trunk. *Standard error.

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340

341 Fig. 5. Old-growth attributes of giant Araucaria trees, with basal cavities and reiterated trunks, ranked by DBH and height (scale 10 m). (A)

342 SaoJ1 - DBH: 3.25m, H39.2 m; (B) Canel - DBH: 2.68 m, H:39 m; (C) Caca1- DBH: 2.38 m, H: 44 m; (D) Fraib1 - DBH: 2.09 m, H: 40 m; (E)

343 SaoJC – DBH: 1.95 m, H: 40.4 m and (F) Fraib3 - DBH: 1.72 m, H: 35.5 m.

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344 Table 6. Pearson’s correlation coefficients of the dendrometric structural variables in

345 giant Araucaria trees. Numbers in bold indicate significant correlations (P < 0.05, n =

346 16).

Max Min Max

Variable DBH H Ncav NTR BACav AHRT HRT LRT DRT

H 0.282 1.000

Ncav 0.538 0.056 1.000

NTR 0.545 0.135 0.459 1.000

BACav 0.615 -0.294 0.534 0.236 1.000

AHRT 0.117 0.211 0.299 0.494 -0.060 1.000

MaxHRT 0.220 0.224 0.366 0.672 -0.026 0.931 1.000

MinLRT 0.290 0.195 0.301 0.489 -0.054 0.337 0.359 1.000

MaxDRT 0.549 0.008 0.566 0.836 0.257 0.498 0.614 0.417 1.000

ALRT 0.344 0.203 0.510 0.735 0.125 0.929 0.969 0.487 0.698

347 Legend: DBH: tree diameter; H: tree height; NCav: numbers of cavities; BACav: open

348 area of the cavities at the base of the main trunk; NTR: number of reiterated trunks;

349 AHRT: average height of the insertion base of reiterated trunks at main trunk;

350 MaxHRT: maximum height of insertion base of the reiterated trunks; MinLRT:

351 minimum length of the reiterated trunks; MaxDRT: maximum diameter of the reiterated

352 trunks; ALRT: average length of the reiterated trunks.

353

354 Discussion

355 The age of Araucaria trees and their changes in crown shape were studied by Seitz

356 (1986), determining that due to its unique crown shape in old age, this tree species is not

357 suitable for dense stands in terms of number of trees per area (Fig. 3). Seitz proposed

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358 that Araucaria trees when young have a conical shape (< 10 m in tall) and when

359 matures they transition to an umbrella shape (>10 m in tall), with branches growing

360 upward. However, this model does not address the longevity of the Araucaria trees and

361 the presence of reiterated trunks on crown over 30 m in tall. Indeed, most previous

362 studies of Araucaria trees cover only juvenile and initial mature stages (Nutto et al.

363 2005; Puchalski et al. 2006; Chassot et al. 2011; Costa et al. 2013), but have not

364 considered the structural dynamics of the now-rare larger-sized Araucaria trees – those

365 with DBH >1.5 m.

366 Compared to the modest sizes of the post-logging Araucaria trees cataloged in the

367 state inventories for southern Brazil, the rare old-growth Araucaria trees documented in

368 this study are noteworthy for their gigantism, with all greater than 1.5 m in diameter

369 (Scipioni et al. 2019a). One expression of this gigantism is that the reiterated canopy

370 trunks of these huge trees are of comparable diameters to the main trunks of the largest

371 Araucaria trees remaining in the state-inventoried Araucaria forests. Indeed, these large

372 reiterated trunks from the relictual giants are the size of entire younger Araucaria trees

373 of the diameter between 0.3 - 1 m, with the ‘giants’ reiterated trunks alone reaching the

374 heights of crowns of younger trees (13 – 97 years old) (Cattaneo et al. 2013; Hess et al.

375 2018; Albiero-Júnior et al. 2020; Curto et al. 2021; Scipioni et al. 2021).

376 A conceptual model of crown development in tall conifers by Van Pelt et al.

377 (2008) shows that trees respond to damage from disturbances by growing replacement

378 structures whose form depends on the tree age and disturbance intensity. Southern

379 Brazil Araucaria trees similarly respond to trunk and crown damage by growing

380 substitute structures in the form of reiterated trunks and epicormic branches. Although

381 we did not quantify the epicormic and original branching in this study as was done in

382 some studies of tall conifers on the West Coast of the United States (Ishii et al. 2000;

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383 Ishii and Wilson 2001; Van Pelt and Sillett 2008; Ishii et al. 2017; Kramer et al. 2019),

384 the presence of epicormic branching on the main trunks clearly constitutes an integral

385 part of the physiognomy of mature and giant Araucaria trees. Their epicormic system is

386 characterized by a cluster of epicormic branches originating from a common locus – and

387 due to the thick bark, epicormic branches are often confined to old branch wounds.

388 Their common locus of origin often forces these epicormic branches to form a fan-

389 shaped array that is common among other conifers (Van Pelt and Sillett 2008).

390 We also observed an increase in the number of reiterated trunks and trunk

391 cavities in the largest Araucaria trees, which likely is a result of tree responses to

392 episodic or chronic disturbances occurring over a long lifespan. While a more

393 symmetrical original branching structure characterizes young Araucaria trees, the

394 distinctive morphology of giant old-growth Araucaria trees develops over time from

395 physical damage, shading, and partial mortality (dieback) – resulting from the reiterated

396 trunks common in old and tall Araucaria trees, as also found in giant conifers on the

397 West Coast of North America (Van Pelt and Sillett 2008; Ishii et al. 2017; Kramer et al.

398 2019). Top dieback and damage to the main trunk stimulates production of reiterated

399 trunks, with repetitive damage leading to trunk reiteration and epicormic branching at

400 multiple hierarchical levels (Van Pelt and Sillett 2008). Over time, various historical

401 injuries also promote formation of trunk cavities due to the action of wood-decay fungi,

402 insects and other pathogens, thereby individually structuring each tree (Van Pelt and

403 Sillett 2008).

404 When the vertical axis of an internal cavity in the main trunk is longer,

405 consequently the cavity’s internal area also increases, probably favored by infiltration of

406 moisture in the cavity's roof that accelerates wood rot. The presence of reiterated trunks

407 has been thought to favor internal damage to the main trunk, but in this study no

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408 correlation was found between increases in the number of reiterated trunks and the

409 number or area of the main trunk cavities. Thus, increases in the size of main-trunk

410 internal cavities may be related to various factors that damage the crown and main

411 trunk, such as cracks due strong winds, lightning, insects, and fungi (Mattheck et al.

412 2006; Mattheck 2007). According to a model of crown development in tall conifers by

413 Van Pelt and Sillett al. (2008), the compartmentalization of wood decay process (Lilly

414 2005) depends on the intensity and frequency of damage to the trees during a prolonged

415 phase of complex crown construction (Van Pelt and Sillett 2008; Sillett et al. 2015);

416 e.g., in Picea sitchensis these processes may take a century or more to develop a

417 complex old-growth crown structure (Kramer et al. 2019). However, additional research

418 using dated tree rings of the reiterated trunks in Araucaria trees needs to be carried out

419 in order to better understand the dynamics of crown formation in this species.

420 All of the Araucaria trees in this study had large trunk cavities, making their

421 dating by growth rings difficult. Dating by tree rings depends on the forest history,

422 environmental conditions, ecological strategies of species, environmental changes, and

423 especially on disturbances to define age of trees (Rozendaal and Zuidema 2011;

424 Schöngart et al. 2017; Albiero-Júnior et al. 2020). Using partial tree-ring increment core

425 samples of the giant Araucaria trees and complete tree-ring increment cores of

426 centenary Araucaria trees may in the future help provide age estimates in Araucaria

427 giants by indirect methods (Altman et al. 2016). As it is conceivable that the ages of

428 Araucaria angustifolia giants may greatly exceed the 400 years mentioned by Oliveira

429 et al. (2010), or perhaps even the 822 years found in the closely-related species A.

430 araucana (Argentina) (Hadad et al. 2020) – particularly given the potential from one

431 individual giant Brazilian Araucaria that is more than 3 m in diameter (SaoJ1) (Scipioni

432 et al. 2019a).

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433 Our current work (this study) indicates that in Araucaria plantation forests with

434 a commercial emphasis on wood production, silvicultural practices likely could avoid

435 large basal cavities by limiting the trunk size of harvested trees to about 1.0 m in

436 diameter - although plantation management for some larger-diameter trees that are

437 greatly valued for furniture manufacture could add high economic returns, as well as

438 greater ecological value. Meanwhile, in “natural” Araucaria forests where native

439 biodiversity considerations are more important, management needs to foster recruitment

440 of Araucaria trees larger than 1.0 m in DBH, due to their absence or rarity in secondary

441 forests from intense historical exploitation of large trees (Scipioni et al. 2019a). As

442 found with old-growth forests globally (Lindenmayer et al. 2014, 2016), where

443 managing Araucaria forests for a broader array of native biodiversity and natural

444 ecosystem services it is essential that forest management also recognizes and allows the

445 development and retention of the old-growth structural characteristics described in this

446 study, such as ancient giant trees, big reiterated canopy trunks, and large trunk cavities,

447 as well as old dead wood in the form of both standing and fallen trunks (Stokland et al.

448 2012).

449 This new frontier in defining the impressive longevity of the few remaining

450 gigantic Araucaria in Brazil could encourage creation of special conservation programs

451 for these rare giant old-growth trees and forests (Lindenmayer et al. 2014; Lutz et al.

452 2018) – which would be further supported by increased recognition, appreciation, and

453 inclusion in forest valuations of the ecologically vital old-tree structural attributes

454 described in this study, such as trunk cavities and large reiterated canopy trunks of these

455 giant Araucaria – which are unique and essential old-growth forest habitat features for

456 many fauna and flora (Pinho et al. 2020). While this native species is widely recognized

457 by its distinctive and unusual “monkey-puzzle” growth form – indeed, it is the visual

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458 logo of the state of Paraná and an important regional symbol for ecosystem services –

459 the survival today of just a few dozen impressive giant Araucaria trees in southern

460 Brazil is little known, and there is little societal recognition yet of the great potential of

461 these magnificent relict giant trees for environmental education, irreplaceable archives

462 of historical environments through scientific tree-ring reconstructions of past climate

463 and disturbances like fire, and nature tourism. Recognition of the structural attributes

464 and ecological benefits of ancient growth in these spectacular giant Araucaria could

465 help promote increased visitation to rural properties and parks with giant Araucaria;

466 e.g., the giant trees at SaoJ1 (Fazenda Pinheirão), Canel (Parque Municipal do Pinheiro

467 Grosso), Frai3 (Parque Ecológico René Frey) could become a source of financial

468 resources through admission to visit these unique trees (Scipioni et al. 2019a), similar to

469 the great tourism attraction of famous giant conifers in North America (Strong 2000;

470 Van Pelt 2001).

471 Although historically a common and dominant component of southern Brazil

472 forests, through logging and land conversion to agriculture A. angustifolia today has

473 been reduced to perhaps just 1% of its historical range and is considered an endangered

474 species that is protected by law (CONAMA, 2001; Thomas 2013). As a result, the

475 management of “natural” forested areas containing Araucaria is mostly forbidden

476 (Costa et al. 2020), and the cutting of Araucaria is authorized only in specific situations

477 by an environmental agency, e.g., when there is risk to life or property, for scientific

478 research, or in cases of public utility such as construction of roads and energy networks

479 (CONAMA 2002). However, some non-commercial exploitation may be authorized of

480 rare native flora like Araucaria angustifolia that are threatened with extinction, largely

481 for consumption in rural properties or possessions of indigenous peoples and traditional

482 populations (CONAMA 2002) – mainly trees felled by natural events such as storms.

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483 The lack of investment by federal and state governments in environmental agencies

484 results in few service offices and trained personnel, which: a) undermines proposals for

485 the proper management and use of endangered species like Araucaria; b) fosters

486 environmental crimes like cutting down endangered and giant trees (Scipioni 2019);

487 and c) discourages the regeneration, recruitment and use Araucaria trees on rural

488 properties. The state of Paraná solved this legal situation with a law (20.233/2020),

489 which encourages the planting and exploitation of Araucaria angustifolia, allowing

490 those who plant this Araucaria in the “plantation” modality the right to exploit directly

491 (wood) and indirectly (seeds) these planted trees, since they are outside environmental

492 protected areas in natural forests (Paraná 2020). However, additional legislation and

493 government incentives are still needed to favor the recruitment of new Araucaria trees

494 in natural forests, and to promote the conservation of old and historic trees and specific

495 inventories to find them – these measures are all essential to keep Araucaria in wild,

496 rural landscapes of southern Brazil for current and future generations (Lindenmayer et

497 al. 2014; Lindenmayer and Laurance 2016; Scipioni et al. 2019b).

498 Conclusion

499 The basal cavities and reiterated trunks are great distinguishing attributes for

500 old-growth attributes in Araucaria angustifolia. The old growth attributes are prominent

501 in Araucaria trees > 1,5 m in diameter and size is justified to distinguish the giant

502 Araucaria trees from young and mature trees. Forest management plans should include

503 old growth attributes promoting the recruitment of larger trees, especially in secondary

504 forests, aiming at perpetuating the species and promoting large trees in forest, such as

505 habitat and food for fauna with araucarias with diameters greater than 1 m (>200 years

506 old).

507 Declarations

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508 The authors have declared that no competing interests exist.

509 Author contributions

510 Marcelo C Scipioni: Conceptualization, Methodology, Writing-Original draft preparation,

511 Visualization, Investigation, Formal analysis, Resources, Funding acquisition. Pedro Higuchi:

512 Formal analysis, Writing-Reviewing and Editing. Guilherme D Folcking:

513 Investigation,Visualization. Craig D. Allen: Writing-Reviewing and Editing.

514 Availability of data and materials

515 The datasets used and/or analyzed during the current study are available from the corresponding

516 author on reasonable request.

517 Funding

518 This study was funded by the CNPq - National Council for Scientific and Technological

519 Development (project n. 423912/2018-6). The funders had no role in study design, data

520 collection and analysis, decision to publish, or preparation of the manuscript.

521 Acknowledgments

522 The authors wish to thank Prof. Mário Dobner Jr. (UFSC) for the availability of data on young

523 trees.

524 References

525 Albiero-Júnior A, Venegas-González A, Rodríguez-Catón M, et al (2020) Edge effects

526 modify the growth dynamics and climate sensitivity of Araucaria angustifolia trees.

527 Tree-Ring Res 76:11–26.

528 Altman J, Dolezal J, Cízek L (2016) Age estimation of large trees : New method based

529 on partial increment core tested on an example of veteran oaks. For Ecol Manage

530 380:82–89. doi: 10.1016/j.foreco.2016.08.033

531 Backes A, Nilson AD (1983) Araucaria angustifolia (Bert.) O. Kuntze, o pinheiro-

532 brasileiro. Iheringia Série Botânica 30:85–96.

533 Carvalho PER (2003) Espécies Arbóreas Brasileiras vol. 1. Embrapa Informação

534 Tecnológica, Brasília

55 28
56
535 Cattaneo N, Fassola H, Pahr N, et al (2013) Sex-related , growth-climate association of

536 Araucaria angustifolia in the neotropical ombrophilous woodlands of Argentina.

537 Dendrochronologia 31:147–152. doi: 10.1016/j.dendro.2013.01.005

538 Chassot T, Fleig FD, Finger CAG, Longhi SJ (2011) Modelos de crescimento em

539 diâmetro de árvores individuais de Araucaria angustifolia (Bertol.) Kuntze em

540 floresta ombrófila mista. Ciência Florest 21:303–314.

541 Chiavetta U, Sallustio L, Garfı V, et al (2014) Classification of the oldgrowthness of

542 forest inventory plots with dissimilarity metrics in Italian National Parks. Eur J For

543 Res 131:1473–1483. doi: 10.1007/s10342-012-0616-7

544 CONAMA (2001) Resolução Conama n.o 278, de 24 de maio de 2001. Conselho

545 Nacional de Meio Ambiente, Brasília

546 CONAMA (2002) Resolução no 300, de 20 de março de 2002. Conselho Nacional de

547 Meio Ambiente, Brasília

548 Costa AE, Finger CA, Cunha TA (2013) Influência da posição social e do número de

549 raios na estimativa da área de copa em araucária. Floresta 43:429–438.

550 Costa EA, Liesenberg V, Hess AF, et al (2020) Simulating Araucaria angustifolia

551 ( Bertol .) Kuntze Timber Stocks With Liocourt’s Law in a Natural Forest in

552 Southern Brazil. Forest 11:1–14. doi: 10.3390/f11030339

553 Curto R de A, Mattos PP de, Braz EM, Netto SP (2021) Growth and retrospective

554 analysis of competition in an overstocked stand of Araucaria angustifolia. For Ecol

555 Manage 483:1–10. doi: 10.1016/j.foreco.2020.118766

556 Dray S, Dufour A-B (2007) The ade4 Package: Implementing the Duality Diagram for

557 Ecologists. J Stat Softw 22:1–20. doi: 10.1002/wics.10

558 Eckenwalder JE (2009) Conifers of the World. Tree Press, Portalnd

559 Farjon A, Filer D (2013) An Atlas of the Worl´s Conifers: an analysis of their

57 29
58
560 distribution, biogeography, diversity and conservation status. Brill, Leiden

561 Franklin JF, Spies TA (1984) Characterisitics of old-growth Douglas-fir Forests. In:

562 Proceedings of the Society of American Foresters National Convention. Society of

563 American Foresters, Washington, pp 328–334

564 Gorgens EB, Motta AZ, Assis M, et al (2019) The giant trees of the Amazon basin.

565 Front Ecol Environ 373–374. doi: 10.1002/fee.2085

566 Hadad MA, Gabriela J, Molina A, Roig FA (2020) Dendrochronological Study of the

567 Xeric and Mesic Araucaria araucana Forests of Northern Patagonia : Implications

568 for Ecology and Conservation. In: Pompa-García M. CJ (ed) Latin American

569 Dendroecology. Springer, Cham, pp 283–314

570 Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software

571 Package for Education and Data Analysis. v.2.17. Palaeontol Electron 1:1–9.

572 Hess AF, Ricken P, Ciarnoschi LD (2018) Dendrochronology, increment and forest

573 management in Araucaria Forest, Santa Catarina. SC. Ciência Florest 28:1568–

574 1582.

575 Ishii H, Clement JP, Shaw DC (2000) Branch growth and crown form in old coastal

576 Douglas-fir. For Ecol Manage 131:81–91. doi: 10.1016/S0378-1127(99)00202-9

577 Ishii H, Wilson ME (2001) Crown structure of old-growth Douglas-fir in the western

578 Cascade Range, Washington. Can J For Res 31:1250–1261. doi: 10.1139/cjfr-31-7-

579 1250

580 Ishii HR, Sillett SC, Carroll AL (2017) Crown dynamics and wood production of

581 Douglas-fir trees in an old-growth forest. For Ecol Manage 384:157–168. doi:

582 10.1016/j.foreco.2016.10.047

583 Kassambara A, Mundt F (2020) factoextra: Extract and Visualize the Results of

584 Multivariate Data Analyses. R package version 1.0.7. https://CRAN.R-

59 30
60
585 project.org/package=factoextra.

586 Kramer RD, Sillett SC, Pelt R Van, Franklin JF (2019) Forest Ecology and

587 Management Neighborhood competition mediates crown development of Picea

588 sitchensis in Olympic rainforests : Implications for restoration management. For

589 Ecol Manage 441:127–143. doi: 10.1016/j.foreco.2019.03.027

590 Lilly S (2005) Tree Climber’s Guide.

591 Lindenmayer DB, Blanchard W, Mcburney L, et al (2012a) Interacting Factors Driving

592 a Major Loss of Large Trees with Cavities in a Forest Ecosystem. PLoS One. doi:

593 10.1371/journal.pone.0041864

594 Lindenmayer DB, Laurance WF (2016) The ecology, distribution, conservation and

595 management of large old trees. Biol Rev. doi: 10.1111/brv.12290

596 Lindenmayer DB, Laurance WF, Franklin JF, et al (2014) New policies for old trees:

597 Averting a global crisis in a keystone ecological structure. Conserv Lett 7:61–69.

598 doi: 10.1111/conl.12013

599 Lindenmayer DB, Laurance WF, Franklin JF (2012b) Global decline in large old trees.

600 Science (80- ) 338:1305–1306. doi: 10.1126/science.1231070

601 Longhi RV, Schneider PR, Longhi SJ, et al (2018) Growth dynamics of Araucaria after

602 management Interventions in natural forest. Floresta e Ambient 25:1–10.

603 Lutz JA, Furniss TJ, Johnson DJ, et al (2018) Global importance of large-diameter trees.

604 Glob. Ecol. Biogeogr.

605 Mattheck C (2007) Updated field guide for Visual Tree Assessment. Verlag

606 Forschungszentrum, karlsruhe

607 Mattheck C, Bethge K, Tesari C (2006) Shear effects on failure of hollow trees. Trees

608 20:329–333. doi: 10.1007/s00468-005-0044-0

609 Naimi B, Hamm NAS, Groen TA, et al (2014) Where is positional uncertainty a

61 31
62
610 problem for species distribution modelling? Ecography (Cop) 37:191–203. doi:

611 10.1111/j.1600-0587.2013.00205.x

612 Nutto L, Spathelf P, Rogers R (2005) Managing diameter growth and natural pruning of

613 Parana pine, Araucaria angustifolia ( Bert .) O Ktze., to produce high value timber.

614 Ann For Sci 62:163–173. doi: 10.1051/forest

615 Oliveira JM, Roig FA, Pillar VD (2010) Climatic signals in tree-rings of Araucaria

616 angustifolia in the southern Brazilian highlands. Austral Ecol 35:134–147. doi:

617 10.1111/j.1442-9993.2009.02018.x

618 Paraná (2020) Lei 20.233. Assembeia Legislativa do Estado do Paraná, Curitiba

619 Percel G, Parmain G, Laroche F, Bouget C (2018) The larger, the better? Effects of

620 delayed diameter-limit cutting on old-growth attributes and saproxylic beetle

621 diversity in temperate oak forests. Eur J For Res. doi: 10.1007/s10342-018-1103-6

622 Pinho BX, Peres CA, Leal IR, Tabarelli M (2020) Critical role and collapse of tropical

623 mega-trees: A key global resource. Adv Ecol Res 62:253–294. doi:

624 10.1016/bs.aecr.2020.01.009

625 Puchalski Â, Mantovani M, Reis MS dos (2006) Variation in Araucaria angustifolia

626 (Bert.) O.Kuntze natural populations associated with climate and soil conditions.

627 Sci For 70:137–148.

628 R Development Core Team (2020) R: A language and environment for statistical

629 computing.

630 Remm J, Lõhmus A (2011) Forest Ecology and Management Tree cavities in forests –

631 The broad distribution pattern of a keystone structure for biodiversity. For Ecol

632 Manage 262:579–585. doi: 10.1016/j.foreco.2011.04.028

633 Rozendaal DMA, Zuidema PA (2011) Dendroecology in the tropics : a review. Trees

634 25:3–16. doi: 10.1007/s00468-010-0480-3

63 32
64
635 Schöngart J, Bräuning A, Barbosa ACMC, et al (2017) Dendroecological Studies in the

636 Neotropics : History, Status and Future Challenges. In: Amoroso MM, Daniels LD,

637 Baker PJ, Camarero JJ (eds) Dendroecology: Tree-Ring Analyses Applied to

638 Ecological Studies. Springer, pp 35–73

639 Scipioni MC (2019) Monumental tree trunks as indicators of forest degradation in

640 southern Brazil. Ciência Florest 29:1–14. doi: 10.5902/1980509835588

641 Scipioni MC, Dobner Jr M, Longhi SJ, et al (2019a) The last giant Araucaria trees in

642 southern Brazil. Sci Agric 76:220–226. doi: 10.1590/1678-992x-2017-0264

643 Scipioni MC, Fontana C, Morales J, et al (2021) Effects of cold conditions on the

644 growth rates of a subtropical conifer. Dendrochronologia 68:125858. doi:

645 10.1016/j.dendro.2021.125858

646 Scipioni MC, Salomão R de P, Vibrans AC, Uller HF (2019b) Decline in giant tree

647 numbers: status report for Santa Catarina state and perspectives for Brazil. Floresta

648 e Ambient 26:1–5. doi: 10.1590/2179-8087.003919

649 Seitz RA (1986) Erste Hinweise für die waldbauliche Behandlung von

650 Araukarienplantagenwäldern. Ann Sci For 43:327–338.

651 Shenkin A, Chandler CJ, Boyd DS, et al (2019) The World ’ s Tallest Tropical Tree in

652 Three Dimensions. Front For Glob Chang 2:1–5. doi: 10.3389/ffgc.2019.00032

653 Shortle WC, Dudzik KR (2012) Wood decay in living and dead trees : A pictorial

654 overview. Gen. Tech Rep. NRS-97. Newt. Square, PA U.S. Dep. Agric. For. Serv.

655 North. Res. Station. 26.

656 Sillett SC, Pelt Van R, Carroll AL, et al (2015) How do tree structure and old age affect

657 growth potential of California redwoods? Ecol Monogr 85:181–212.

658 Sillett SC, Van Pelt R, Koch GW, et al (2010) Increasing wood production through old

659 age in tall trees. For Ecol Manage 259:976–994. doi:

65 33
66
660 10.1016/J.FORECO.2009.12.003

661 Souza AF (2007) Ecological interpretation of multiple population size structures in

662 trees: The case of Araucaria angustifolia in South America. Austral Ecol 32:524–

663 533. doi: 10.1111/j.1442-9993.2007.01724.x

664 Souza AF, Cortez LSR, Longhi SJ (2012) Native forest management in subtropical

665 South America: long-term effects of logging and multiple-use on forest structure

666 and diversity. Biodivers Conserv 21:1953–1969. doi: 10.1007/s10531-012-0287-1

667 Stokland JN, Siitonen J, Jonsson BG (2012) Biodiversity in Dead Wood. Cambridge

668 University Press, Cambridge, New York, Melbourne, Madrid, Cape Town,

669 Singapore, São Paulo, Delhi, Mexico City

670 Strong D (2000) From Pioneers to Preservationists: a brief history of Sequoia and King

671 Canyon National Parks. Sequoia Natural History Association, Three Rivers

672 Thomas P (2013) Araucaria angustifolia. In: IUCN Red List Threat. Species 2013.

673 Van Pelt R (2001) Forest giants of the Pacific coast. University of Washington Press,

674 Seattle

675 Van Pelt R (2007) Identifying mature and old forests in western Washington.

676 Washington State Department of Natural Resources, Olympia

677 Van Pelt R, Sillett SC (2008) Crown development of coastal Pseudotsuga menziesii,

678 including a conceptual model for tall conifers. Ecol Monogr 78:283–311. doi:

679 10.1890/07-0158.1

680 Van Pelt R, Sillett SC, Nadkarni NM (2004) Quantifying and Visualizing Canopy

681 Structure in Tall Forests. Methods and a Case Study. In: Forest Canopies: Second

682 Edition, Second Edi. Elsevier Inc., pp 49–72

683 Wei T, Simko V (2017) R package “corrplot”: Visualization of a Correlation Matrix

684 (Version 0.84). Available from: https://github.com/taiyun/corrplot.

67 34
68
685 Wu C, Jiang B, Yuan W, et al (2020) On the Management of Large-Diameter Trees in

686 China’s Forests. Forests 11:1–9.

687

69 35
70