Abstract
Studies on animal camouflage offer some of the most compelling examples of microevolution via natural selection. If selection favouring camouflage is indeed widespread, the colour of the vegetation might act as a filter by removing non-camouflaged species. Consequently, the colouration and diversity of colours of animal communities may follow similar patterns to those of the vegetation. During wet and dry periods of the year, we extracted physical descriptors of chromatic and achromatic dimensions of arthropods and vegetation items collected from neighbouring vegetational types: a seasonal savanna (cerrado) and an evergreen gallery forest. Here, colouration can be understood as a trait, and we seek to describe and comprehend patterns at the community-level. The colours of the arthropods in the gallery forest were similar to the vegetation and followed the relatively small changes in this vegetational type. This could indicate the potential for the studied animals to be, overall, camouflaged against the vegetation. Conversely, the cerrado vegetation during the dry season was dominated by dry grasses and a homogeneous beige tint. After the dry season, the vegetation shifted to a bimodal distribution, dominated by the green of new leaves. The diversity of arthropod colours changed, to some extent, in concert with the vegetation. However, the peak location of arthropod colouration did not follow the vegetation. The Cerrado colour variation could act as one of the filters in these arthropod communities.
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Data are publicly available at Figshare (figshare.com). https://doi.org/10.6084/m9.figshare.14547441.
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Code is publicly available at Figshare (figshare.com). https://doi.org/10.6084/m9.figshare.14547441.
References
Bürkner PC (2018) Advanced Bayesian multilevel modeling with the R package brms. The R J 10(1):395–411. https://doi.org/10.32614/RJ-2018-017
Camargo MGG, Cazetta E, Morellato LPC, Schaefer HM (2014) Characterising background heterogeneity in visual communication. Basic Appl Ecol 15(4):326–335. https://doi.org/10.1016/j.baae.2014.06.002
Carpenter B, Gelman A, Hoffman MD, Lee D, Goodrich B, Betancourt M, Brubaker M, Guo J, Li P, Riddell A (2017) Stan: a probabilistic programming language. J Stat Softw 76(1). https://doi.org/10.18637/jss.v076.i01
Caves EM, Brandley NC, Johnsen S (2018) Visual acuity and the evolution of signals. Trends Ecol Evol 33(5):358–372. https://doi.org/10.1016/j.tree.2018.03.001
Curado AC (2018) A influência da heterogeneidade ambiental sobre os padrões de coloração crípticos. Master Thesis. Universidade Federal de Goiânia, Goiânia, Brazil
Cuthill IC, Allen WL, Arbuckle K, Caspers B, Chaplin G, Hauber ME, Hill GE, Jablonski NG, Jiggins CD, Kelber A, Mappes J, Marshall J, Merrill R, Osorio D, Prum R, Roberts NW, Roulin A, Rowland HM, Sherratt TN, Caro T (2017) The biology of color. Science 357(6350):eaan0221–eaan0229. https://doi.org/10.1126/science.aan0221
Cuthill IC, Stevens M, Sheppard J, Maddocks T, Párraga CA, Troscianko TS (2005) Disruptive coloration and background pattern matching. Nature 434(7029):72–74. https://doi.org/10.1038/nature03312
De Bello F, Vandewalle M, Reitalu T, Leps J, Prentice HC, Lavorel S, Sykes MT (2013) Evidence for scale- and disturbance-dependent trait assembly patterns in dry semi-natural grasslands. J Ecol 101:1237–1244
Defrize J, Thery M, Casas J (2010) Background colour matching by a crab spider in the field: a community sensory ecology perspective. J Exp Biol 213(9):1425–1435. https://doi.org/10.1242/jeb.039743
Duong T (2007) ks: Kernel density estimation and kernel discriminant analysis for multivariate data in R. J Stat Softw 21(7):1–16. https://doi.org/10.18637/jss.v021.i07
Durães R, Marini M (2005) A quantitative assessment of bird diets in the brazilian atlantic forest, with recommendations for future diet studies. Ornitologia Neotropical 16(1):65–83
Dyer LA, Singer MS, Lill JT, Stireman JO, Gentry GL, Marquis RJ, Ricklefs RE, Greeney HF, Wagner DL, Morais HC, Diniz IR, Kursar TA, Coley PD (2007) Host specificity of Lepidoptera in tropical and temperate forests. Nature 448(7154):696–699. https://doi.org/10.1038/nature05884
Endler JA (1984) Progressive background in moths, and a quantitative measure of crypsis. Biol J Linn Soc 22:187–231. https://doi.org/10.1111/j.1095-8312.1984.tb01677.x
Endler JA (2012) A framework for analysing colour pattern geometry: adjacent colours. Biol J Linn Soc 107(2):233–253. https://doi.org/10.1111/j.1095-8312.2012.01937.x
Farkas TE, Mononen T, Comeault AA, Hanski I, Nosil P (2013) Evolution of camouflage drives rapid ecological change in an insect community. Curr Biol 23(19):1835–1843. https://doi.org/10.1016/j.cub.2013.07.067
Forsman A, Karlsson M, Wennersten L, Johansson J, Karpestam E (2011) Rapid evolution of fire melanism in replicated populations of pygmy grasshoppers. Evolution 65(9):2530–2540. https://doi.org/10.1111/j.1558-5646.2011.01324.x
Gawryszewski FM (2018) Color vision models: some simulations, a general n-dimensional model, and the colourvision R package. Ecol Evol 8(16):8159–8170. https://doi.org/10.1002/ece3.4288
Hart NS (2001) The visual ecology of avian photoreceptors. Prog Retin Eye Res 20(5):675–703. https://doi.org/10.1016/s1350-9462(01)00009-x
Johnsen S (2016) How to measure color using spectrometers and calibrated photographs. J Exp Biol 219(6):772–778. https://doi.org/10.1242/jeb.124008
Kettlewell HBD (1955) Selection experiments on industrial melanism in the Lepidoptera. Heredity 9(3):323–342. https://doi.org/10.1038/hdy.1955.36
Leal CRO, Fagundes M, de Neves F (2015) Change in herbivore insect communities from adjacent habitats in a transitional region. Arthropod Plant Interact 9(3):311–320. https://doi.org/10.1007/s11829-015-9362-3
Lecoq M, Pierozzi I (1996) Chromatic polymorphism and geophagy: two outstanding characteristics of Rhammatocerus schistocercoides (Rehn 1906) grasshoppers in Brazil (Orthoptera, Acrididae, Gomphocerinae). J Orthoptera Res 5:13. https://doi.org/10.2307/3503570
Lima SL, Dill LM (2012) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68(4):619–640. https://doi.org/10.1139/z90-092
Manhães MA, Loures-Ribeiro A, Dias MM (2010) Diet of understorey birds in two Atlantic Forest areas of southeast Brazil. J Nat Hist 44(7–8):469–489. https://doi.org/10.1080/00222930903380947
Marquis RJ, Diniz IR, Morais HC (2001) Patterns and correlates of interspecific variation in foliar insect herbivory and pathogen attack in Brazilian cerrado. J Trop Ecol 17(1):127–148. https://doi.org/10.1017/s0266467401001080
Marquis RJ, Morais HC, Diniz IR (2002) Interactions among Cerrado plants and their herbivores: unique or typical? In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil. Columbia University Press, New York, pp 306–328
Mayekar HV, Kodandaramaiah U (2017) Pupal colour plasticity in a tropical butterfly, Mycalesis mineus (Nymphalidae: Satyrinae). PLoS ONE 12(2):e0171482. https://doi.org/10.1371/journal.pone.0171482
Merilaita S (2001) Habitat heterogeneity, predation and gene flow: colour polymorphism in the isopod, Idotea baltica. Evol Ecol 15(2):103–116. https://doi.org/10.1023/a:1013814623311
Moraes VDS (2015) Efeitos da estrutura da vegetação na composição da assembleia de aranhas (Arachnida: Araneae) em estrato arbóreo de diferentes fitofisionomias do Cerrado. Master Thesis. Universidade de Brasília, Brasília, Brazil
Nachman MW, Hoekstra HE, D’Agostino SL (2003) The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci 100(9):5268–5273. https://doi.org/10.1073/pnas.0431157100
Neves FS, Araújo LS, Espírito-Santo MM, Fagundes M, Fernandes GW, Sanchez‐Azofeifa GA, Quesada M (2010) Canopy herbivory and insect herbivore diversity in a dry forest–savanna transition in Brazil. Biotropica 42(1):112–118. https://doi.org/10.1111/j.1744-7429.2009.00541.x
Oliveira-Filho T, Ratter JA (2002) Vegetation physiognomies and woody flora of the Cerrado biome. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil. Columbia University Press, New York, pp 91–120
Price N, Green S, Troscianko J, Tregenza T, Stevens M (2019) Background matching and disruptive coloration as habitat-specific strategies for camouflage. Sci Rep 9(7840):1–10. https://doi.org/10.1038/s41598-019-44349-2
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry, 1st edn. Oxford University Press, Oxford, pp 1–262
Schaefer HM, Stobbe N (2006) Disruptive coloration provides camouflage independent of background matching. Proc R Soc Lond Ser B Biol Sci 273(1600):2427–2432. https://doi.org/10.1098/rspb.2006.3615
Shapiro AM (1976) Seasonal polyphenism. In: Hecht MK, Steere WC, Wallace B (eds) Evolutionary biology, vol 9. Plenum Press, New York, pp 259–333
Siqueira P, Vasconcelos M, Gonçalves R, Leite L (2015) Assessment of stomach contents of some amazonian birds. Ornitologia Neotropical 26:79–88
Stevens M, Merilaita S (2008) Animal camouflage: current issues and new perspectives. Philos Trans R Soc B Biol Sci 364(1516):423–427. https://doi.org/10.1098/rstb.2008.0217
Stevens M, Párraga CA, Cuthill IC, Partridge JC, Troscianko TS (2007) Using digital photography to study animal coloration. Biol J Linn Soc 90(2):211–237. https://doi.org/10.1111/j.1095-8312.2007.00725.x
Troscianko J, Stevens M (2015) Image calibration and analysis toolbox—a free software suite for objectively measuring reflectance, colour and pattern. Methods Ecol Evol 6(11):1320–1331. https://doi.org/10.1111/2041-210x.12439
van Bergen E, Beldade P (2019) Seasonal plasticity in anti-predatory strategies: matching of color and color preference for effective crypsis. Evol Lett 3(3):313–320. https://doi.org/10.1002/evl3.113
Xiao F, Cuthill IC (2016) Background complexity and the detectability of camouflaged targets by birds and humans. Proc R Soc B Biol Sci 283(1838):20161527. https://doi.org/10.1098/rspb.2016.1527
Ximenes N, Gawryszewski FM (2018) Prey and predators perceive orb-web spider conspicuousness differently: evaluating alternative hypotheses for colour polymorphism evolution. Curr Zool 65(5):559–570. https://doi.org/10.1093/cz/zoy069
Acknowledgements
We are grateful to Pedro Togni and Marcos R. Lima for insightful comments on the manuscript, Caroline M. Goulart for performing the image segmentation, Izabel C. S. C. Salvi, Victor H. Pimentel, Julia G. Silva, and Gustavo M. Tostes for helping with arthropod collections, and José R. Pujol-Luz, Leonardo F. de Sousa, Milena S. Leite, and Pedro H. O. Ribeiro for helping with spider and insect identification.
Funding
The following research grants supported this study: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil), 428141/2016-1 and Fundação de Apoio à Pesquisa do Distrito Federal (FAP/DF, Brazil), 00193-00002164/2018-5. Universidade de Brasília Edital DPI/DPG 03/2020 provided funds for manuscript editing.
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FMG designed the study. NDM and LGFS collected the data. FMG performed the statistical analyses. NDM, LGFS and FMG wrote the manuscript. NDM and LGFS contributed equally to this study.
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Mello, N.D., Sanchez, L.G.F. & Gawryszewski, F.M. Spatio-temporal colour variation of arthropods and their environment. Evol Ecol 36, 117–133 (2022). https://doi.org/10.1007/s10682-021-10144-7
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DOI: https://doi.org/10.1007/s10682-021-10144-7