Abstract

High-resolution 3D imaging technology has found a number of applications in many biological fields. However, the existing 3D imaging tools are often too time-consuming to use on large-scale specimens, such as centimeter-sized insects. In addition, most 3D imaging systems discard the natural color information of the specimens. To surmount these limitations, we present a structured illumination-based approach capable of delivering large field-of-view three-dimensional images. With this approach, 580nm lateral resolution full-color 3D images and 3D morphological data in the size range of typical insect samples can be obtained. This method provides a promising approach that can be used to support many different types of entomological investigations, including taxonomy, evolution, bionics, developmental biology, functional morphology, paleontology, forestry, etc.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2017 (1)

2016 (4)

X. Zhou, M. Lei, D. Dan, B. Yao, Y. Yang, J. Qian, G. Chen, and P. R. Bianco, “Image recombination transform algorithm for superresolution structured illumination microscopy,” J. Biomed. Opt. 21(9), 96009 (2016).
[Crossref] [PubMed]

J. Liu, C. Liu, J. Tan, B. Yang, and T. Wilson, “Super-aperture metrology: overcoming a fundamental limit in imaging smooth highly curved surfaces,” J. Microsc. 261(3), 300–306 (2016).
[Crossref] [PubMed]

D. M. Lodge, P. W. Simonin, S. W. Burgiel, R. P. Keller, J. M. Bossenbroek, C. L. Jerde, A. M. Kramer, E. S. Rutherford, M. A. Barnes, M. E. Wittmann, W. L. Chadderton, J. L. Apriesnig, D. Beletsky, R. M. Cooke, J. M. Drake, S. P. Egan, D. C. Finnoff, C. A. Gantz, E. K. Grey, M. H. Hoff, J. G. Howeth, R. A. Jensen, E. R. Larson, N. E. Mandrak, D. M. Mason, F. A. Martinez, T. J. Newcomb, J. D. Rothlisberger, A. J. Tucker, T. W. Warziniack, and H. Zhang, “Risk Analysis and Bioeconomics of Invasive Species to Inform Policy and Management,” Annu. Rev. Environ. Resour. 41(1), 453–488 (2016).
[Crossref]

L. Xing, R. C. McKellar, M. Wang, M. Bai, J. K. O’Connor, M. J. Benton, J. Zhang, Y. Wang, K. Tseng, M. G. Lockley, G. Li, W. Zhang, and X. Xu, “Mummified precocial bird wings in mid-Cretaceous Burmese amber,” Nat. Commun. 7(1), 12089 (2016).
[Crossref] [PubMed]

2015 (3)

B. Bartkowski, N. Lienhoop, and B. Hansjürgens, “Capturing the complexity of biodiversity: A critical review of economic valuation studies of biological diversity,” Ecol. Econ. 113, 1–14 (2015).
[Crossref]

J. Qian, M. Lei, D. Dan, B. Yao, X. Zhou, Y. Yang, S. Yan, J. Min, and X. Yu, “Full-color structured illumination optical sectioning microscopy,” Sci. Rep. 5(1), 14513 (2015).
[Crossref] [PubMed]

Z. Wang, M. Lei, B. Yao, Y. Cai, Y. Liang, Y. Yang, X. Yang, H. Li, and D. Xiong, “Compact multi-band fluorescent microscope with an electrically tunable lens for autofocusing,” Biomed. Opt. Express 6(11), 4353–4364 (2015).
[Crossref] [PubMed]

2014 (4)

C. X. Song, F. Liu, Y. H. Hao, X. H. Hu, Y. F. Zhang, and X. H. Liu, “Multilayer manipulated diffraction in flower beetles Torynorrhina flammea: intraspecific structural colouration variation,” J. Opt. 16(10), 105302 (2014).
[Crossref]

R. Tingley, M. Vallinoto, F. Sequeira, and M. R. Kearney, “Realized niche shift during a global biological invasion,” Proc. Natl. Acad. Sci. U.S.A. 111(28), 10233–10238 (2014).
[Crossref] [PubMed]

C. V. Nguyen, D. R. Lovell, M. Adcock, and J. La Salle, “Capturing natural-colour 3D models of insects for species discovery and diagnostics,” PLoS One 9(4), e94346 (2014).
[Crossref] [PubMed]

F. Peyrin, P. Dong, A. Pacureanu, and M. Langer, “Micro- and nano-CT for the study of bone ultrastructure,” Curr. Osteoporos. Rep. 12(4), 465–474 (2014).
[Crossref] [PubMed]

2013 (3)

A. S. Mori, T. Furukawa, and T. Sasaki, “Response diversity determines the resilience of ecosystems to environmental change,” Biol. Rev. Camb. Philos. Soc. 88(2), 349–364 (2013).
[Crossref] [PubMed]

D. Simberloff, J. L. Martin, P. Genovesi, V. Maris, D. A. Wardle, J. Aronson, F. Courchamp, B. Galil, E. García-Berthou, M. Pascal, P. Pyšek, R. Sousa, E. Tabacchi, and M. Vilà, “Impacts of biological invasions: what’s what and the way forward,” Trends Ecol. Evol. (Amst.) 28(1), 58–66 (2013).
[Crossref] [PubMed]

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref] [PubMed]

2012 (2)

J. Michels and S. N. Gorb, “Detailed three-dimensional visualization of resilin in the exoskeleton of arthropods using confocal laser scanning microscopy,” J. Microsc. 245(1), 1–16 (2012).
[Crossref] [PubMed]

B. Wiesner, O. Hybl, and G. Häusler, “Improved white-light interferometry on rough surfaces by statistically independent speckle patterns,” Appl. Opt. 51(6), 751–757 (2012).
[Crossref] [PubMed]

2011 (1)

E. Shevtsova, C. Hansson, D. H. Janzen, and J. Kjærandsen, “Stable structural color patterns displayed on transparent insect wings,” Proc. Natl. Acad. Sci. U.S.A. 108(2), 668–673 (2011).
[Crossref] [PubMed]

2010 (1)

S. J. Schambach, S. Bag, L. Schilling, C. Groden, and M. A. Brockmann, “Application of micro-CT in small animal imaging,” Methods 50(1), 2–13 (2010).
[Crossref] [PubMed]

2009 (1)

2008 (1)

2007 (2)

J. Michels, “Confocal laser scanning microscopy: using cuticular autofluorescence for high resolution morphological imaging in small crustaceans,” J. Microsc. 227(Pt 1), 1–7 (2007).
[Crossref] [PubMed]

J. P. Vigneron, J. M. Pasteels, D. M. Windsor, Z. Vértesy, M. Rassart, T. Seldrum, J. Dumont, O. Deparis, V. Lousse, L. P. Biró, D. Ertz, and V. Welch, “Switchable reflector in the Panamanian tortoise beetle Charidotella egregia (Chrysomelidae: Cassidinae),” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 76(3 Pt 1), 031907 (2007).
[Crossref] [PubMed]

2006 (1)

W. A. Kalender, “X-ray computed tomography,” Phys. Med. Biol. 51(13), R29–R43 (2006).
[Crossref] [PubMed]

2005 (4)

S. Kinoshita and S. Yoshioka, “Structural colors in nature: the role of regularity and irregularity in the structure,” ChemPhysChem 6(8), 1442–1459 (2005).
[Crossref] [PubMed]

J. A. Conchello and J. W. Lichtman, “Optical sectioning microscopy,” Nat. Methods 2(12), 920–931 (2005).
[Crossref] [PubMed]

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref] [PubMed]

L. P. Lee and R. Szema, “Inspirations from biological optics for advanced photonic systems,” Science 310(5751), 1148–1150 (2005).
[Crossref] [PubMed]

Adcock, M.

C. V. Nguyen, D. R. Lovell, M. Adcock, and J. La Salle, “Capturing natural-colour 3D models of insects for species discovery and diagnostics,” PLoS One 9(4), e94346 (2014).
[Crossref] [PubMed]

Apriesnig, J. L.

D. M. Lodge, P. W. Simonin, S. W. Burgiel, R. P. Keller, J. M. Bossenbroek, C. L. Jerde, A. M. Kramer, E. S. Rutherford, M. A. Barnes, M. E. Wittmann, W. L. Chadderton, J. L. Apriesnig, D. Beletsky, R. M. Cooke, J. M. Drake, S. P. Egan, D. C. Finnoff, C. A. Gantz, E. K. Grey, M. H. Hoff, J. G. Howeth, R. A. Jensen, E. R. Larson, N. E. Mandrak, D. M. Mason, F. A. Martinez, T. J. Newcomb, J. D. Rothlisberger, A. J. Tucker, T. W. Warziniack, and H. Zhang, “Risk Analysis and Bioeconomics of Invasive Species to Inform Policy and Management,” Annu. Rev. Environ. Resour. 41(1), 453–488 (2016).
[Crossref]

Aronson, J.

D. Simberloff, J. L. Martin, P. Genovesi, V. Maris, D. A. Wardle, J. Aronson, F. Courchamp, B. Galil, E. García-Berthou, M. Pascal, P. Pyšek, R. Sousa, E. Tabacchi, and M. Vilà, “Impacts of biological invasions: what’s what and the way forward,” Trends Ecol. Evol. (Amst.) 28(1), 58–66 (2013).
[Crossref] [PubMed]

Bag, S.

S. J. Schambach, S. Bag, L. Schilling, C. Groden, and M. A. Brockmann, “Application of micro-CT in small animal imaging,” Methods 50(1), 2–13 (2010).
[Crossref] [PubMed]

Bai, M.

L. Xing, R. C. McKellar, M. Wang, M. Bai, J. K. O’Connor, M. J. Benton, J. Zhang, Y. Wang, K. Tseng, M. G. Lockley, G. Li, W. Zhang, and X. Xu, “Mummified precocial bird wings in mid-Cretaceous Burmese amber,” Nat. Commun. 7(1), 12089 (2016).
[Crossref] [PubMed]

Barnes, M. A.

D. M. Lodge, P. W. Simonin, S. W. Burgiel, R. P. Keller, J. M. Bossenbroek, C. L. Jerde, A. M. Kramer, E. S. Rutherford, M. A. Barnes, M. E. Wittmann, W. L. Chadderton, J. L. Apriesnig, D. Beletsky, R. M. Cooke, J. M. Drake, S. P. Egan, D. C. Finnoff, C. A. Gantz, E. K. Grey, M. H. Hoff, J. G. Howeth, R. A. Jensen, E. R. Larson, N. E. Mandrak, D. M. Mason, F. A. Martinez, T. J. Newcomb, J. D. Rothlisberger, A. J. Tucker, T. W. Warziniack, and H. Zhang, “Risk Analysis and Bioeconomics of Invasive Species to Inform Policy and Management,” Annu. Rev. Environ. Resour. 41(1), 453–488 (2016).
[Crossref]

Bartkowski, B.

B. Bartkowski, N. Lienhoop, and B. Hansjürgens, “Capturing the complexity of biodiversity: A critical review of economic valuation studies of biological diversity,” Ecol. Econ. 113, 1–14 (2015).
[Crossref]

Beletsky, D.

D. M. Lodge, P. W. Simonin, S. W. Burgiel, R. P. Keller, J. M. Bossenbroek, C. L. Jerde, A. M. Kramer, E. S. Rutherford, M. A. Barnes, M. E. Wittmann, W. L. Chadderton, J. L. Apriesnig, D. Beletsky, R. M. Cooke, J. M. Drake, S. P. Egan, D. C. Finnoff, C. A. Gantz, E. K. Grey, M. H. Hoff, J. G. Howeth, R. A. Jensen, E. R. Larson, N. E. Mandrak, D. M. Mason, F. A. Martinez, T. J. Newcomb, J. D. Rothlisberger, A. J. Tucker, T. W. Warziniack, and H. Zhang, “Risk Analysis and Bioeconomics of Invasive Species to Inform Policy and Management,” Annu. Rev. Environ. Resour. 41(1), 453–488 (2016).
[Crossref]

Benton, M. J.

L. Xing, R. C. McKellar, M. Wang, M. Bai, J. K. O’Connor, M. J. Benton, J. Zhang, Y. Wang, K. Tseng, M. G. Lockley, G. Li, W. Zhang, and X. Xu, “Mummified precocial bird wings in mid-Cretaceous Burmese amber,” Nat. Commun. 7(1), 12089 (2016).
[Crossref] [PubMed]

Bianco, P. R.

X. Zhou, M. Lei, D. Dan, B. Yao, Y. Yang, J. Qian, G. Chen, and P. R. Bianco, “Image recombination transform algorithm for superresolution structured illumination microscopy,” J. Biomed. Opt. 21(9), 96009 (2016).
[Crossref] [PubMed]

Biró, L. P.

J. P. Vigneron, J. M. Pasteels, D. M. Windsor, Z. Vértesy, M. Rassart, T. Seldrum, J. Dumont, O. Deparis, V. Lousse, L. P. Biró, D. Ertz, and V. Welch, “Switchable reflector in the Panamanian tortoise beetle Charidotella egregia (Chrysomelidae: Cassidinae),” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 76(3 Pt 1), 031907 (2007).
[Crossref] [PubMed]

Bossenbroek, J. M.

D. M. Lodge, P. W. Simonin, S. W. Burgiel, R. P. Keller, J. M. Bossenbroek, C. L. Jerde, A. M. Kramer, E. S. Rutherford, M. A. Barnes, M. E. Wittmann, W. L. Chadderton, J. L. Apriesnig, D. Beletsky, R. M. Cooke, J. M. Drake, S. P. Egan, D. C. Finnoff, C. A. Gantz, E. K. Grey, M. H. Hoff, J. G. Howeth, R. A. Jensen, E. R. Larson, N. E. Mandrak, D. M. Mason, F. A. Martinez, T. J. Newcomb, J. D. Rothlisberger, A. J. Tucker, T. W. Warziniack, and H. Zhang, “Risk Analysis and Bioeconomics of Invasive Species to Inform Policy and Management,” Annu. Rev. Environ. Resour. 41(1), 453–488 (2016).
[Crossref]

Bradski, G.

E. Rublee, V. Rabaud, K. Konolige, and G. Bradski, “ORB: an efficient alternative to SIFT or SURF,” in IEEE International Conference on Computer Vision (2011), pp. 2564–2571.
[Crossref]

Brockmann, M. A.

S. J. Schambach, S. Bag, L. Schilling, C. Groden, and M. A. Brockmann, “Application of micro-CT in small animal imaging,” Methods 50(1), 2–13 (2010).
[Crossref] [PubMed]

Burgiel, S. W.

D. M. Lodge, P. W. Simonin, S. W. Burgiel, R. P. Keller, J. M. Bossenbroek, C. L. Jerde, A. M. Kramer, E. S. Rutherford, M. A. Barnes, M. E. Wittmann, W. L. Chadderton, J. L. Apriesnig, D. Beletsky, R. M. Cooke, J. M. Drake, S. P. Egan, D. C. Finnoff, C. A. Gantz, E. K. Grey, M. H. Hoff, J. G. Howeth, R. A. Jensen, E. R. Larson, N. E. Mandrak, D. M. Mason, F. A. Martinez, T. J. Newcomb, J. D. Rothlisberger, A. J. Tucker, T. W. Warziniack, and H. Zhang, “Risk Analysis and Bioeconomics of Invasive Species to Inform Policy and Management,” Annu. Rev. Environ. Resour. 41(1), 453–488 (2016).
[Crossref]

Cai, Y.

Chadderton, W. L.

D. M. Lodge, P. W. Simonin, S. W. Burgiel, R. P. Keller, J. M. Bossenbroek, C. L. Jerde, A. M. Kramer, E. S. Rutherford, M. A. Barnes, M. E. Wittmann, W. L. Chadderton, J. L. Apriesnig, D. Beletsky, R. M. Cooke, J. M. Drake, S. P. Egan, D. C. Finnoff, C. A. Gantz, E. K. Grey, M. H. Hoff, J. G. Howeth, R. A. Jensen, E. R. Larson, N. E. Mandrak, D. M. Mason, F. A. Martinez, T. J. Newcomb, J. D. Rothlisberger, A. J. Tucker, T. W. Warziniack, and H. Zhang, “Risk Analysis and Bioeconomics of Invasive Species to Inform Policy and Management,” Annu. Rev. Environ. Resour. 41(1), 453–488 (2016).
[Crossref]

Chen, G.

X. Zhou, M. Lei, D. Dan, B. Yao, Y. Yang, J. Qian, G. Chen, and P. R. Bianco, “Image recombination transform algorithm for superresolution structured illumination microscopy,” J. Biomed. Opt. 21(9), 96009 (2016).
[Crossref] [PubMed]

Conchello, J. A.

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D. M. Lodge, P. W. Simonin, S. W. Burgiel, R. P. Keller, J. M. Bossenbroek, C. L. Jerde, A. M. Kramer, E. S. Rutherford, M. A. Barnes, M. E. Wittmann, W. L. Chadderton, J. L. Apriesnig, D. Beletsky, R. M. Cooke, J. M. Drake, S. P. Egan, D. C. Finnoff, C. A. Gantz, E. K. Grey, M. H. Hoff, J. G. Howeth, R. A. Jensen, E. R. Larson, N. E. Mandrak, D. M. Mason, F. A. Martinez, T. J. Newcomb, J. D. Rothlisberger, A. J. Tucker, T. W. Warziniack, and H. Zhang, “Risk Analysis and Bioeconomics of Invasive Species to Inform Policy and Management,” Annu. Rev. Environ. Resour. 41(1), 453–488 (2016).
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Wilson, T.

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D. M. Lodge, P. W. Simonin, S. W. Burgiel, R. P. Keller, J. M. Bossenbroek, C. L. Jerde, A. M. Kramer, E. S. Rutherford, M. A. Barnes, M. E. Wittmann, W. L. Chadderton, J. L. Apriesnig, D. Beletsky, R. M. Cooke, J. M. Drake, S. P. Egan, D. C. Finnoff, C. A. Gantz, E. K. Grey, M. H. Hoff, J. G. Howeth, R. A. Jensen, E. R. Larson, N. E. Mandrak, D. M. Mason, F. A. Martinez, T. J. Newcomb, J. D. Rothlisberger, A. J. Tucker, T. W. Warziniack, and H. Zhang, “Risk Analysis and Bioeconomics of Invasive Species to Inform Policy and Management,” Annu. Rev. Environ. Resour. 41(1), 453–488 (2016).
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Supplementary Material (8)

NameDescription
» Visualization 1       3D imaging result related to Fig. 3(a)
» Visualization 2       3D imaging result related to Fig. 3(b)
» Visualization 3       3D imaging result related to Fig. 3(c)
» Visualization 4       3D imaging result related to Fig. 4(a)
» Visualization 5       3D imaging result related to Fig. 4(e)
» Visualization 6       3D imaging result related to Fig. 5(a)
» Visualization 7       3D imaging result related to Fig. 5(d)
» Visualization 8       3D imaging result related to Fig. 6(a)

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Figures (6)

Fig. 1
Fig. 1 Schematic diagram of the C-SIM system. (a) Light path diagram. LED source: white light LED with a maximum power of 3W; DMD: maximal binary pattern rate of 32kHz at 1024 × 768 pixels with a pixel pitch of 13.8μm;Tube lens: Ф25.4mm achromatic lens with focal length of 200mm; Collimating lens: Ф50.8mm achromatic lens with focal length of 200mm. Objective lens: 4 × /NA0.2 or 20 × /NA0.45. Camera: maximum full-frame rate of 80fps at 2048 × 2048pixels. (b) Apparatus diagram. Including the LED source①, the compact microscope②, the color CMOS camera③, the motorized sample stage④, and the DMD coupling elements of TIR-prism and mirrors⑤.
Fig. 2
Fig. 2 Timing diagram of the controlling system for the hardware. The red line represents the trigger signal of DMD. The purple line represents the trigger signal of camera which is synchronized with DMD. After each exposure, when the rising edge of the green line arrives, the image is written to the PC. The blue line represents the trigger signal of stage Z, after each three images are written to the PC, the stage starts to move to next slice. The brown line represents the trigger signal of stage XY, after image collecting of one FOV, the stage starts to move to next FOV when the falling edge of the green line arrives. In this FOV, stage Z moves to the opposite direction compared to the previous FOV (see the blue line).
Fig. 3
Fig. 3 Results of maximum intensity projection images. (a) A shining leaf chafer (Mimela sp.) observed with 4 × objective. The 3D volume is rendered from 50 data sets stitching. We sliced 181 layers at 20 μm axial intervals and captured 543 raw images in 2048 × 2048 pixels for each data set. The 3D volume is about 7.6 × 13.1 × 3.6 mm3 (see Visualization 1). The data acquisition time is 570.9 seconds, that is 50 FOVs × ((11 ms exposure time + 0.031 ms DMD switching time) × 3 patterns × 181 layers + 30 ms Z-stage settling time × 180 axial slice intervals.)) + 49 FOVs × 30ms XY-stage settling time. (b) A shining leaf chafer (Anomala corrugata Bates, 1866) observed with 4 × objective and 12ms exposure time. The 3D volume is rendered from 55 data sets stitching. The 3D volume is about 7.7 × 11.5 × 3.6 mm3 (see Visualization 2). The data acquisition time is 654.3 seconds. (c) A leaf beetle (Clitenella fulminans (Faldermann, 1835)) observed with 4 × objective and 20ms exposure time. The 3D volume is rendered from 15 data sets stitching. The 3D volume is about 4.4 × 7.3 × 3.5 mm3 (see Visualization 3). The data acquisition time is 237.8 seconds. The images indicated by the red arrow in the bottom are observed with 20 × /NA 0.45objective.
Fig. 4
Fig. 4 Imaging results of two tiger beetles. (a) Maximum intensity projection image of a tiger beetle. We sliced 350 layers at 20 μm axial intervals and captured 1050 raw images for each data set (see Visualization 4). The whole image is stitched by 84 data sets (6 rows and 14 columns), and the data acquisition time is 1766.7 seconds. (b) Maximum intensity projection image of the compound eye shown in (a) in the red rectangular box, the SIM image is observed with 20 × /NA 0.45 objective at 200nm axial intervals. (c) The 3D height map. (d) The profile along the blue line-scan (Fig. 4(c)). (e) Maximum intensity projection image of another tiger beetle. The whole image is stitched by 65 data sets (5 rows and 13 columns) and 990 raw images for each data set are captured (see Visualization 5). The data acquisition time is 1288.9 seconds. (f) Maximum intensity projection image of the compound eye shown in (e) in the red rectangular box, the SIM image is observed with 20 × /NA 0.45 objective at 200nm axial intervals. (g) The 3D height map. (h) The profile along the blue line-scan (Fig. 4(g)). a-d: Cicindela chinensis DeGeer, 1774; e-h: Cosmodela separata (Fleutiaux, 1893).
Fig. 5
Fig. 5 Maximum intensity projection image of a melolonthine beetle and a monkey beetle. (a) A melolonthine beetle with white scales covered the entire body observed with 4 × objective. We sliced 333 layers at 20μm axial intervals and captured 999 raw images for each data set (see Visualization 6). The data acquisition time of the whole 3D insect is 1100 seconds with 10ms single exposure time. (b) shows much more details and colors of the insect which are observed with 20 × objective at 200nm axial intervals. (c) is the extracted 3D morphological height map of this white scale covering back. (d) A monkey beetle with golden heart shaped scales covered in the back observed with 4 × objective. 494 raw images with 148 layers at 20μm axial intervals are captured for each data set (see Visualization 7). The data acquisition time of the whole 3D insect is 323.5 seconds. (e) shows rough surfaces and more colors of these scales which are observed with 20 × objective at 200nm axial intervals. (f) is the extracted 3D morphological height map of the scales. a-c: Cyphochilus sp.; d-f: Ectinohoplia auriventris Moser, 1915.
Fig. 6
Fig. 6 Imaging results of a shining leaf chafer. (a) A shining leaf chafer observed with 4 × objective. (Mimela sp.). The back in the left and the abdomen in the right. The 3D volume is rendered from 60 data sets stitching (see Visualization 8). The whole FOV is 9.7 × 13.1 × 4.0 mm3. (b) Maximum intensity projec-tion image of the hair shown in A in the red rectangular box, the SIM image is observed with 20 × /NA 0.45 objective at 200nm axial intervals. (c) 3D height map.

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