Insect monitoring with fluorescence lidar techniques: field experiments

doi:10.1364/AO.49.005133

Insect monitoring with fluorescence lidar techniques: field experiments

Zuguang Guan, Mikkel Brydegaard, Patrik Lundin, Maren Wellenreuther, Anna Runemark, Erik I. Svensson, and Sune Svanberg »View Author Affiliations

Applied Optics, Vol. 49, Issue 27, pp. 5133-5142 (2010)
http://dx.doi.org/10.1364/AO.49.005133

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Abstract

Results from field experiments using a fluorescence lidar system to monitor movements of insects are reported. Measurements over a river surface were made at distances between 100 and $300 m$ , detecting, in particular, damselflies entering the $355 nm$ pulsed laser beam. The lidar system recorded the depolarized elastic backscattering and two broad bands of laser-induced fluorescence, with the separation wavelength at $500 nm$ . Captured species, dusted with characteristic fluorescent dye powders, could be followed spatially and temporally after release. Implications for ecological research are discussed.

OCIS Codes
(280.3640) Remote sensing and sensors : Lidar
(300.2530) Spectroscopy : Fluorescence, laser-induced

ToC Category:
Remote Sensing and Sensors

History
Original Manuscript: June 9, 2010
Manuscript Accepted: July 20, 2010
Published: September 16, 2010

Virtual Issues
Vol. 5, Iss. 14 Virtual Journal for Biomedical Optics
September 15, 2010 Spotlight on Optics

Citation
Zuguang Guan, Mikkel Brydegaard, Patrik Lundin, Maren Wellenreuther, Anna Runemark, Erik I. Svensson, and Sune Svanberg, "Insect monitoring with fluorescence lidar techniques: field experiments," Appl. Opt. 49, 5133-5142 (2010)
http://www.opticsinfobase.org/vjbo/abstract.cfm?URI=ao-49-27-5133

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References

R. M. Measures, Laser Remote Sensing: Fundamentals and Applications (Wiley, 1984).
S. Svanberg, “LIDAR,” in Springer Handbook of Lasers and Optics, F.Träger, ed. (Springer, 2007), pp. 1031–1052.
X. Chu and G. C. Papen, “Resonance fluorescence lidar,” in Laser Remote SensingT.Fujii and T.Fukuchi, eds. (CRC, 2005), Chap. 5, pp. 179–432. [CrossRef]
S. Svanberg, “Fluorescence spectroscopy and imaging of lidar targets,” in Laser Remote SensingT.Fujii and T.Fukuchi, eds. (CRC, 2005), Chap. 6, pp. 433–468,. [CrossRef]
P. Weibring, H. Edner, and S. Svanberg, “Versatile mobile lidar system for environmental monitoring,” Appl. Opt. 42, 3583–3594 (2003). [CrossRef] [PubMed]
L. Palombi, D. Lognoli, V. Raimondi, G. Cecchi, J. Hällström, K. Barup, C. Conti, R. Grönlund, A. Johansson, and S. Svanberg, “Hyperspectral fluorescence lidar imaging at the Colosseum, Rome: elucidating past conservation interventions,” Opt. Express 16, 6794–680 (2008). [CrossRef] [PubMed]
M. Campero, F. Ollevier, and R. Stoks, “Ecological relevance and sensitivity depending on the exposure time for two biomarkers,” Environ. Toxicol. 22, 572–581 (2007). [CrossRef] [PubMed]
R. Hickling, D. B. Roy, J. K. Hill, and C. D. Thomas, “A northward shift of range margins in British odonata,” Glob. Change Biol. 11, 502–506 (2005). [CrossRef]
T. J. Case and M. L. Taper, “Interspecific competition, environmental gradients, gene flow, and the coevolution of species borders,” Am. Nat. 155, 583–605 (2000). [CrossRef] [PubMed]
M. Joron and P. M. Brakefield, “Captivity masks inbreeding effects on male mating success in butterflies,” Nature 424, 191–194 (2003). [CrossRef] [PubMed]
J. A. Shaw, N. L. Seldomridge, D. L. Dunkle, P. W. Nugent, L. H. Spangler, J. J. Bromenshank, C. B. Henderson, J. H. Churnside, and J. J. Wilson, “Polarization lidar measurements of honey bees in flight for locating land mines,” Opt. Express 13, 5853–5863 (2005). [CrossRef] [PubMed]
K. S. Repasky, J. A. Shaw, R. Scheppele, C. Melton, J. L. Carsten, and L. H. Spangler, “Optical detection of honeybees by use of wing-beat modulation of scattered laser light for locating explosives and land mines,” Appl. Opt. 45, 1839–1843(2006). [CrossRef] [PubMed]
D. S. Hoffman, A. R. Nehrir, K. S. Repasky, J. A. Shaw, and J. L. Carlsten, “Range-resolved optical detection of honeybees by use of wing-beat modulation of scattered light for locating land mines,” Appl. Opt. 46, 3007–3012 (2007). [CrossRef] [PubMed]
M. Brydegaard, Z. G. Guan, M. Wellenreuther, and S. Svanberg, “Insect monitoring with fluorescence lidar techniques: feasibility study,” Appl. Opt. 48, 5668–5677 (2009). [CrossRef] [PubMed]
C. af Klinteberg, M. Andreasson, O. Sandström, S. Andersson-Engels, and S. Svanberg, “Compact medical fluorosensor for minimally invasive tissue characterization,” Rev. Sci. Instrum. 76, 034303 (2005). [CrossRef]
P. S. Corbet, Dragonflies: Behavior and Ecology of Odonata Essex (Harley, 1999).
E. Anderson, Z. Bai, C. Bischof, S. Blackford, J. Demmel, J. Dongarra, J. Du Croz, A. Greenbaum, S. Hammarling, A. McKenney, and D. Sorensen, LAPACK User’s Guide, 3rd ed. (Society for Industrial and Applied Mathematics, 1999). [CrossRef]
R. Johansson, System Modeling and Identification (Prentice Hall, 1993).
E. M. C. Hillman and A. Moore, “All-optical anatomical co-registration for molecular imaging of small animals using dynamic contrast,” Nat. Photon. 1, 526–530 (2007). [CrossRef]
R. B. Bradbury, R. A. Hill, D. C. Mason, S. A. Hinsley, J. D. Wilson, H. Balzter, G. Q. A. Anderson, M. J. Wittingham, I. J. Davenport, and P. E. Bellamy, “Modeling relationships between birds and vegetation structure using airborne lidar data: a review with case studies from agricultural and woodland environments,” Ibis 147, 443–452 (2005). [CrossRef]
K. T. Vierling, L. A. Vierling, W. A. Gould, S. Martinuzzi, and R. M. Clawges, “Lidar: Shedding new light on habitat characterization and modeling,” Front. Ecol. Environ. 6, 90–98 (2008). [CrossRef]
C. N. Parmesan, “Climate and species’ range,” Nature 382, 765–766 (1996). [CrossRef]
C. N. Parmesan, C. Ryrholm, C. Steganescu, J. K. Hill, C. D. Thomas, B. Descimon, B. Huntley, L. Kaila, J. Kullberg, T. Tammaru, W. J. Tennent, J. A. Thomas, and M. Warren, “Poleward shifts in geographical ranges of butterfly species associated with regional warming,” Nature 399, 579–583 (1999). [CrossRef]
K. Tynkkynen, M. J. Rantala, and J. Suhonen, “Interspecific aggression and character displacement in the damselfly Calopteryx splendens,” J. Evol. Biol. 17, 759–767 (2004). [CrossRef] [PubMed]
K. Tynkkynen, J. S. Kotiaho, M. Luojumäki, and J. Suhonen, “Interspecific aggression causes negative selection on sexual characters,” Evolution 59, 1838–1843 (2005). [PubMed]
K. Tynkkynen, J. S. Kotiaho, M. Luojumäki, and J. Suhonen, “Interspecific territoriality in Calopteryx damselflies: the role of secondary sexual characters,” Anim. Behav. 71, 299–306(2006). [CrossRef]
G. Rüppel, D. Hilfert-Rüppel, G. Rehfeldt, and C. Schütte, Die Prachtlibellen Europas (Westarp Wissenschaften, 2005).
A. Cordero, “Forced copulations and female contact guarding at a high male density in a Calopterygid damselfly,” J. Insect Behav. 12, 27–37 (1999). [CrossRef]
A. Chaput-Bardy, A. Gregoire, M. Baguette, A. Pagano, and J. Secondi, “Condition and phenotype-dependent dispersal in a damselfly, Calopteryx splendens,” PLoS ONE 5, e10694(2010). [CrossRef] [PubMed]
K. F. Conrad, K. H. Willson, K. Whitfield, I. F. Harvey, C. J. Thomas, and T. N. Sherrat, “Characteristics of dispersing Ischnura elegans and Coenagrion puella (odonata): age, sex, size morph and ectoparasitism,” Ecography 25, 439–445(2002). [CrossRef]
L. Ward and P. J. Mill, “Habitat factors influencing the presence of adult Calopteryx splendens (odonata: Zygoptera),” Euro. J. Entomol. 102, 47–51 (2005).
D. W. Gibbons and D. Pain, “The influence of river flow rate on the breeding behaviour of calopteryx damselflies,” J. Anim. Ecol. 61, 283–289 (1992). [CrossRef]
F. S. Chapin, E. S. Zavaleta, V. T. Eviner, R. L. Naylor, P. M. Vitousek, H. L. Reynolds, D. U. Hooper, S. Lavore, O. E. SalaI, S. E. Hobbie, M. C. Mack, and S. Díaz, “Consequences of changing biodiversity,” Nature 405, 234–242 (2000). [CrossRef] [PubMed]
P. M. Hammond, “Species inventory,” in Global Diversity Status of the Earth Living Resources, B.Groombridge, ed. (Chapman and Hall, 1992), pp. 17–39.
J. A. Thomas, M. G. Telfer, D. B. Roy, C. D. Preston, J. J. D. Greenwood, J. Asher, R. Fox, R. T. Clarke, and J. H. Lawton, “Comparative losses of British butterflies, birds, and plants and the global extinction crisis,” Science 303, 1879–1881 (2004). [CrossRef] [PubMed]

Am. Nat.

T. J. Case and M. L. Taper, “Interspecific competition, environmental gradients, gene flow, and the coevolution of species borders,” Am. Nat. 155, 583–605 (2000). [CrossRef] [PubMed]

Anim. Behav.

K. Tynkkynen, J. S. Kotiaho, M. Luojumäki, and J. Suhonen, “Interspecific territoriality in Calopteryx damselflies: the role of secondary sexual characters,” Anim. Behav. 71, 299–306(2006). [CrossRef]

Appl. Opt.

Ecography

K. F. Conrad, K. H. Willson, K. Whitfield, I. F. Harvey, C. J. Thomas, and T. N. Sherrat, “Characteristics of dispersing Ischnura elegans and Coenagrion puella (odonata): age, sex, size morph and ectoparasitism,” Ecography 25, 439–445(2002). [CrossRef]

Environ. Toxicol.

M. Campero, F. Ollevier, and R. Stoks, “Ecological relevance and sensitivity depending on the exposure time for two biomarkers,” Environ. Toxicol. 22, 572–581 (2007). [CrossRef] [PubMed]

Euro. J. Entomol.

L. Ward and P. J. Mill, “Habitat factors influencing the presence of adult Calopteryx splendens (odonata: Zygoptera),” Euro. J. Entomol. 102, 47–51 (2005).

Evolution

K. Tynkkynen, J. S. Kotiaho, M. Luojumäki, and J. Suhonen, “Interspecific aggression causes negative selection on sexual characters,” Evolution 59, 1838–1843 (2005). [PubMed]

Front. Ecol. Environ.

K. T. Vierling, L. A. Vierling, W. A. Gould, S. Martinuzzi, and R. M. Clawges, “Lidar: Shedding new light on habitat characterization and modeling,” Front. Ecol. Environ. 6, 90–98 (2008). [CrossRef]

Glob. Change Biol.

R. Hickling, D. B. Roy, J. K. Hill, and C. D. Thomas, “A northward shift of range margins in British odonata,” Glob. Change Biol. 11, 502–506 (2005). [CrossRef]

Ibis

R. B. Bradbury, R. A. Hill, D. C. Mason, S. A. Hinsley, J. D. Wilson, H. Balzter, G. Q. A. Anderson, M. J. Wittingham, I. J. Davenport, and P. E. Bellamy, “Modeling relationships between birds and vegetation structure using airborne lidar data: a review with case studies from agricultural and woodland environments,” Ibis 147, 443–452 (2005). [CrossRef]

J. Anim. Ecol.

D. W. Gibbons and D. Pain, “The influence of river flow rate on the breeding behaviour of calopteryx damselflies,” J. Anim. Ecol. 61, 283–289 (1992). [CrossRef]

J. Evol. Biol.

K. Tynkkynen, M. J. Rantala, and J. Suhonen, “Interspecific aggression and character displacement in the damselfly Calopteryx splendens,” J. Evol. Biol. 17, 759–767 (2004). [CrossRef] [PubMed]

J. Insect Behav.

A. Cordero, “Forced copulations and female contact guarding at a high male density in a Calopterygid damselfly,” J. Insect Behav. 12, 27–37 (1999). [CrossRef]

Nat. Photon.

E. M. C. Hillman and A. Moore, “All-optical anatomical co-registration for molecular imaging of small animals using dynamic contrast,” Nat. Photon. 1, 526–530 (2007). [CrossRef]

Nature

M. Joron and P. M. Brakefield, “Captivity masks inbreeding effects on male mating success in butterflies,” Nature 424, 191–194 (2003). [CrossRef] [PubMed]
C. N. Parmesan, “Climate and species’ range,” Nature 382, 765–766 (1996). [CrossRef]
C. N. Parmesan, C. Ryrholm, C. Steganescu, J. K. Hill, C. D. Thomas, B. Descimon, B. Huntley, L. Kaila, J. Kullberg, T. Tammaru, W. J. Tennent, J. A. Thomas, and M. Warren, “Poleward shifts in geographical ranges of butterfly species associated with regional warming,” Nature 399, 579–583 (1999). [CrossRef]
F. S. Chapin, E. S. Zavaleta, V. T. Eviner, R. L. Naylor, P. M. Vitousek, H. L. Reynolds, D. U. Hooper, S. Lavore, O. E. SalaI, S. E. Hobbie, M. C. Mack, and S. Díaz, “Consequences of changing biodiversity,” Nature 405, 234–242 (2000). [CrossRef] [PubMed]

Opt. Express

PLoS ONE

A. Chaput-Bardy, A. Gregoire, M. Baguette, A. Pagano, and J. Secondi, “Condition and phenotype-dependent dispersal in a damselfly, Calopteryx splendens,” PLoS ONE 5, e10694(2010). [CrossRef] [PubMed]

Rev. Sci. Instrum.

C. af Klinteberg, M. Andreasson, O. Sandström, S. Andersson-Engels, and S. Svanberg, “Compact medical fluorosensor for minimally invasive tissue characterization,” Rev. Sci. Instrum. 76, 034303 (2005). [CrossRef]

Science

J. A. Thomas, M. G. Telfer, D. B. Roy, C. D. Preston, J. J. D. Greenwood, J. Asher, R. Fox, R. T. Clarke, and J. H. Lawton, “Comparative losses of British butterflies, birds, and plants and the global extinction crisis,” Science 303, 1879–1881 (2004). [CrossRef] [PubMed]

Other

P. M. Hammond, “Species inventory,” in Global Diversity Status of the Earth Living Resources, B.Groombridge, ed. (Chapman and Hall, 1992), pp. 17–39.
G. Rüppel, D. Hilfert-Rüppel, G. Rehfeldt, and C. Schütte, Die Prachtlibellen Europas (Westarp Wissenschaften, 2005).
P. S. Corbet, Dragonflies: Behavior and Ecology of Odonata Essex (Harley, 1999).
E. Anderson, Z. Bai, C. Bischof, S. Blackford, J. Demmel, J. Dongarra, J. Du Croz, A. Greenbaum, S. Hammarling, A. McKenney, and D. Sorensen, LAPACK User’s Guide, 3rd ed. (Society for Industrial and Applied Mathematics, 1999). [CrossRef]
R. Johansson, System Modeling and Identification (Prentice Hall, 1993).
R. M. Measures, Laser Remote Sensing: Fundamentals and Applications (Wiley, 1984).
S. Svanberg, “LIDAR,” in Springer Handbook of Lasers and Optics, F.Träger, ed. (Springer, 2007), pp. 1031–1052.
X. Chu and G. C. Papen, “Resonance fluorescence lidar,” in Laser Remote SensingT.Fujii and T.Fukuchi, eds. (CRC, 2005), Chap. 5, pp. 179–432. [CrossRef]
S. Svanberg, “Fluorescence spectroscopy and imaging of lidar targets,” in Laser Remote SensingT.Fujii and T.Fukuchi, eds. (CRC, 2005), Chap. 6, pp. 433–468,. [CrossRef]

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[1] R. M. Measures, Laser Remote Sensing: Fundamentals and Applications (Wiley, 1984).

[2] S. Svanberg, “LIDAR,” in Springer Handbook of Lasers and Optics, F.Träger, ed. (Springer, 2007), pp. 1031–1052.

[3] X. Chu and G. C. Papen, “Resonance fluorescence lidar,” in Laser Remote SensingT.Fujii and T.Fukuchi, eds. (CRC, 2005), Chap. 5, pp. 179–432. [CrossRef]

[4] S. Svanberg, “Fluorescence spectroscopy and imaging of lidar targets,” in Laser Remote SensingT.Fujii and T.Fukuchi, eds. (CRC, 2005), Chap. 6, pp. 433–468,. [CrossRef]

[5] P. Weibring, H. Edner, and S. Svanberg, “Versatile mobile lidar system for environmental monitoring,” Appl. Opt. 42, 3583–3594 (2003). [CrossRef] [PubMed]

[6] L. Palombi, D. Lognoli, V. Raimondi, G. Cecchi, J. Hällström, K. Barup, C. Conti, R. Grönlund, A. Johansson, and S. Svanberg, “Hyperspectral fluorescence lidar imaging at the Colosseum, Rome: elucidating past conservation interventions,” Opt. Express 16, 6794–680 (2008). [CrossRef] [PubMed]

[7] M. Campero, F. Ollevier, and R. Stoks, “Ecological relevance and sensitivity depending on the exposure time for two biomarkers,” Environ. Toxicol. 22, 572–581 (2007). [CrossRef] [PubMed]

[8] R. Hickling, D. B. Roy, J. K. Hill, and C. D. Thomas, “A northward shift of range margins in British odonata,” Glob. Change Biol. 11, 502–506 (2005). [CrossRef]

[9] T. J. Case and M. L. Taper, “Interspecific competition, environmental gradients, gene flow, and the coevolution of species borders,” Am. Nat. 155, 583–605 (2000). [CrossRef] [PubMed]

[10] M. Joron and P. M. Brakefield, “Captivity masks inbreeding effects on male mating success in butterflies,” Nature 424, 191–194 (2003). [CrossRef] [PubMed]

[11] J. A. Shaw, N. L. Seldomridge, D. L. Dunkle, P. W. Nugent, L. H. Spangler, J. J. Bromenshank, C. B. Henderson, J. H. Churnside, and J. J. Wilson, “Polarization lidar measurements of honey bees in flight for locating land mines,” Opt. Express 13, 5853–5863 (2005). [CrossRef] [PubMed]

[12] K. S. Repasky, J. A. Shaw, R. Scheppele, C. Melton, J. L. Carsten, and L. H. Spangler, “Optical detection of honeybees by use of wing-beat modulation of scattered laser light for locating explosives and land mines,” Appl. Opt. 45, 1839–1843(2006). [CrossRef] [PubMed]

[13] D. S. Hoffman, A. R. Nehrir, K. S. Repasky, J. A. Shaw, and J. L. Carlsten, “Range-resolved optical detection of honeybees by use of wing-beat modulation of scattered light for locating land mines,” Appl. Opt. 46, 3007–3012 (2007). [CrossRef] [PubMed]

[14] M. Brydegaard, Z. G. Guan, M. Wellenreuther, and S. Svanberg, “Insect monitoring with fluorescence lidar techniques: feasibility study,” Appl. Opt. 48, 5668–5677 (2009). [CrossRef] [PubMed]

[15] C. af Klinteberg, M. Andreasson, O. Sandström, S. Andersson-Engels, and S. Svanberg, “Compact medical fluorosensor for minimally invasive tissue characterization,” Rev. Sci. Instrum. 76, 034303 (2005). [CrossRef]

[16] P. S. Corbet, Dragonflies: Behavior and Ecology of Odonata Essex (Harley, 1999).

[17] E. Anderson, Z. Bai, C. Bischof, S. Blackford, J. Demmel, J. Dongarra, J. Du Croz, A. Greenbaum, S. Hammarling, A. McKenney, and D. Sorensen, LAPACK User’s Guide, 3rd ed. (Society for Industrial and Applied Mathematics, 1999). [CrossRef]

[18] R. Johansson, System Modeling and Identification (Prentice Hall, 1993).

[19] E. M. C. Hillman and A. Moore, “All-optical anatomical co-registration for molecular imaging of small animals using dynamic contrast,” Nat. Photon. 1, 526–530 (2007). [CrossRef]

[20] R. B. Bradbury, R. A. Hill, D. C. Mason, S. A. Hinsley, J. D. Wilson, H. Balzter, G. Q. A. Anderson, M. J. Wittingham, I. J. Davenport, and P. E. Bellamy, “Modeling relationships between birds and vegetation structure using airborne lidar data: a review with case studies from agricultural and woodland environments,” Ibis 147, 443–452 (2005). [CrossRef]

[21] K. T. Vierling, L. A. Vierling, W. A. Gould, S. Martinuzzi, and R. M. Clawges, “Lidar: Shedding new light on habitat characterization and modeling,” Front. Ecol. Environ. 6, 90–98 (2008). [CrossRef]

[22] C. N. Parmesan, “Climate and species’ range,” Nature 382, 765–766 (1996). [CrossRef]

[23] C. N. Parmesan, C. Ryrholm, C. Steganescu, J. K. Hill, C. D. Thomas, B. Descimon, B. Huntley, L. Kaila, J. Kullberg, T. Tammaru, W. J. Tennent, J. A. Thomas, and M. Warren, “Poleward shifts in geographical ranges of butterfly species associated with regional warming,” Nature 399, 579–583 (1999). [CrossRef]

[24] K. Tynkkynen, M. J. Rantala, and J. Suhonen, “Interspecific aggression and character displacement in the damselfly Calopteryx splendens,” J. Evol. Biol. 17, 759–767 (2004). [CrossRef] [PubMed]

[25] K. Tynkkynen, J. S. Kotiaho, M. Luojumäki, and J. Suhonen, “Interspecific aggression causes negative selection on sexual characters,” Evolution 59, 1838–1843 (2005). [PubMed]

[26] K. Tynkkynen, J. S. Kotiaho, M. Luojumäki, and J. Suhonen, “Interspecific territoriality in Calopteryx damselflies: the role of secondary sexual characters,” Anim. Behav. 71, 299–306(2006). [CrossRef]

[27] G. Rüppel, D. Hilfert-Rüppel, G. Rehfeldt, and C. Schütte, Die Prachtlibellen Europas (Westarp Wissenschaften, 2005).

[28] A. Cordero, “Forced copulations and female contact guarding at a high male density in a Calopterygid damselfly,” J. Insect Behav. 12, 27–37 (1999). [CrossRef]

[29] A. Chaput-Bardy, A. Gregoire, M. Baguette, A. Pagano, and J. Secondi, “Condition and phenotype-dependent dispersal in a damselfly, Calopteryx splendens,” PLoS ONE 5, e10694(2010). [CrossRef] [PubMed]

[30] K. F. Conrad, K. H. Willson, K. Whitfield, I. F. Harvey, C. J. Thomas, and T. N. Sherrat, “Characteristics of dispersing Ischnura elegans and Coenagrion puella (odonata): age, sex, size morph and ectoparasitism,” Ecography 25, 439–445(2002). [CrossRef]

[31] L. Ward and P. J. Mill, “Habitat factors influencing the presence of adult Calopteryx splendens (odonata: Zygoptera),” Euro. J. Entomol. 102, 47–51 (2005).

[32] D. W. Gibbons and D. Pain, “The influence of river flow rate on the breeding behaviour of calopteryx damselflies,” J. Anim. Ecol. 61, 283–289 (1992). [CrossRef]

[33] F. S. Chapin, E. S. Zavaleta, V. T. Eviner, R. L. Naylor, P. M. Vitousek, H. L. Reynolds, D. U. Hooper, S. Lavore, O. E. SalaI, S. E. Hobbie, M. C. Mack, and S. Díaz, “Consequences of changing biodiversity,” Nature 405, 234–242 (2000). [CrossRef] [PubMed]

[34] P. M. Hammond, “Species inventory,” in Global Diversity Status of the Earth Living Resources, B.Groombridge, ed. (Chapman and Hall, 1992), pp. 17–39.

[35] J. A. Thomas, M. G. Telfer, D. B. Roy, C. D. Preston, J. J. D. Greenwood, J. Asher, R. Fox, R. T. Clarke, and J. H. Lawton, “Comparative losses of British butterflies, birds, and plants and the global extinction crisis,” Science 303, 1879–1881 (2004). [CrossRef] [PubMed]

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Insect monitoring with fluorescence lidar techniques: field experiments