Draft · 2017-07-11 · Draft 1 1 Lepidoptera wing scales: a new paleoecological indicator for...

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Lepidoptera wing scales: a new paleoecological indicator to

reconstruct spruce budworm abundance

Journal: Canadian Journal of Forest Research

Manuscript ID cjfr-2017-0009.R2

Manuscript Type: Note

Date Submitted by the Author: 13-Jun-2017

Complete List of Authors: Navarro, Lionel; Université du Québec à Chicoutimi, Laboratoire d'écologie végétale et animale (local P3-2040) Harvey, Anne-Élizabeth; Université du Québec à Chicoutimi, Laboratoire d'écologie végétale et animale (local P3-2040) Morin, Hubert; Université du Québec à Chicoutimi,

Keyword: boreal forest, insect outbreak, paleoindicator, moth, butterfly

Is the invited manuscript for consideration in a Special

Issue? : IUFRO 2016 Special Issue

https://mc06.manuscriptcentral.com/cjfr-pubs

Canadian Journal of Forest Research

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Lepidoptera wing scales: a new paleoecological indicator for reconstructing spruce 1

budworm abundance 2

Lionel Navarro* ([email protected]), Anne-Élizabeth Harvey (anne-3

[email protected]), Hubert Morin ([email protected]) 4

5

Département des Sciences Fondamentales, Université du Québec à Chicoutimi, 555 6

boulevard de l’université, G7H-2B1, Chicoutimi (QC), Canada. Tel.: 418-545-5011 ext. 7

2330 8

*Corresponding author: [email protected], Tel.: 418-545-5011 ext. 2330 9

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Running title: Wing scales, a new paleoecological proxy 11

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Abstract 13

Natural disturbances have a major impact on boreal forest landscape dynamics and, 14

although fire history is well documented at the Holocene scale, spruce budworm (SBW) 15

dynamics are only known for the last three centuries. This is likely due to the difficulty in 16

using and interpreting existing indicators (cephalic head capsules and feces). In this 17

methodological study, we present an original approach using lepidopteran wing scales to 18

reconstruct insect abundance. We analyzed two sediment cores from the boreal forest in 19

central Quebec and extracted wing scales at every stratigraphic level. The required 20

quantity of sediment for paleoecological analysis is relatively small given the large 21

quantity of wing scales produced by Lepidoptera and their small size. Scales are well-22

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preserved due to their chitinous structure and their great variety of shapes offer a high 23

potential for taxonomic identification. A statistical model based on the shape of scales of 24

the three major epidemic lepidopterans in Quebec discriminated 68 % of SBW scales. 25

This indicator allows a more efficient and more precise reconstruction of SBW history 26

with respect to the use of cephalic head capsules or feces. 27

Résumé 28

Les perturbations naturelles ont un impact majeur sur la dynamique des paysages en forêt 29

boréale, et bien que l’historique des feux soit étudié à l’échelle holocène, la dynamique 30

de la tordeuse des bourgeons de l’épinette (TBE) n’est connue que pour les trois derniers 31

siècles. Ce manque peut s’expliquer par la difficulté d’utilisation et d’interprétation des 32

indicateurs disponibles (capsules céphaliques et fèces). Cette étude méthodologique 33

présente une méthode originale qui permet d’utiliser les écailles de lépidoptère pour 34

reconstruire l’abondance de l’insecte. L’étude de deux carottes de surface échantillonnées 35

dans la réserve faunique des Laurentides a permis de retrouver des microrestes à tous les 36

niveaux stratigraphiques. La grande quantité d’écailles produite par papillons ainsi que la 37

taille des microrestes a permis de réduire considérablement le volume de sédiments 38

requis. Les écailles se conservent bien grâce à leur structure chitineuse et leur grande 39

variété de formes présente un fort potentiel d’identification taxonomique. Un modèle 40

statistique basé sur la mesure de la forme des écailles des trois principaux lépidoptères 41

épidémiques au Québec a permis de discriminer 68 % des écailles de TBE. Cet indicateur 42

permet donc une reconstitution plus efficace et plus précise de l’historique des 43

populations de TBE par rapport à l’utilisation des capsules céphaliques ou des fèces. 44

Keywords: boreal forest; insect outbreaks; moth; butterfly; paleoindicator 45

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Introduction 46

Climate change is a major challenge in ecology, greatly affecting forest disturbance 47

dynamics and ecosystem diversity (Gauthier et al. 2015). Boreal forests are the largest 48

terrestrial ecosystems on the planet and produce more than a third of the world’s lumber 49

(Gauthier et al. 2015, Montoro Girona et al. 2016). Due to the ecological and economic 50

impacts of insect outbreaks in this ecosystem, it is important to develop a better 51

understanding of how climate change affect these, often devastating, insect events. 52

Forecasts project an increase in the frequency, duration, and timing of insect outbreaks 53

(Nelson et al. 2013). However, there remains a shortage of indicators that permit a more 54

thorough assessment of cycles and impacts of insect outbreaks at the Holocene scale 55

(Simard et al. 2002). 56

Spruce budworm (Choristoneura fumiferana, Clemens) (SBW) is one of the most 57

important agents of natural disturbance in the boreal forests of North America 58

(Shorohova et al. 2011), causing major loss of productivity and death of host species 59

(Hennigar et al. 2013). In the eastern Canadian boreal forest, SBW is, by far, the most 60

damaging defoliator of conifers, reaching cyclically epidemic population densities that 61

allow the insect to affect large forest areas (Pureswaran et al. 2015). During the last 62

outbreak of the 20th century (1974–1988) SBW affected 55 million hectares causing the 63

loss of 139 to 238 million m3 of fir and spruce (Boulet et al. 1996). This forest pests’ 64

short life cycle, mobility, and high reproductive potential allow a rapid response to 65

changes in environmental conditions (Menéndez 2007). Nevertheless, long-term studies 66

of landscape natural variability focus on the use of charcoal fragments to determine fire 67

activity and often conceal the effect of forest insect outbreaks (Bergeron et al. 1998). 68

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However, in eastern Quebec SBW is considered a more important disturbance than fire 69

and the lack of knowledge about its pluri-millennial dynamics is the cause of a serious 70

bias in the understanding of landscape variability. It is therefore important to assess the 71

relative importance of SBW outbreaks and the role played in the entire boreal forest 72

ecosystem at the longest temporal scale possible. 73

Dendrochronological studies have revealed the epidemic history of SBW over the last 74

three centuries (Boulanger et al. 2012). Tree-ring analysis provides important insights 75

into impact from defoliation as well as the periodicity and synchronism of insect 76

outbreaks across huge areas of forest. Nevertheless, dendrochronology is an indirect 77

measure of SBW impact and its interpretation is limited as multiple factors may influence 78

tree growth (Davis and Hoskins 1980). In addition, dendrochronology is restricted to the 79

age of survivor trees and reconstruction of long-term chronologies using subfossil trees 80

buried in lakes and ponds is promising but, for the moment, remains challenging. 81

Paleoecology allows a longer-term reconstruction of SBW activity. Macrofossils such as 82

cephalic head capsules (Lavoie et al. 2009) or feces (Simard et al. 2006) have been used 83

as direct indicators of the occurrence of insect outbreaks. However, the long-term 84

dynamics remain poorly documented as analysis is time-consuming, and temporal 85

resolution is low due to the amount of sediment to be examined. The number of cephalic 86

head capsules extracted from a relatively large amount of sediment or peat material tends 87

to be low and feces become increasingly difficult to identify with depth due to 88

decomposition. 89

Butterfly and moth wings are covered with thousands of minute overlapping scales of 90

variable shape, forming colour patterns on the wing surface (Dinwiddie et al. 2014). 91

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These scales assume many different functions, from attracting and selecting mates 92

(Burghardt et al. 2000) to camouflage (Brakefield and Liebert 2000), and thermal 93

regulation (Srinivasarao 1999). 94

SBW scales are partly made of chitin fibrils (Richards 1947) that are well-preserved in 95

sediments due to increasingly favorable conservation conditions with depth under 96

anaerobic conditions (Sturz and Robinson 1986). As these scales are produced in a very 97

high quantity, particularly during outbreaks, this should permit many of these 98

microfossils to be retrieved from a very small quantity of sediments. There is also a great 99

potential for taxonomic identification owing to the high diversity of scale shapes. These 100

considerations led us to ask whether lepidopteran scales microfossils are a more suitable 101

paleoindicator of SBW abundance. We hypothesize that this indicator can be extracted in 102

a significant quantity and that its abundance peaks will match known periods of SBW 103

outbreaks. 104

This methodological investigation proposes a practical technique to collect and extract 105

fossil scales from sediment cores and discusses the potential benefits and difficulties of 106

using scale shape as an indicator of Lepidoptera species. We also present examples from 107

two short sediment cores recovered from a pair of lakes in the central boreal region of 108

Quebec. 109

Proposed methodology for scale extraction 110

Scale extraction and analysis 111

To set the extraction parameters (sucrose solution density, sieve mesh size, centrifugation 112

speed and duration…), we used a trial and error approach with test samples in which we 113

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added a relatively constant quantity of scales (one entire forewing of a SBW per sample). 114

The parameters presented here are those that gave the best results. 115

We dried samples from a sectioned sediment core at 105 °C for 24 h. For each interval of 116

interest, we collected a 0.5 g subsample of dry sediment (± 5 cm3) and heated it in a 117

100 mL 10 % potassium hydroxide (KOH) solution at 70 °C for 30 min or until complete 118

deflocculation had occurred (Frey 1986). The slurry was then sieved through a 53 µm 119

mesh to retain most of the scales. Small particles (mostly fragments of organic matter) 120

were discarded to allow us to analyze a more concentrated sediment subsample. We 121

centrifuged the samples at 500 RCF for 10 min in a 10 mL sucrose solution (relative 122

density = 1.24) to remove higher density particles. This centrifuging was repeated three 123

times. After each run, we recovered the supernatant, refilled the vial with the sucrose 124

solution, and centrifuged again. We combined the three supernatants in a 50 mL plastic 125

vial and, to precipitate scales and any remaining particles, we centrifuged the combined 126

supernatant at 3900 RCF for 20 min. The final pellet was mounted onto microscope 127

slides for microfossil counting. This operation permitted most of the scales to be easily 128

extracted, at low cost, without using destructive chemicals. 129

Taxonomic identification of scales and the potential of using scale shape 130

There is very little existing literature about the taxonomic value of lepidopteran scales for 131

paleoecological work. Species of Lepidoptera are usually distinguished by studying wing 132

venation or genitalia, features that are not preserved in the sediment record. Among the 133

other discriminant criteria, the most studied are the iridescent ultrastructure of scales and 134

structural colour production (Dinwiddie et al. 2014). Ultrastructure analysis requires 135

expensive and time-consuming scanning electron microscopy (SEM) that is not easily 136

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applicable to paleoecological studies. In the case of moths, colour patterns are dull and 137

extraction techniques, including the use of hot alkali solution, could alter the 138

pigmentation of scales. In some rare cases, when these identification criteria are not 139

sufficient to distinguish two sibling species, scale shape has been used (Anken and 140

Bremen 1996, Yang and Zhang 2011). 141

To test the interspecific variability of shape parameters and their taxonomic potential, we 142

selected three of the major epidemic defoliator lepidopterans in the North American 143

boreal forest: spruce budworm (Choristoneura fumiferana Clemens), forest tent 144

caterpillar (Malacosoma disstria Hübner) and hemlock looper (Lambdina fiscellaria 145

Guénée) (Shorohova et al. 2011). We used eight specimens for each species, half of each 146

sex to take sexual dimorphism into account, and studied scales from the upper and lower 147

surface of each wing. Scales were separated from the wing using a fine brush and 148

mounted on glycerol-coated microscope slides. To ensure random and systematic 149

selection, we used a 10×10 grid beneath the slide and selected the first scale encountered 150

in each cell. We analyzed 2400 scales per species. We used Elliptic Fourier Descriptors 151

(EFDs) and some non-size correlated shape parameters as quantitative measures of scales 152

shape. EFD coefficients were calculated from the chain-coded contours of each scale 153

obtained with SHAPE package v.1.3 (Iwata and Ukai 2006) using 20 harmonics. These 154

coefficients were normalized to be invariant with respect to the size, rotation, and 155

position. This procedure generated multiple coefficients for each scale. As such, we used 156

principal component analysis (PCA) to summarize the data. We used the six principal 157

components scores as shape characteristics. Using image processing software ImageJ 158

v.1.48v (Schneider et al. 2012), we also measured the aspect ratio (��

��), circularity 159

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(4π × ��

�� ), solidity (

��

��) and the number of apical indentations. We 160

used all these shape parameters to build a discriminating model that correctly classified 161

68 % of the SBW scales, 79 % of the hemlock looper scales and 62 % of the forest tent 162

caterpillar scales (Fig. 3). We used well-classified scales having a probability >0.8 to 163

construct ten morphotypes for each species based on a K-mean cluster analysis (Fig. 4). 164

Each cluster was characterized by the shape of the median scale and of the first two 165

standard deviations. We also reconstructed the ten most common morphotypes 166

(misclassified, probability <0.5). Specific shapes were observed such as the very deep 167

indentations in Malacosoma disstria specimens as noted by Grodnitsky and Kozlov 168

(1990) for Lasiocantpidae. Choristoneura fumiferana morphotypes showed a higher 169

circularity with a relatively high number of small indentations. In contrast, most of the 170

Lambdina fiscellaria morphotypes have little to no indentation. Moreover, shape analysis 171

revealed a high intra-specific variability for shape variation, confirming a hypothesis of 172

mostly common scale shapes and some specialized ones (Ghiradella 1994). 173

These morphotypes based on shape measurement still have limitations as a systematic 174

taxonomic identification tool. Indeed, accurate identification of fossil scales extracted 175

from sediment is not always possible due to the conservation state of scales (broken or 176

folded) (Fig. 7e) or the soft focus effect. However, it can help differentiate peaks that 177

may be caused by outbreaks of two or more lepidopteran species. 178

In Canada, 18 species, representing 1 to 2 % of forest lepidopterans, are cyclically 179

outbreaking (Faeth 1987, Mason 1987). From long-term abundance reconstruction 180

studies of SBW in Quebec, we can exclude potentially introduced and western species. 181

Moreover, since 1975, 95 % of areas affected by defoliation were caused by SBW. In 182

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addition, spatial extension of bioclimatic domains have been quite stable in eastern 183

Canada since 5 ka BP (Dyke 2005). SBW feces in the sediment record from the northern 184

part of its distribution area attests to its presence since 8 ka BP (Simard et al. 2006). As 185

such, we can assume, with a low risk of misinterpretation, that high variations in fossil 186

scales abundance in Quebec are mainly due to SBW dynamics. 187

Case study: results and interpretation 188

Study sites 189

The paleoecological protocol was tested on surface sediment cores from two lakes 190

located at the Simoncouche Experimental Forest of the Université du Québec à 191

Chicoutimi, Quebec. Lac Flévy (48°13’00.04’’N; 71°12’57.21’’W) covers an area of 192

2.33 ha at an altitude of 376 m. Lac Hautbois (48°12’30.65’’N; 71°13’22.92’’W) covers 193

3.9 ha and is at an altitude of 398 m (Fig. 2).We chose small lakes having low outflows, 194

to ensure high sedimentation rates (Millspaugh and Whitlock 1995, Ali et al. 2009). Both 195

studied sites lie on undifferentiated glacial till and fluvioglacial deposits constituted of 196

loose or compact unsorted deposit (Ministère de l’Énergie des Mines et des Ressources 197

1976). Each lake is surrounded by even-aged trembling aspen (Populus tremuloides) 198

stands and mixed even-aged stands of black spruce (Picea mariana) and poplar. The age 199

structure indicated that these forest stands originated from an intense fire that occurred in 200

1922 (Gagnon 1989). SBW has been present in the area for a minimum of 8240 years 201

(Simard et al. 2006) and recurrent outbreaks were reported during the last three centuries, 202

becoming more frequent during the 20th century (Blais 1983). Aerial surveys indicate 203

that defoliation has occurred in the study area since 2012 reaching severe levels after 204

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2015 (Ministère des Ressources Naturelles et de la Faune 2012, Ministère des Forêts de 205

la Faune et des Parcs 2015). 206

Sediment core recovery and preparation 207

We collected two sediment cores from the deepest portion of each lake, one for isotopic 208

dating and the second core for extracting scales. We used a Glew gravity corer for 209

sediment sampling to ensure the sediment/water interface was not disturbed (Glew 1988). 210

The core lengths for the microfossil cores were 32 cm and 24 cm for Lac Flévy and Lac 211

Hautbois, respectively. The cores collected for the analysis of micro-remains were 212

subsampled in the field at a 1-cm-thick resolution using a vertical extruder (Glew 1988). 213

Isotopic dating 214

Samples used for dating were dried (105 °C for 24 h) and then sent to the 215

Radiochronology Laboratory at the Centre d’études nordiques, Université Laval for 210Pb 216

and 137Cs analyses by gamma spectrometry (San Miguel et al. 2005). We selected a 217

constant rate of supply (CRS) model for the 210Pb dating of both cores (Turner and 218

Delorme 1996). 219

Results from scale extraction 220

Despite the small subsample size (0.5 g dry sediment) and the fact that surface samples 221

are not the most suitable for this kind of analysis (high levels of bioturbation, high water 222

content…), we obtained a substantial quantity of scales from each sampled interval of the 223

sediment cores from both lakes (Fig. 5 and 6). This result is inconsistent with Kristensen 224

and Simonsen’s (2003) assumption that Lepidoptera fossils are strikingly scarce in 225

lacustrine sediments. All the collected microfossils were well-preserved and the 226

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accumulation rate of scales presented a similar order of magnitude in both lakes. Lac 227

Flévy presented two distinctive peaks, the first corresponding to the mid-20th century (± 228

15 years) and the second corresponding to the beginning of the 21st century (Fig. 5). Both 229

peaks match with known periods of high SBW abundance in the study area. Although the 230

stratigraphy of Lac Hautbois is less clear, it is comparable to that of Lac Flévy: we 231

extracted the most scales from depths corresponding to the early 21st century and the 232

scale accumulation rate decreases slightly prior to the 20th century (Fig. 6). Due to our 233

conservative identification criteria, our results represent a quite low morphotype 234

identification rate suggesting that this method should be used as a validation tool rather 235

than as a systematic identification method. Nevertheless, in both lakes the species with 236

the highest rate of morphotype match was Choristoneura fumiferana (Fig 5 and 6), 237

confirming that SBW is the most common outbreaking Lepidoptera in the area. Finally, 238

the identified SBW were similar to the unidentified scales suggesting that some SBW 239

scales were unidentified due to a lack in identification criteria or a degraded physical 240

condition. However, surface core scale abundance requires careful interpretation as 210Pb 241

dating precision decreases with depth (Fig. 5). A lower resolution long-term 14C dated 242

stratigraphy should be undertaken for SBW abundance analysis, which will be the subject 243

of a later study. 244

Advantages and shortcomings 245

The use of fossil scales of Lepidoptera presents some advantages over other 246

paleoecological proxies. Scales are less degradable than feces and much more abundant 247

than cephalic head capsules. They have been found in nearly every sample analyzed to 248

date, including the examples presented above and within longer sediment cores analyzed 249

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for an upcoming publication. Moreover, the use of wing scales requires a relatively small 250

amount of sediment to prepare, simplifying the sampling procedure and allowing wing 251

scales to be analyzed along with additional proxies such as charcoal and pollen from the 252

same core material. Insect infestations should thus be included in any future studies of 253

long-term disturbance dynamics to allow forest management policies to be based on more 254

complete and realistic information. Finally, scale count data can benefit from data 255

processing methods such as the use of a LOESS smoothing to distinguish background 256

variation from locally defined peaks (Higuera et al. 2010). 257

Nevertheless, as all paleoecological studies, this kind of research is time-consuming, 258

restricting the replicability across multiple sites. In addition, the development of other 259

discriminant criteria (texture, pigmentation, ultrastructure characteristic…) to improve 260

the relevance of interpretation is pertinent due to the taxonomic potential of scales. This 261

method could be adapted for use in different environments such as bogs, fens, ponds, or 262

peat deposits to be directly comparable with existing proxies (feces and cephalic head 263

capsules). Finally, future studies should explore the taphonomic processes affecting scale 264

deposition, transport and sedimentation, and the magnitude of scale accumulation in 265

endemic areas versus epidemic areas. 266

This study demonstrates that wing scales can be used as a paleoecological indicator for 267

reconstructing insect outbreak history, being a more effective proxy than feces and 268

cephalic head capsules. Fossil scales have a great potential to improve our understanding 269

of the long-term dynamics of lepidopteran defoliator species that are still poorly known, 270

especially in the boreal forest. This contribution will be essential for improving the 271

accuracy of natural disturbance projections within the context of future climate change. 272

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Acknowledgements 273

This study was supported by the Natural Sciences and Engineering Research Council of 274

Canada. We thank Patrick Nadeau for his help in the field and Milla Rautio, Claire 275

Fournier, Marianne Desmeules, and Noémie Blanchette-Henry for their help and advice 276

in the laboratory. We also thank Miguel Montoro, Alison Garside and Murray Hay for 277

their help in reading and improving the quality of this manuscript. 278

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Figure captions 411

Figure 1: Scale analysis protocol. 412

Figure 2: Location of the two studied lakes. 413

Figure 3: Discriminant analysis of the three species of outbreaking lepidopterans based 414

on EFDs principal component scores and four scale shape parameters. Colour points 415

represent highly specific shapes and faded points represent more common shapes. 416

Figure 4: Scales morphotypes extract from K-mean cluster analysis of (a) Choritoneura 417

fumiferana, (b) Lambdina fiscellaria, and (c) Malacosoma disstria specific scales and (d) 418

more common scales of the three species . The bold scale represents the median shape for 419

each cluster and light grey scales represent the first standard deviation shape in each 420

cluster. 421

Figure 5: Stratigraphy of Lac Flévy. (a) Lead-210 dating based on a constant rate of 422

supply (CRS) model; (b) Total accumulation rate for the extracted scales; (c) 423

Accumulation rate of unidentified scales (scales that did not match any morphotypes, 424

common scale morphotypes, damaged scales, etc.); (d–f) Scales matching a specific 425

morphotype of one of the three outbreaking species. 426

Figure 6: Stratigraphy of Lac Hautbois. (a) Lead-210 dating based on constant rate of 427

supply (CRS) model; (b) Total accumulation rate of extracted scales; (c) Accumulation 428

rate of unidentified scales (scales that did not match any morphotypes, common scale 429

morphotypes, damaged scales, etc.); (d–f) Scales that matched a specific morphotype of 430

one of the three outbreaking species. 431

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Figure 7: Examples of (a) unidentified scales; (b) scales matching a Choristoneura 432

fumiferana morphotype; (c) scales matching a Lambdina fiscellaria morphotype; (d) 433

scales matching a Malacosoma disstria morphotype; (e) a damaged scale. 434

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Scale analysis protocol.

134x142mm (300 x 300 DPI)

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Location of the two studied lakes.

157x196mm (300 x 300 DPI)

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Discriminant analysis of the three species of outbreaking lepidopterans based on EFDs principal component scores and four scale shape parameters. Colour points represent highly specific shapes and faded points

represent more common shapes.

154x107mm (300 x 300 DPI)

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Scales morphotypes extract from K-mean cluster analysis of (a) Choritoneura fumiferana, (b) Lambdina fiscellaria, and (c) Malacosoma disstria specific scales and (d) more common scales of the three species .

The bold scale represents the median shape for each cluster and light grey scales represent the first

standard deviation shape in each cluster.

154x107mm (300 x 300 DPI)

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Stratigraphy of Lac Flévy. (a) Lead-210 dating based on a constant rate of supply (CRS) model; (b) Total accumulation rate for the extracted scales; (c) Accumulation rate of unidentified scales (scales that did not match any morphotypes, common scale morphotypes, damaged scales, etc.); (d–f) Scales matching a

specific morphotype of one of the three outbreaking species.

153x105mm (300 x 300 DPI)

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Stratigraphy of Lac Hautbois. (a) Lead-210 dating based on constant rate of supply (CRS) model; (b) Total accumulation rate of extracted scales; (c) Accumulation rate of unidentified scales (scales that did not match any morphotypes, common scale morphotypes, damaged scales, etc.); (d–f) Scales that matched a specific

morphotype of one of the three outbreaking species.

153x105mm (300 x 300 DPI)

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Examples of (a) unidentified scales; (b) scales matching a Choristoneura fumiferana morphotype; (c) scales matching a Lambdina fiscellaria morphotype; (d) scales matching a Malacosoma disstria morphotype; (e) a

damaged scale.

205x490mm (300 x 300 DPI)

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