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Zeitschrift/Journal: Entomologie heute

Jahr/Year: 2012

Band/Volume: 24

Autor(en)/Author(s): Mielewczik Michael, Liebisch Frank, Walter Achim, Greven Hartmut

Artikel/Article: Near-Infrared (NIR)-Reflectance in – Phenetic Studies of 181 Species. Infrarot (NIR)-Reflexion bei Insekten – phänetische Untersuchungen an 181 Arten 183-216 Near-Infrared (NIR)-Refl ectance of Insects 183

Entomologie heute 24 (2012): 183-215

Near-Infrared (NIR)-Reflectance in Insects – Phenetic Studies of 181 Species

Infrarot (NIR)-Reflexion bei Insekten – phänetische Untersuchungen an 181 Arten

MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER & HARTMUT GREVEN

Summary: We tested a camera system which allows to roughly estimate the amount of refl ectance prop- erties in the near infrared (NIR; ca. 700-1000 nm). The effectiveness of the system was studied by tak- ing photos of 165 species including some subspecies from museum collections (105 Coleoptera, 11 (), 12 Hymenoptera, 10 , 9 Mantodea, 4 Odonata, 13 , 1 Phasmatodea) and 16 living insect species (1 Lepidoptera, 3 Mantodea, 4 Orthoptera, 8 Phasmato- dea), from which four are exemplarily pictured herein. The system is based on a modifi ed standard consumer DSLR camera (Canon Rebel XSi), which was altered for two-channel colour infrared photography. The camera is especially sensitive in the spectral range of 700-800 nm, which is well- suited to visualize small scale spectral differences in the steep of increase in refl ectance in this range, as it could be seen in some species. Several of the investigated species show at least a partial infrared refl ectance. NIR-refl ectance is especially pronounced in specimens of an overall white, red, orange and yellow colouration, but was also found in numerous green insects (e.g. the leaf katydids Ancylecha fenestrata and Stipnochlora couloniana and the walking leaf Phyllium celebicum). In contrast, other green wings, as for example the metallic green wings of the butterfl y Troides priamus or the metallic green elytra of several jewel such as Chrysaspis aurovittata, do not refl ect NIR-radiation.

Keywords: infrared photography, NDVI, infrared refl ectance, cuticle, insect, phenotyping

Zusammenfassung: Wir stellen ein Kamerasystem vor, mit dem man in erster Annäherung die Refl exionseigenschaften von Insekten im Nah-Infrarotbereich (NIR; etwa 700-1000 nm) bestim- men kann und haben dies anhand von entsprechenden Aufnahmen von 165 Insektenarten aus Sammlungen (105 Coleoptera, 11 Hemiptera (Pentatomidae), 12 Hymenoptera, 10 Lepidoptera, 9 Mantodea, 4 Odonata, 13 Orthoptera, 1 Phasmatodea) und 16 lebenden Insektenarten (1 Lepido- ptera, 3 Mantodea, 4 Orthoptera, 8 Phasmatodea) geprüft, von denen wir vier Arten hier exemplarisch abbilden. Das System beruht auf einer modifi zierten Standard-Digitalen Spiegelrefl exkamera (Canon Rebel XSi), welche für den Einsatz als Zweikanal-Farbinfrarotkamera umgebaut wurde. Die Kamera ist besonders empfi ndlich im spektralen Bereich zwischen 700 und 800 nm, da in diesem Bereich oft kleinere Unterschiede der Steigung im Anstieg in der Refl exion bei verschiedenen Arten unterschieden werden können. Von den untersuchten Insektenarten zeigen einige zumindest partiell eine NIR- Refl exion. Diese ist besonders deutlich bei weißen, roten, orangefarbenen, gelben und besonders aus- geprägt bei einer Reihe von grünen Insektenarten (z. B. bei den Blattheuschrecken Ancylecha fenestrata und Stipnochlora couliana sowie dem Wandelnden Blatt Phyllium celebicum). Im Gegensatz dazu zeigen die Flügel anderer grüner Insektenarten, wie die metallisch grünen Elytren einer Reihe von Prachtkäfern, z. B. Chrysaspis aurovittata, oder die leuchtend grünen Flügel des Schwalbenschwanzes Troides priamus keine NIR-Refl exion.

Schlüsselwörter: Infrarot-Fotografi e, NDVI, Infrarotrefl exion, Kutikula, NIR, Insekten, Phäno- typisierung

Entomologie heute 24 (2012) 184 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN

1. Introduction 2) present the results obtained from al- together 181 species including some subspe- Insects are variously coloured and the cies (some of them are shown in NDVI- colouration has variegated functions such photographs), and 3) shortly touch the as advertisement, warning, crypsis etc. (for nature of infrared reflectance and its review see COTT 1940; FOX 1979; CHAPMAN possible adaptive value. Generally, our study 1998; LUNAU 2011). Typically, the coloura- indicates that NIR-reflectance of insect tion is produced by physical means (e.g. integuments seems to be more widespread diffraction, interference and scattering by than the existing literature suggests. nanostructures) and/or by pigments that absorb or emit light, and both, nanostruc- 2. Material and methods tures and pigments, have been thoroughly studied in insects (for review see CROMARTIE 2.1. 1959; FOX 1976; VIGNERON & SIMONIS 2010). However, investigations concerning insects We examined 165 species from the collection primarily cover colouration patterns and of the Aquazoo/Löbbecke-Museum Düs- their spectral refl ectance characteristics in seldorf and the Entomological Collection of the range from 400 to 700 nm, which is vis- the ETH Zürich, i. e. 105 Coleo ptera, 11 He- ible for humans and many other vertebrates miptera (Pentatomidae), 12 Hymenoptera, (visible spectrum of light = VIS), and the 10 Lepidoptera, 9 Mantodea, 4 Odonata, short-wave spectrum (ultraviolet/UV, 300- 13 Orthoptera, 1 Phasmatodea (Tab. 1; see 400 nm). Perceiving these patterns enable appendix) and 16 living insect species, i.e. insects to recognize mating partners, hosts, 1 caterpillar (Lepidoptera), 3 Mantodea, 4 food etc. (see MENZEL 1979; KELBER et al. Orthoptera, 8 Phasmatodea) (Tab. 2; see 2003). Studies of infrared refl ectance of appendix). We included a large number the insect integument, i.e. between 700 and of green specimens, as it is known from 1400 nm (near infrared = NIR), are rare, vertebrates that even though specimens even though initial studies of insects were can show a comparable green colouration, already performed by some of the early refl ectance in the NIR-might be completely pioneers in infrared photography (TRISTAN different (SCHWALM et al. 1977; DODD 1981; & MICHAUD 1916). COTT (1940) was one KREMPELS 1989; EMERSON et al. 1990). From of the fi rst authors, who paid attention to the museum specimens colour photos and infrared photography to study different infrared images were taken under the same green animals that may greatly differ in their conditions, the latter with a modifi ed DSLR absorption of infrared light. He presented (digital single-lens refl ex) camera (see 2.2.). infrared photographs showing a tettigoniid Colour images were acquired with a Canon grasshopper that clearly contrasted against EOS 550D and 600D camera. Images of the background of green leaves, whereas specimens from terraria were taken under the green caterpillar of Smerinthus ocellatus the local lighting conditions. Green leaves merges with the surrounding vegetation (see were used as references to quantify the COTT 1940, plates 3 & 5). amount of infrared refl ectance. All images In the present note we revive these studies were acquired in highest quality as JPEG or by screening NIR-refl ectance of a larger Canon Raw image fi les. number of dead and living insects. In de- Generally we adopted the scientifi c names tail we 1) report on some basic principles of the insects directly from the collections. of the red-edge based NDVI-photogra- In a few cases we changed the species epi- phy we used for this phenetic screening, thethon or the genus name. Near-Infrared (NIR)-Refl ectance of Insects 185

2.2. Digital infrared and red edge pho- different light intensities, the calculation of tography the NDVI-might be benefi cial. NDVI-= (RE-B)/(RE+B) For image capture a modifi ed handheld 12.2 megapixel DSLR camera (Canon Rebel XSi, Using the equation, we tested the hypothesis modifi ed by LDP LLD, Carlsted, USA, www. that the fl ash integrated in the camera and maxmax.com) was used. Such cameras are a white balance (white card) are useful to successfully used in monitoring the cover standardize image quality and small scale of vegetation (e.g. BOKHORST et al. 2012) differences under different light regimes by calculating the normalized difference (Fig. 3 A). We selected areas on images of vegetation index (NDVI) as described be- typical background vegetation such as grass low. The camera is therefore advertised as (examples can be seen in Fig. 2 A, B). NDVI-camera, a term we also use in this To evaluate the image quality and identify an study. Here we apply the same camera to optimal image procedure for image acquisi- differentiate NIR-refl ecting and NIR-non- tion we therefore compared NDVI-results reflecting insects and their surrounding under sunny and shadowy conditions (Fig. surfaces. The modifi ed camera detects light 3 B). Based on those fi ndings, which clearly in two wave length bands in the range of show that good illumination conditions are blue light (B, 370 to 480 nm) and in the preferable, we used the internal camera fl ash range of the so called red edge (RE). The for all photos. Images of the insect collections red edge lies between red and near infrared were acquired with an additional illumina- (NIR) and is characterized by a wave length tion provided by a 500 W halogen lamp to ranging from 675 to 775 nm. provide suffi cient light in the NIR-range of The 2-band model offers the possibility the spectrum. All fi gures were prepared using to differentiate between NIR-refl ecting Adobe Photoshop CS5 and Corel Draw X4. and NIR-non-refl ecting surfaces already Box plots in fi gure 3 were created and based by viewing the images. The former appear on statistical analysis performed with R 2.15.1 strongly red, whereas the latter appear (R-DEVELOPMENT-CORE-TEAM, 2008). (dark) blue. Discrimination of NIR-refl ect- ing and non-refl ecting surfaces can be easily 2.3. Abbreviations performed using the 2-band images without normalization (see below), as human vision B = blue light; NDVI-= normalized differ- itself can differentiate blue and red. For ence vegetation index; NIR-= near infrared an initial test of the camera we used two (700-1400 nm); RE = red edge (~700-800 green vertebrate species (Morelia viridis and nm); VIS = visible spectrum (400-700 nm); a green Furcifer pardalis), which are known to CCD = charged coupled device; CMOS = differ in their infrared refl ectivity marked- complementary metal-oxide semiconductor; ly (DODD 1981; KREMPELS 1989; GEHRING DSLR = digital single-lens refl ex. & WITTE 2007) (Fig. 1). Two examples for colour rendering of different natural 3. Results material provided by the modified two channel NDVI-camera are given in fi gure 3.1. Optimizing image acquisition 2. Differences are quite clear; therefore we think that normalization procedures for the The NDVI-camera is not only highly effi - images are not necessary in many cases. cient in analysing differences of vegetation However, for quantitative analyses and refl ectance, but also to differentiate high comparison of insect images taken under from low refl ectance items (Fig. 3 A, B).

Entomologie heute 24 (2012) 186 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN

Fig. 1: The NDVI-camera clearly shows refl ectance differences in the NIR. Contrary to the green tree python Morelia viridis (A), the green panther chameleon Furcifer pardalis (B) shows a high NIR- refl ectance, which is comparable to that of green coloured leaves (C). Abb. 1: Die NDVI-Kamera zeigt deutlich Refl exionsunterschiede im Infrarotbereich. Im Gegensatz zum grünen Baumpython Morelia viridis (A) zeigt das grüne Pantherchamäleon Furciger pardalis (B) eine starke Refl exion, ähnlich der Refl exion der grünen Blätter (C). Near-Infrared (NIR)-Refl ectance of Insects 187

Fig. 2: Colour rendering of the infrared sensitive NDVI-camera. A Landscape with different materials. Vegetation appears pink to light red (high NIR-refl ectance), stones and sand are violet to blue (low NIR-refl ectance). B Depending on shadow, illumination, kind of leaves and light quality, vegetation may show small variations, but the high refl ectance in the NIR is always obvious. However, other colours than green, e.g. the yellow fur of a tiger (Panthera tigris), reveal a similar NIR-refl ectance as the vegetation. Abb. 2: Farbrendering der infrarotsensitiven NDVI-Kamera. A Landschaft mit verschiedenen Materialien. Die Vegetation erscheint pink oder rot (hohe NIR-Refl exion), Steine und Sand sind violett bis blau (niedrige NIR-Refl exion). B In Abhängigkeit von Schatten, Lichtintensität, Blattbe- schaffenheit und Lichtqualität kann die Farbdarstellung der Vegetation variieren, jedoch ist die starke Refl exion im NIR klar erkennbar. Auch andere sichtbare Farben als Grün können eine ähnlich starke Infrarotrefl exion aufweisen, z.B. weist das orangerote Fell des Tigers (Panthera tigris) eine ähnliche NIR-Refl exion auf wie die Pfl anzen im Schatten.

Entomologie heute 24 (2012) 188 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN

Using a white card and the integrated 3.2 1. Coleoptera (museum specimens) camera-flash clearly shows that under shadowy conditions NDVI-values of dif- Black species such as scabrosus ferent background vegetation increase and typically show no NIR-refl ectance. In con- variation decreases (Fig. 3 A). Further, it is trast, most dark brownish to red brownish shown that under strong light regimes the specimens show a weak to medium refl ec- differences between samples are more pro- tance. Such beetles were found in nearly all nounced (Fig. 3 B). Images of specimens groups of brownish coleopteran investi- were thus all acquired using automatic gated, e.g. in the Buprestidae, Dynastidae, white balance and the internal compulsory Elateridae and Scarabidae (see Tab. 1; Fig. fl ash of the camera. 5). Beetles, which possess orange, yellow Even though limited to a two colour mo- or red colouration or markings, typically del, the acquired images share a coloura- possess a higher NIR-refl ectance than dark- tion scheme, which is highly comparable brown specimens. In some cases (e. g. in to those of fi lm-based, classic 3-colour- Eudicella smithi or Sternotomis bohndorfi i) the infrared photography (for comparisons orange legs or antennas showed a medium see GIBSON 1978). NIR-refl ectance. The highest phenetic plas- ticity was found in green-coloured beetles. 3.2. NIR-refl ectance in insects Most metallic green beetles, as for example Sternocera sternicornis, Sternotomis bohndorfi i and Generally, our NIR-images reveal a remark- Stephanorrhina guttata, do not show a marked able variation not only concerning the NIR-refl ectance, in contrast to their orange occurrence of NIR-refl ectance, but also patterns. There was also a small number concerning the refl ectance patterns (for an of green beetles (for example Smaragdesthes overview see Tabs. 1, 2; Figs. 4-10). Only for africana and Caelorrhina superba), in which a description we herein use fi ve categories to medium refl ectance could be found. In C. characterize refl ectance: no, very weak, weak, superior fi ve of the examined specimens did medium, strong (see Fig. 4). not show any NIR-refl ectance, while two

Fig. 3: A NDVI-values of grass vegetation under shadowy (left) and sunny (right) conditions as affected by the corrective treatments (norm = without corrective treatment, wb = white card used for image capture, wb+fl ash = white card and internal fl ash used for image capture). The NDVI- values increase, when a white card and a white card plus internal fl ash of the camera are used under shadowy conditions. Under sunny conditions NDVI-values are highest and corrective measures have no effect. In the boxplots (n = 9 replicates) the horizontal line represents the median, the bottom and the top of the box show the 25th and 75th percentile, respectively, and whiskers represent either the maximum value or 1.5 times the interquartile range, which ever is the smaller. Points higher than 1.5 times are shown as single points (potential outlier). B Differences of various background vegetation samples under shadowy (top) and sunny (bottom) conditions (n = 3). A better light regime reduces the variance and allows a better discrimination of the different surfaces. Abb. 3: A NDVI-Werte von Grasvegetation unter schattigen (links) und sonnigen (rechts) Umwelt- bedingungen in Abhängigkeit von Korrekturen während der Aufnahmen (norm = ohne Korrektur, wb = Weißabgleich mit weißer Karte während der Bildaufnahme, wb+fl ash = Weißabgleich mit gleichzeitig verwendetem Blitz). Durch den Einsatz der weißen Karte und der weißen Karte mit Blitz steigt der NDVI-Wert unter schattigen Bedingungen. Unter sonnigen Bedingungen sind die NDVI-Werte am größten und die zusätzlichen Korrekturmaßnahmen haben keinen Effekt. In den Boxplots (n = 9 Replikate) repräsentiert die horizontale Linie den Median und das untere und obere Ende der Box jeweils den 25- und 75-Perzentil. Die Whisker zeigen entweder den Maximalwert Near-Infrared (NIR)-Refl ectance of Insects 189

shadow sun

norm wb wb + fl ash norm wb wb + fl ash

corrective treatment corrective treatment

shadow

sun

sample oder den 1.5-Interquartilbereich. Einzelpunkte zeigen Werte außerhalb dieses Bereichs (potenzielle Ausreißer). B Unterschiede zwischen verschiedenen Vegetationsbeispielen bei schattigen (oben) und sonnigen (unten) Bedingungen (n = 3). Bessere Lichtverhältnisse reduzieren die Varianz und machen verschiedene Oberfl ächen besser voneinander unterscheidbar.

Entomologie heute 24 (2012) 190 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN

Fig. 4: Different Pentatomidae species in a showcase. Overview (A) and NIR (B-F) and conven- tional color photos (G-K) of selected species, which either do not refl ect NIR (B) or refl ect (C) very weak, (D) weak , (E) with medium intensity and (F) high. (B+G) Trochycocoris rotundatus, (C+H) Dolycoris baccarum, (D+I) juniperina, (E+J) viridissima and (F+K) Nezara viridula. Abb. 4: Verschiedene Pentatomiden in einem Schaukasten. Übersicht (A) sowie NIR- (B-F) und Farbaufnahmen (G-K) einzelner Arten, die entweder (B) kein NIR refl ektieren oder (C) sehr schwach, (D) schwach, (E) mittelstark und (F) stark refl ektieren. (B+G) Trochycocoris rotundatus, (C+H) Dolycoris baccarum, (D+I) Chlorochroa juniperina, (E+J) Palomena viridissima, (F+K) Nezara viridula. Near-Infrared (NIR)-Refl ectance of Insects 191 showed either a weak or medium to strong paris showed a somewhat higher refl ec- refl ectance (Fig. 6). The latter specimens tance, compared to the rest of the wings. A showed a slight reddish tint in their green higher refl ectance was also found in yellow colouration when viewed in the visible or orange markings of euchenor and spectrum. Teinopalpus imperialis. The green iridescent areas on the wings of T. imperialis and P. 3.2.2. Hemiptera (Pentatomidae, mu- paris showed a very weak NIR-refl ectance, seum specimens) if any.

Black specimens, e.g. Trochicocoris rotundatus, 3.2.5. Odonata (museum specimen) did not show any NIR-refl ectance in the black parts of their body (see Fig 4, Tab. 1). In contrast to the yellow spots on the abdo- In contrast, in green and brown specimens men of a female Libellula depressa, the dark of Chlorochroa juniperina, Dolycoris baccarum, body parts of Odonata species did not show Palomena prasina and Palomena viridissima va- any NIR-refl ectance (see Tab. 1). Whitish rious shades of NIR-refl ectance were found transparent exuviae of various unclassifi ed (Fig. 4 A, C-E). Nezara viridula showed an species generally showed a high refl ectance exemplarily high NIR-refl ectance. (data not shown).

3.2.3. Hymenoptera (museum speci- 3.2.6. Mantodea, Orthoptera and mens) Phasmatodea (museum and living specimens) NIR-refl ectance of the black body parts was low in all Hymenoptera species investigated A green living specimen of Mantis religiosa (Tab. 1), whereas the yellow striped mark- showed an extremely high NIR-refl ectance, ings of different wasps showed a medium comparable to that of green leaves (Tab. 2). refl ectance. The transparent wings appearing The brownish wandering violin mantis Gon- yellowish in the visible spectrum showed a gylus gongylodes showed only a weak to me- higher refl ectance. dium refl ectance, similar to the twigs in its terrarium. Similar observations were made 3.2.4. Lepidoptera (museum and living on several other green and brown species specimens) of Orthoptera and Phasmatodea (Tab. 2). Green leaf katydids such as Ancylecha fe- Dark patterns of caterpillars from muse- nestrata and Stilpnochlorchis couloniana showed um specimens generally showed a reduced a strong NIR-refl ectance comparable to or no NIR-refl ectance. The green cater- that of green leaves (Fig. 8). Yellow or green pillars of Endromis versicoloura and Saturnia coloured body parts of Schistocerca gregaria pavonia revealed a medium refl ectance. A showed a strong reflectance. This also high NIR-refl ectance was found in living applies to juvenile stages that, however, green caterpillars of the Atlas Atta- possess large black, non-refl ecting mar- cus atlas (Fig. 7). Cocoons of this species kings. Very young nymphs are completely showed a weak to medium refl ectance black and easy to discriminate from back- comparable to that of bark. Brown wing ground vegetation in the NIR-photos. We parts of adult butterfl ies such as Prepona also observed a slight sexual dimorphism chromus typically show a weak to medium in this species regarding NIR-refl ectance refl ectance. The light blue markings of (Fig. 9). A very high NIR-reflectance this species and the Paris peacock Papilio was also observed in green Phasmato-

Entomologie heute 24 (2012) 192 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN

Fig. 5: Specimens of different beetle species shown in conventional colour (A,C,E) and NIR-photos (B,D,F). The brown to red brown jewel beetle Sternocera hildebrandti (A+B) shows a medium NIR- refl ectance, as the light brown elytra of the stag beetle Dicranocephalus bowringi (E+F). The green cetoniid Ischiosopha lucivorax (C+D) does not show any NIR-refl ectance. Abb. 5: Individuen von verschiedenen Käfern gezeigt in Farb- (A,C,E) und NIR- (B,D,F) Foto- grafi e. Die braun bis rotbraunen Prachtkäfer Sternocera hildebrandti (A+B) zeigen eine mittlere NIR- Refl exion, wie die hellbraunen Flügeldecken des Hirschkäfers, Dicranocephalus bowringi (E+F). Die grünen Rosenkäfer Ischiosopha lucivorax (C+D) zeigen keine NIR-Refl exion. Near-Infrared (NIR)-Refl ectance of Insects 193

Fig. 6: Specimens of the rose chafer Caelorrhina superba (A) differ considerably concerning NIR- refl ectance (B). Black beetles such as Carabus scabrosus tauricus (C) generally do not show NIR- refl ectance (D). Abb. 6: Individuen des Rosenkäfers Caelorrhina superba (A) unterscheiden sich hinsichtlich ihrer NIR-Refl exion beträchtlich (B). Schwarze Käfer wie Carabus scabrosus tauricus (C) zeigen generell keine NIR-Refl exion (D). dea species such as Heteropteryx dilatata, 4. Discussion Diapherodes gigantea and Phyllium celebicum. In contrast, brown Phasmatodea as Ex- Techniques of infrared photography are at tatosoma tiaratum appeared darker and hand now for more than 100 years, beginn- blueish in NIR-images similar to the co- ing with the discovery that vegetation or louration of twigs and dry brown leaves. better green leaves possess an extremely Observations from living specimens gene- high refl ectance in the NIR-range of the rally agree with those of dead museum speci- spectrum and, thus, appear snow-white in mens. Yet, it should be noted that colours of monochrome infrared images (WOOD 1910 green and yellow Mantodea and Orthoptera a, b). This unusual photographic peculiarity species in the collection tend to fade. is commonly known as the Wood effect,

Entomologie heute 24 (2012) 194 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN

Fig. 7: The bluish-green caterpillar of the Atlas moth Attlacus atlas (A) exhibits a high NIR-refl ectance (C), which markedly differs from that of the leaves because of its high blue light refl ection. The seemingly higher NIR-refl ectance of the leaves is caused by their low blue light refl ectance. The brownish cocoon shows a much lower refl ectance in both wave bands (B). Abb. 7: Die blau-grüne Raupe der Atlasmotte Attlacus atlas (A) weist eine hohe NIR-Refl exion auf (C), die sich wegen ihrer starken Blaulichtrefl exion stark von der der NIR-Refl exion der Blätter unterscheidet. Die scheinbare höhere NIR-Refl exion der Blätter ist durch ihre geringe Blaulichtrefl exion bedingt. Die braune Puppe zeigt eine viel geringere Refl exion in beiden Wel- lenlängenbereichen (B). Near-Infrared (NIR)-Refl ectance of Insects 195

Fig. 8: The Malaysian katydid Ancylecha fenestrata (A) shows a strong NIR-refl ectance (B). Abb. 8: Die Malaysische Blattschrecke Ancylecha fenestrata (A) zeigt eine starke NIR-Refl exion (B). a term still widely used by enthusiastic of science (e.g. CLARK 1947; GIBSON 1978; amateurs and professional infrared photo- VERHOEVEN 2008). graphers. Since then infrared photography More recently film-based infrared pho- has been frequently used in different fi elds tography has been substituted by digital

Entomologie heute 24 (2012) 196 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN

Fig. 9: The female of the desert locust Schistocerca gregaria appears slightly darker compared to the male that shows a NIR-refl ectance similar to the grass vegetation; the nymphs (on the top) do not refl ect any NIR. Abb. 9: Das Weibchen der Wanderheuschrecke Schistocerca gregaria erscheint etwas dunkler als das Männchen, das eine sehr starke NIR-Refl exion zeigt; die Nymphen (oben) refl ektieren kein NIR. Near-Infrared (NIR)-Refl ectance of Insects 197

Fig. 10: The leaf insect Phyllium celebicum (A) and its NIR-refl ectance (B) similarly strong as the surrounding vegetation. Abb. 10: Das Wandelnde Blatt Phyllium celebicum (A) refl ektiert im NIR (B) ähnlich stark wie die umgebende Vegetation. cameras, with the consequence that co- In principle, however, all CCD (charge- lour infrared fi lms are no longer available coupled device) and CMOS (complemen- (VERHOEVEN 2008) and that commercial tary metal-oxide-semiconductor) sensors of laboratories have ceased fi lm processing. digital consumer cameras are also sensitive

Entomologie heute 24 (2012) 198 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN to near-infrared up to 1100 nm due to directly on the CCD sensor by the manufac- the intrinsic physical properties of silicon turer. In consequence, both the view fi nder (FREDEMBACH & SÜSSTRUNK 2008, 2010). and the live view mode are fully functional. Yet, in front of the CCD sensor a more or (2) There are also no limitations to auto- less effi cient “hot-mirror” is integrated into exposure and sensor cleaning functions. the camera sensor to block infrared light, (3) The narrow RE-bandwidth of the which improves the overall image quality. camera limited to the range of about Therefore, any consumer DSLR camera 675 to 800 nm. Therefore any problems can be used to acquire NIR-images, if related to wavelength-dependent shifts in the exposure time is suffi ciently long and the camera focus typically occuring in NIR- if a fi lter is used to block the visible light photography are minimized and even the (VERHOEVEN 2008). However, very long autofocus can be used. (4) There appear exposure times are often not practicable to be no limitations concerning the use of and may reduce image quality, but most various lenses. digital consumer cameras can be modifi ed For general visualization of differences in into NIR-sensitive cameras by removing NIR-refl ectance it does not appear to be the internal hot-mirror (used in normal necessary to normalize the generated images photography to block NIR-light) and using (see equation p. 185), though it can be help- different red or infrared band-pass fi lters, ful whenever quantitative imaging is needed, similar to those used in classical infrared e. g. in vegetation studies. Under shadowy photography (see GIBSON 1978 for fi lters condition (e. g. cloudy sky, tree canopy, in- used in infrared photography and TETLEY door) image quality can be improved by us- & YOUNG 2007, 2009 for details on infrared ing white cards and internal fl ashes. That in camera modifi cation). Commonly, those fi l- our study these NDVI-values did not reach ters can be attached either to the front lens NDVI-values obtained in full sun can be of the camera or they are mounted behind explained by the weak fl ash of the camera. the lens on the sensor during camera modi- Using a stronger external fl ash will probably fi cation. As fi lter usage is not standardized increase these values. We showed that addi- presently, digital colour infrared photog- tional light during image capture improves raphy requires digital post-processing, e.g. image quality for analytical purposes. manual colour adjustments. Infrared photography for image-based phe- The herein presented results show that the notyping of animals has already been pro- modifi ed NDVI-camera used by us is an posed by DODD (1981) and especially KREM- effi cient and useful alternative to perform PELS (1989). Now digital infrared cameras digital infrared photography for scientifi c enormously simplify this method, not only purposes (for references on digital infrared because it is easier to acquire many images in photography see VERHOEVEN 2008). Ad- a short time, but also (even more important vantages are a colour scheme based on two to our opinion) because time-consuming and bands, which is not only easy to understand, costly fi lm processing in a darkroom specifi - but also matches partially the false colour cally equipped for infrared photography has rendering of previous colour infrared fi lms become obsolete. In addition, recent digital (for reference see GIBSON 1978). Concern- consumer cameras have further advantages ing applied NIR-photography, the NDVI- very useful for image-based phenotyping, i. camera has several advantages: (1) It is not e. additional meta-information can be auto- necessary to apply any additional fi lter in matically integrated into the image during front of the lens to block the visible light, image acquisition such as used lens, exposure as the fi lter has been integrated back-lens time, fl ash mode etc., which can be accessed Near-Infrared (NIR)-Refl ectance of Insects 199 later on any computer (MIELEWCZIK 2002, that were dried and stored in drawers. This 2003 a, 2003 b). Also various epithetha can shows that these specimens retained this be attached to the images using additional property at least in part. We assume that meta-data fi elds provided by the IPTC image NIR-refl ectance observed in these speci- fi le extensions (see for example MIELEWCZIK mens is largely attributed to the organization 2007 a), which is helpful in managing huge and pigmentation of the cuticle; the under- databases with several thousand images. We lying epidermis should be destroyed. The believe it is best to acquire images in RAW general “lamellate” structure for example and JPEG mode simultaneously. RAW of the elytron cuticle – hardly or not to be image fi les generally provide the highest seen in the exocuticle – is conserved (e.g. quality and degree of freedom for post- VAN DE KAMP & GREVEN 2010). The same processing purposes (see for example applies for structural colours of the cuticle, MIELEWCZIK 2007 b), while JPEG fi les are e. g. the multilayered refl ectors in the cuticle much easier to handle in day-to day-use due of beetles (SEAGO et al. 2009), which can be to their smaller size. identifi ed even in fossils (PARKER & MCKEN- ZIE 2003; TANAKA et al. 2010; MCNAMARA et 4.1. Infrared refl ectance of insects al. 2012). Also preserved are dark and brown patterns caused generally by tanning (elytra The most striking result of our study is the are often heavily sclerotized), but also by fact that many green insects show a very high melanization, which was seen in many of NIR-refl ectance, which closely resembles the species examined. that of leaves. This was especially found in However, some pigments appear to fade living specimens of walking leaves (Phasma- in course of the time, e.g. in the green and todea) and green Orthoptera such as Phyl- otherwise coloured species of Mantodea, lium celebicum and couloniana. All Phasmatodea, Orthoptera and also in light species are known for camoufl age and phy- coloured caterpillars. Their green and yel- tomimesis (for summary see LUNAU 2011). low patterns are caused by the simultaneous Spectral similarities between green insects, presence of selectively blue (carotenes) and such as caterpillars, grasshoppers, mantis red absorbing pigments, such as chromo- and walking leaves, and true leaves have proteins containing non-covalently bound been known for a long time (BECQUEREL & biliverdin IXα as prosthetic group (PRZIBRAM BRONGNIART 1894; PRZIBAM 1913). However, & LEDERER 1933; KAWOOYA et al. 1985; OKAY to our knowledge it has never been reported 1945; PASSAMA-VUILLAUME & BARBIER 1966; for any mantid or orthopteran species that RÜDIGER 1970; HOLDEN et al. 1987; WIL- this property extends into the NIR-range LIG 1969). Therefore, we assume that here of the spectrum. Spectra of green insect photo-oxidation and chemical degradation species showing a high NIR-refl ectance are are responsible for bleaching, but, neverthe- known from a caterpillar (Rhodenia fugax: less, some NIR-refl ectance is retained. SAITO 2001) and in the metallic green beetles We think that also some further parameters Calloodes grayanus (PARKER et al. 1998) and may affect NIR-refl ectance such as thinness Charidotella egregia (VIGNERON et al. 2007). of the cuticle and their dehydration. An opposite effect (i.e. higher refl ectance) is 4.1.1. Museum specimens known from stacking of leaves due to the reduced transmission (ALLEN & RICHARDSON We found different intensities of NIR- 1968, see also GATES 1980). Further, drying reflectance in a large number of dead of the cuticle may lead to another effect, also specimens from the museum collections known from studies of leaves: Scattering co-

Entomologie heute 24 (2012) 200 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN effi cients in diffuse refl ectance over the VIS If these suggestions are right, putative and NIR-range of the spectrum generally predators or prey must be able to see in increase in dehydrated tissues (ALLEN & the NIR-and RE range of the spectrum. RICHARDSON 1968; see GATES 1980). De- Spectral tuning of NIR-reflectance and hydrated leaves show an increase in refl ec- the steep increase of refl ectance in the RE tance over the whole range of the spectrum might be benefi cial to baffl e predators that from 400-2500 nm (CARTER 1991; RASCHER show a shift toward longer wavelengths in et al. 2007), although only the increased re- their spectral sensitivity. Up to date true fl ectance in the range of 1000 to 2500 nm is sensitivity in the NIR, fi rst suggested by early thought to be directly related to absorption pioneers in infrared photography (TRISTAN of water (JACQUEMOUD et al. 1996; RASCHER & MICHAUD 1916), has been reported in et al. 2010). Nevertheless, the acquired a limited number of various invertebrate NDVI-infrared images of the insects exam- and vertebrate taxa, e.g. Crustacea (Mysis ined herein show areas and patterns of dark relicta: LINDSTRÖM & MEYER-ROCHOW 1987), and brown colourations that are retained Coleo ptera (Hypera postica: Meyer 1976), in the museum specimens and play a ma- Teleostei (Rutilus rutilus: LOEW & LYTHGOE jor role in the overall spectral and spatial 1985; Oreochromis mossambicus: SHCHERBAKOV absorption in the RE- and NIR-range of et al. 2012), Dipnoi (Neoceradotus fosteri: the spectrum. HART 2008), Squamata (Anolis carolinensis: Further, our study indicates that insect KAWAMURA & YOKOYAMA 1998; PROVENCIO et species with a considerably high NIR- al. 1992), Mammalia (Mustelus furo: NEWBOLD refl ectance are found throughout the world 2007, NEWBOLD & KING 2009). Infrared and in different taxa. We think that this vision in birds (VANDERPLANCK 1934, WOJ- phenomenon might be more common in TUSIAK 1949) and turtles (WOJTUSIAK 1947) species living on leaves. Here, NIR-refl ec- has been doubted (for discussions see for tance matches to the green background. example MATTHEWS & MATTHEWS 1939, IN Similarly, NIR-refl ectance of dark or brown DEN BOSCH 1987). insects may match to their local substrate. It is also possible that refl ectance in the Generally, however, the adaptive value of far-red and near-infrared has an adaptive NIR-refl ectance of insects and animals is value with respect to interspecifi c visual largely unknown and only a few sugges- interactions, as it has been suggested for tions are given herein: KREMPELS (1989), example in fi sh and some squamates (PAR- who studied infrared refl ectance of several TRIDGE et al. 1989; PROVENCIO et al. 1992). frogs and squamates assumed an adaptive NIR-refl ectance may also affect thermo- camoufl age of predators and suggested regulation as heatload may be increased that IR-refl ectance in coral snakes con- (for discussion see IN DEN BOSCH 1987). tributes to their aposematic colouration. Furthermore, it had been suggested, that Interestingly, we found NIR-refl ectance in IR-refl ectance might be only an inevitable the green predatory Mantis religiosa, which by-product of the colour pattern in the in turn may baffl e its prey. Brownish or visible part of the spectrum (IN DEN BOSCH red colouration is accompanied by a weak 1987). For all suggestions convincing ex- to medium NIR- refl ectance (Buprestidae: perimental evidence is missing. WAGNER 1971; and many other dark insects To our knowledge the structural basis of IR- including several phasmids). This fi ts very refl ectance is not yet satisfactorily clarifi ed. In well into the general cryptic protective Lepidoptera pterin is suggested to contribute strategies of many stick insects (Phasmato- to the overall refl ectance of the longer wave- dae) (for review see BEDFORD 1978). lengths within the visible spectrum (RUTOWSKI Near-Infrared (NIR)-Refl ectance of Insects 201 et al. 2005) and therefore may also cover the Dr. ANDREAS MÜLLER and FRANZISKA SCHMID NIR-range. We believe that the very high (Institute of Agricultural Sciences, Applied NIR-refl ectance demonstrated in various in- Entomology Group, ETH Zürich), who sects or their larvae is based on the structural made available to us the insect specimens properties of their integument, i.e. the cuticle from the collection of the Museum, and and epidermis. These properties may lead to a SUSANNE TITTMANN (Forschungszentrum broadband high and diffuse refl ectance, span- Geisenheim) for support in photography ning the VIS and NIR-spectrum. The NIR- on excursions. refl ectance is furthermore characterized by absorption of brownish and dark pigments. Literature Additional blue and red absorbing pigments such as erythropterin and carotenoids (blue ALLEN, W.A., & RICHARDSON, A.J. (1968): Interac- absorbing) and biliverdin (red absorbing) tion of light with a plant canopy. Journal of occurring in both, the cuticle and the epi- the Optical Society of America 58: 1023-1028. BECQUEREL, H., & BRONGNIART, C. (1894): La dermis (LENAU & BARFOED 2008), may lead matière verte chez les Phyllies. Comptes to the green appearance of the specimens. In rendus hebdomadaires des séances de l’Aca- addition, multiple layers with an alternating démie des sciences 118: 1299-1303. pattern of low and high refractive indices, as BEDFORD, G.O. (1978): Biology and ecology of typical for the cuticle in general, the phasmatodea. Annual Review of Ento- can defi ne not only visible colours (LAND mology 23: 125-49. 1966; LENAU & BARFOED 2008), but may also BOKHORST, S., TØMMERVIK, H., CALLAGHAN, T.V., defi ne NIR-refl ectance. PHOENIX G.K., & BJERKE, J.W. (2012): Veg- Especially the various taxa of green metallic- etation recovery following extreme winter coloured beetles such as Stephanorrhina gut- warming events in the sub-Arctic estimated using NDVI-from remote sensing and hand- tata and some butterfl ies such as Teinopalpus held passive proximal sensors. Environmental imperialis show a wide range of variation in and Experimental Botany 81: 18-25. the intensity of NIR-refl ectance, which may CARTER, G.A. (1991): Primary and secondary be related to the different modes of colour effects of water content on the spectral refl ec- production (e.g. scattering, diffraction or tance of leaves. American Journal of Botany interference effects) (for references see FOX 78: 916-924. & VEVERS 1960; CHAPMAN 1998; MICHIELSEN CHAPMAN, R.F. (1998): The insects. Structure and function. 3rd edition. University Press; & STAVENGA 2008; LENAU & BARFOED 2008). More diffi cult to explain are interspecifi c Cambridge. CLARK, W. (1947): Photography by infrared – Its differences as demonstrated in Caelorrhina principles and application. 2nd edition. John superba. Here polarizing effects in the nano- Wiley & Sons; London, New York. structure may affect NIR-refl ectance. COTT, H.B. 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Appendix Individuen Die Anzahl der untersuchten e. fi Insektenartenexion von aus Museumssammlungen basierend auf “Red-Edge”-Fotogra c name. c ectance of Number of “Red-Edge”-Photography. collections as estimated by insects from museum examined specimens in brackets fl fi fl NIR-re NIR-Re Tab. 1: Namen. steht in Klammern hinter dem wissenschaftlichen Tab. 1: after the scienti

Entomologie heute 24 (2012) 206 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN Continued. Fortsetzung. Tab. 1: Tab. 1: Tab. Near-Infrared (NIR)-Refl ectance of Insects 207 Continued. Fortsetzung. Tab. 1: Tab. 1: Tab.

Entomologie heute 24 (2012) 208 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN Continued. Fortsetzung. Tab. 1: Tab. 1: Tab. Near-Infrared (NIR)-Refl ectance of Insects 209 Continued. Fortsetzung. Tab. 1: Tab. 1: Tab.

Entomologie heute 24 (2012) 210 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN Continued. Fortsetzung. Tab. 1: Tab. 1: Tab. Near-Infrared (NIR)-Refl ectance of Insects 211 Continued. Fortsetzung. Tab. 1: Tab. 1: Tab.

Entomologie heute 24 (2012) 212 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN Continued. Fortsetzung. Tab. 1: Tab. 1: Tab. Near-Infrared (NIR)-Refl ectance of Insects 213 Continued. Fortsetzung. Tab. 1: Tab. 1: Tab.

Entomologie heute 24 (2012) 214 MICHAEL MIELEWCZIK, FRANK LIEBISCH, ACHIM WALTER, & HARTMUT GREVEN Continued. Fortsetzung. Tab. 1: Tab. 1: Tab. Near-Infrared (NIR)-Refl ectance of Insects 215 e. fi lebenden Insekten basierend aufexion von „Red-Edge“-Fotogra ectance of Red-Edge-Photography. insects as estimated by living fl fl NIR-re NIR-Re Tab. 2: Tab. 2: Tab.

Entomologie heute 24 (2012)