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Colors of night: climate–morphology relationships of geometrid moths along spatial gradients in southwestern China


Color lightness of insects is an important ecological trait affecting their performance through multiple functions such as thermoregulation, UV protection and disease resistance. The geographical pattern of color lightness in diurnal insects are relatively well understood and largely driven by thermal melanism through the enhancement of insect activity. In nocturnal insects, however, the ecological function of color lightness in response to climatic factors is poorly understood, particularly at small spatial scales. In this study, we investigated color lightness of nocturnal moth assemblages along environmental gradients. Using geometrid moths collected with comparable methodologies (light trapping), we examined assemblage-level changes in color lightness across elevational gradients and vertical strata (canopy vs understory) across three climatically different locations in Yunnan, China. The results showed that moths are darker in color at higher elevations. Such patterns are most apparent in canopy assemblages. In addition, the strength of the elevational pattern on color lightness varied across location, being most pronounced in the canopy of the subalpine site. These patterns are likely driven by UV protection and/or thermoregulation. Our study highlights the importance of abiotic factors such as temperature and solar radiation in structuring morphological patterns of nocturnal ectothermic assemblages along elevational gradients of climatically harsh environments.

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  1. Abraham D, Ryrholm N, Wittzell H, Holloway JD, Scoble MJ, Löfstedt C (2001) Molecular phylogeny of the subfamilies in Geometridae (Geometroidea: Lepidoptera). Mol Phylogenet Evol 20:65–77

  2. Ashton LA, Nakamura A, Basset Y, Burwell CJ, Cao M, Eastwood R, Odell E, Oliveira EG, Hurley K, Katabuchi M, Maunsell S, McBroom J, Schmidl J, Sun Z, Tang Y, Whitaker T, Laidlaw MJ, McDonald WJF, Kitching RL (2016a) Vertical stratification of moths across elevation and latitude. J Biogeogr 43:59–69

  3. Ashton LA, Nakamura A, Burwell CJ, Tang Y, Cao M, Whitaker T, Sun Z, Huang H, Kitching RL (2016b) Elevational sensitivity in an Asian ‘hotspot’: moth diversity across elevational gradients in tropical, sub-tropical and sub-alpine China. Sci Rep 6:26513

  4. Axmacher JC, Holtmann G, Scheuermann L, Brehm G, Müller-Hohenstein K, Fiedler K (2004) Diversity of geometrid moths (Lepidoptera: Geometridae) along an Afrotropical elevational rainforest transect. Divers Distrib 10:293–302

  5. Bartholomew GA, Casey TM (1978) Oxygen consumption of moths during rest, pre-flight warm-up, and flight in relation to body size and wing morphology. J Exp Biol 76:11–25

  6. Barton K (2016) MuMIn: multi-model inference. R package version 1.15.6. Accessed 31 May 2018

  7. Bastide H, Yassin A, Johanning EJ, Pool JE (2014) Pigmentation in Drosophila melanogaster reaches its maximum in Ethiopia and correlates most strongly with ultra-violet radiation in sub-Saharan Africa. BMC Evol Biol 14:179

  8. Battisti A, Avcı M, Avtzis DN, Jamaa ML, Berardi L, Berretima W, Branco M, Chakali G, El Fels MA, Frérot B, Hódar JA, Ionescu-Mălăncuş I, İpekdal K, Larsson S, Manole T, Mendel Z, Meurisse N, Mirchev P, Nemer N, Paiva MR, Pino J, Protasov A, Rahim N, Rousselet J, Santos H, Sauvard D (2015) Natural history of the processionary moths (Thaumetopoea spp.): new insights in relation to climate change. In: Roques A (ed) Processionary moths and climate change: an update. Springer-Quae, Dordrecht, pp 15–80

  9. Beck J, McCain CM, Axmacher JC, Ashton LA, Bärtschi F, Brehm G, Choi SW, Cizek O, Colwell RK, Fiedler K, Francois CL, Highland S, Holloway JD, Intachat J, Kadlec T, Kitching RL, Maunsell SC, Merckx T, Nakamura A, Odell E, Sang W, Toko PS, Zamecnik J, Zou Y, Novotny V (2017) Elevational species richness gradients in a hyperdiverse insect taxon: a global meta-study on geometrid moths. Glob Ecol Biogeogr 26:412–424

  10. Bishop TR, Robertson MP, Gibb H, Van Rensburg BJ, Braschler B, Chown SL, Foord SH, Munyai TC, Okey I, Tshivhandekano PG, Werenkraut V, Parr CL (2016) Ant assemblages have darker and larger members in cold environments. Glob Ecol Biogeogr 25:1489–1499

  11. Blumthaler M, Ambach W, Ellinger R (1997) Increase in solar UV radiation with altitude. J Photochem Photobiol 39:130–134

  12. Boardman M, Askew RR, Cook LM (1974) Experiments on resting site selection by nocturnal moths. J Zool 172:343–355

  13. Bohlman SA, Matelson TJ, Nadkarni NM (1995) Moisture and temperature patterns of canopy humus and forest floor soil of a montane cloud forest, Costa Rica. Biotropica 27:13–19

  14. Brehm G, Homeier J, Fiedler K (2003) Beta diversity of geometrid moths (Lepidoptera: Geometridae) in an Andean montane rainforest. Divers Distrib 9:351–366

  15. Burtt EH Jr, Ichida JM (2004) Gloger’s rule, feather-degrading bacteria, and color variation among song sparrows. Condor 106:681–686

  16. Chen IC, Shiu HJ, Benedick S, Holloway JD, Chey VK, Barlow HS, Hill JK, Thomas CD (2009) Elevation increases in moth assemblages over 42 years on a tropical mountain. Proc Natl Acad Sci 106:1479–1483

  17. Cheng W, Xing S, Chen Y, Lin R, Bonebrake TC, Nakamura A (2018) Dark butterflies camouflaged from predation in dark tropical forest understories. Ecol Entomol.

  18. Church NS (1960) Heat loss and body temperature of flying insects. II. Heat conduction within the body and its loss by radiation and convection. J Exp Biol 37:186–312

  19. Clusella-Trullas S, van Wyk JH, Spotila JR (2007) Thermal melanism in ectotherms. J Therm Biol 32:235–245

  20. Clusella-Trullas S, Terblanche JS, Blackburn TM, Chown SL (2008) Testing the thermal melanism hypothesis: a macrophysiological approach. Funct Ecol 22:232–238

  21. Dalrymple RL, Flores-Moreno H, Kemp DJ, White TE, Laffan SW, Hemmings FA, Hitchcock TD, Moles AT (2017) Abiotic and biotic predictors of macroecological patterns in bird and butterfly coloration. Ecol Monogr 88:204–224

  22. Dillon ME, Frazier MR, Dudley R (2006) Into thin air: physiology and evolution of alpine insects. Integr Comp Biol 46:49–61

  23. Ellers J, Boggs CL (2002) The evolution of wing color in Colias butterflies: heritability, sex linkage, and population divergence. Evolution 56:836–840

  24. Ellers J, Boggs CL (2004) Functional ecological implications of intraspecific differences in wing melanization in Colias butterflies. Biol J Linn Soc 82:79–87

  25. Endler JA (1993) The color of light in forests and its implications. Ecol Monogr 63:1–27

  26. Goulson D (1994) Determination of larval melanization in the moth, Mamestra brassicae, and the role of melanin in thermoregulation. Heredity 73:471–479

  27. Gunn A (1998) The determination of larval phase coloration in the African armyworm, Spodoptera exempta and its consequences for thermoregulation and protection from UV light. Entomol Exp Appl 86:125–133

  28. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162

  29. Heath JE, Adams PA (1967) Regulation of heat production by large moths. J Exp Biol 47:21–33

  30. Heidrich L, Friess N, Fiedler K, Brändle M, Hausmann A, Brandl R, Zeuss D (2018) The dark side of Lepidoptera: colour lightness of geometrid moths decreases with increasing latitude. Glob Ecol Biogeogr.

  31. Heinrich B (1987) Thermoregulation by winter-flying endothermic moths. J Exp Biol 127:313–332

  32. Hodkinson ID (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev 80:489–513

  33. Jankowski JE, Londoño GA, Robinson SK, Chappell MA (2013) Exploring the role of physiology and biotic interactions in determining elevational ranges of tropical animals. Ecography 36:1–12

  34. Kawahara AY, Plotkin D, Hamilton CA, Gough H, St Laurent R, Owens HL, Homziak NT, Barber JR (2018) Diel behavior in moths and butterflies: a synthesis of data illuminates the evolution of temporal activity. Org Divers Evol 18:13–27

  35. Kingsolver JG (1983) Thermoregulation and flight in Colias butterflies: elevational patterns and mechanistic limitations. Ecology 64:534–545

  36. Kingsolver JG (1985) Thermoregulatory significance of wing melanization in Pieris butterflies (Lepidoptera: Pieridae): physics, posture, and pattern. Oecologia 66:546–553

  37. Kingsolver JG (1995) Viability selection on seasonally polyphenic traits: wing melanin pattern in western white butterflies. Evolution 49:932–941

  38. Kitching RL (1977) Time resources and population dynamics in insects. Austral Ecol 2:31–42

  39. Krams I, Burghardt GM, Krams R, Trakimas G, Kaasik A, Luoto S, Rantala MJ, Krama T (2016) A dark cuticle allows higher investment in immunity, longevity and fecundity in a beetle upon a simulated parasite attack. Oecologia 182:99–109

  40. Lev-Yadun S, Dafni A, Flaishman MA, Inbar M, Izhaki I, Katzir G, Ne’eman G (2004) Plant coloration undermines herbivorous insect camouflage. BioEssays 26:1126–1130

  41. Lindstedt C, Lindström L, Mappes J (2009) Thermoregulation constrains effective warning signal expression. Evolution 63:469–478

  42. Majerus MEN (1998) Melanism: evolution in action. Oxford University Press, Oxford

  43. Ounap E, Viidalepp J, Truuverk A (2016) Phylogeny of the subfamily Larentiinae (Lepidoptera: Geometridae): integrating molecular data and traditional classifications. Syst Entomol 41:824–843

  44. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2015) nlme: linear and nonlinear mixed effects models. R package version 3.1-122. Accessed 31 May 2018

  45. Pinkert S, Brandl R, Zeuss D (2017) Colour lightness of dragonfly assemblages across North America and Europe. Ecography 40:1110–1117

  46. Porter WP, Gates DM (1969) Thermodynamic equilibria of animals with environment. Ecol Monogr 39:227–244

  47. Regier JC, Mitter C, Zwick A, Bazinet AL, Cummings MP, Kawahara AY, Sohn JC, Zwickl DJ, Cho S, Davis DR, Baixeras J, Brown J, Parr C, Weller S, Lees DC, Mitter KT (2013) A large-scale, higher-level, molecular phylogenetic study of the insect order Lepidoptera (moths and butterflies). PLoS One 8:e58568

  48. Rich PM, Clark DB, Clark DA, Oberbauer SF (1993) Long-term study of solar radiation regimes in a tropical wet forest using quantum sensors and hemispherical photography. Agr For Meteorol 65:107–127

  49. Roslin T, Hardwick B, Novotny V, Petry WK, Andrew NR, Asmus A, Barrio IC, Basset Y, Boesing AL, Bonebrake TC, Cameron EK, Dattilo W, Donoso DA, Drozd P, Gray CL, Hik DS, Hill SJ, Hopkins T, Huang S, Koane B, Laird-Hopkins B, Laukkanen L, Lewis OT, Milne S, Mwesige I, Nakamura A, Nell CS, Nichols E, Prokurat A, Sam K, Schmidt NM, Slade A, Slade V, Suchankova A, Teder T, van Nouhuys S, Vandvik V, Weissflog A, Shukovich V, Slade E (2017) Higher predation risk for insect prey at low latitudes and elevations. Science 356:742–744

  50. Sargent TD (1966) Background selections of geometrid and noctuid moths. Science 154:1674–1675

  51. Scheffers BR, Williams SE (2018) Tropical mountain passes are out of reach–but not for arboreal species. Front Ecol Environ 16:101–108

  52. Scheffers BR, Phillips BL, Laurance WF et al (2013) Increasing arboreality with altitude: a novel biogeographic dimension. Proc R Soc Lond B Biol Sci 280:20131581

  53. Scoble MJ (1992) The Lepidoptera. Form, function and diversity. Oxford University Press, Oxford

  54. Sihvonen P, Mutanen M, Kaila L, Brehm G, Hausmann A, Staude HS (2011) Comprehensive molecular sampling yields a robust phylogeny for geometrid moths (Lepidoptera: Geometridae). PLoS One 6:e20356

  55. Southwood TRE, Henderson PA (2000) Ecological methods. Blackwell Science, Hoboken

  56. Stuart-Fox D, Newton E, Clusella-Trullas S (2017) Thermal consequences of colour and near-infrared reflectance. Philos Trans R Soc B 372:20160345

  57. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Accessed 31 May 2018

  58. True JR (2003) Insect melanism: the molecules matter. Trends Ecol Evol 18:640–647

  59. Walstad JD, Anderson RF, Stambaugh WJ (1970) Effects of environmental conditions on two species of muscardine fungi (Beauveria bassiana and Metarrhizium anisopliae). J Invertebr Pathol 16:221–226

  60. Watt WB (1968) Adaptive significance of pigment polymorphisms in Colias butterflies. I. Variation of melanin pigment in relation to thermoregulation. Evolution 22:437–458

  61. Wilson K, Cotter SC, Reeson AF, Pell JK (2001) Melanism and disease resistance in insects. Ecol Lett 4:637–649

  62. Wittkopp PJ, Beldade P (2009) Development and evolution of insect pigmentation: genetic mechanisms and the potential consequences of pleiotropy. Semin Cell Dev Biol 20:65–71

  63. Xing S, Bonebrake TC, Tang CC, Pickett EJ, Cheng W, Greenspan SE, Williams SE, Scheffers BR (2016) Cool habitats support darker and bigger butterflies in Australian tropical forests. Ecol Evol 6:8062–8074

  64. Xing S, Cheng W, Nakamura A, Tang CC, Pickett EJ, Huang S, Odell E, Goodale E, Goodale UM, Bonebrake TC (2018) Elevational clines in morphological traits of subtropical and tropical butterfly assemblages. Biol J Linnean Soc 123:506–517

  65. Zeuss D, Brandl R, Brändle M, Rahbek C, Brunzel S (2014) Global warming favours light-coloured insects in Europe. Nat Commun 5:3874

  66. Zeuss D, Brunzel S, Brandl R (2017) Environmental drivers of voltinism and body size in insect assemblages across Europe. Glob Ecol Biogeogr 26:154–165

  67. Zou Y, Sang W, Hausmann A, Axmacher JC (2016) High phylogenetic diversity is preserved in species-poor high-elevation temperate moth assemblages. Sci Rep 6:23045

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We thank Gray Williams, Jacintha Ellers and Richard Saunders, and three anonymous referees for valuable comments on the manuscript. Discussions with Evan Pickett and Toby Tsang also improved the statistical analyses. This research was supported by the Queensland/Chinese Academy of Sciences Biotechnology Fund (GJHZ1130). SX and TCB were supported by the Research Grants Council (GRF 17152316) of Hong Kong, ZS by the Applied Fundamental Research Foundation of Yunnan Province (2013FB079) and AN by the National Natural Science Foundation of China General Program (31770472), and the CAS 135 Programs (2017XTBG-T01 and 2017XTBG-F01).

Author information

SX and RLK originally conceived the idea. RLK, LAA, AN, TCB and SX developed the methodology. LAA, RLK, MC, ZS and AN collected the field data and specimens. SX and JCH conducted the morphological analysis. SX performed the statistical analysis. SX and AN wrote the manuscript; other authors provided editorial advice.

Correspondence to Akihiro Nakamura.

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Communicated by Roland A. Brandl.

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Xing, S., Bonebrake, T.C., Ashton, L.A. et al. Colors of night: climate–morphology relationships of geometrid moths along spatial gradients in southwestern China. Oecologia 188, 537–546 (2018).

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  • Morphology
  • Solar radiation
  • Temperature
  • Nocturnal
  • Insect