Skip to main content
Log in

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

  • Community ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Barton K (2016) MuMIn: multi-model inference. R package version 1.15.6. https://CRAN.R-project.org/package=MuMIn. Accessed 31 May 2018

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1111/een.12499

    Article  Google Scholar 

  • 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

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1111/geb.12703

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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. http://www.cran.r-project.org/package=nlme. Accessed 31 May 2018

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed 31 May 2018

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

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

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Akihiro Nakamura.

Additional information

Communicated by Roland A. Brandl.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 3868 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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). https://doi.org/10.1007/s00442-018-4219-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-018-4219-y

Keywords

Navigation