Abstract
Selective pressures have favored conspicuous coloration across a wide variety of taxa. A particularly striking example of conspicuous coloration is the brilliant red chest patch of male geladas (Theropithecus gelada), a species of cercopithecine monkey found in the high-altitude regions of Ethiopia. Previous research found that gelada chest patch redness increases with age (adult vs subadult), social status (“leader” vs non-leader), and mating opportunities (number of adult females), but the mechanism mediating changes in redness has not yet been examined. First, we validated and compared multiple color measurement methods (Adobe Photoshop, micaToolbox designed for use with ImageJ, and a subjective measure using the human eye). Second, we demonstrated that chest patch redness is positively associated with high-intensity physical activity, the application of a heat pack directly to the chest skin, and higher chest skin surface temperatures. Together, these results suggest that increases in chest redness are mediated by increased blood flow to this area with a concomitant increase in surface temperature. Further research is needed to understand both the energetic costs associated with redness and how other males respond to variation in the signal.
Similar content being viewed by others
Change history
30 September 2022
Supplementary Information was updated.
References
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using Lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bell RB, Bradley BJ, Kamilar JM (2021) The evolutionary ecology of primate hair coloration: a phylogenetic approach. J Mamm Evol. https://doi.org/10.1007/s10914-021-09547-8
Benítez ME (2016) Sizing up strangers: sexual selection and vocal signals in gelada males. PhD thesis. University of Michigan, Ann Arbor.
Benítez ME, Le Roux A, Fischer J, Beehner JC, Bergman TJ (2016) Acoustic and temporal variation in gelada (Theropithecus gelada) loud calls advertise male quality. Int J Primatol 37:568–585. https://doi.org/10.1007/s10764-016-9922-0
Bergman TJ (2010) Experimental evidence for limited vocal recognition in a wild primate: implications for the social complexity hypothesis. Proc Biol Sci 277:3045–3053. https://doi.org/10.1098/rspb.2010.0580
Bergman TJ, Beehner JC (2008) A simple method for measuring colour in wild animals: validation and use on chest patch colour in geladas (Theropithecus gelada). Biol J Linn Soc Lond 94:231–240. https://doi.org/10.1111/j.1095-8312.2008.00981.x
Bergman TJ, Sheehan MJ (2013) Social knowledge and signals in primates. Am J Primatol. https://doi.org/10.1002/ajp.22103
Bergman TJ, Ho L, Beehner JC (2009) Chest color and social status in male geladas (Theropithecus gelada). Int J Primatol 30:791–806. https://doi.org/10.1007/s10764-009-9374-x
Bowmaker JK, Astell S, Hunt DM, Mollon JD (1991) Photosensitive and photostable pigments in the retinae of Old World monkeys. J Exp Biol 156:1–19
Bradley BJ, Mundy NI (2008) The primate palette: The evolution of primate coloration. Evol Anthropol 17:97–111. https://doi.org/10.1002/evan.20164
Caro T (2005) The adaptive significance of coloration in mammals. Bioscience 55:125–136. https://doi.org/10.1641/0006-3568(2005)055[0125:TASOCI]2.0.CO;2
Changizi MA, Zhang Q, Shimojo S (2006) Bare skin, blood and the evolution of primate colour vision. Biol Lett 2:217–221. https://doi.org/10.1098/rsbl.2006.0440
Chappell MA, Hammond KA (2004) Maximal aerobic performance of deer mice in combined cold and exercise challenges. J Comp Physiol B 174:41–48. https://doi.org/10.1007/s00360-003-0387-z
Cheviron ZA, Bachman GC, Storz JF (2013) Contributions of phenotypic plasticity to differences in thermogenic performance between highland and lowland deer mice. J Exp Biol 216:1160–1166. https://doi.org/10.1242/jeb.075598
Cicchetti DV (1994) Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. Psychol Assess 6(4):284–290. https://doi.org/10.1037/1040-3590.6.4.284
Cooper VJ, Hosey GR (2003) Sexual dichromatism and female preference in Eulemur fulvus subspecies. Int J Primatol 24:1177–1188. https://doi.org/10.1023/B:IJOP.0000005986.21477.ad
Cuthill I, Stevens M, Sheppard J, Maddocks C, Párraga A, Troscianko TS (2005) Disruptive coloration and background pattern matching. Nature 434:72–74. https://doi.org/10.1038/nature03312
DeLacey PM, Bergman TJ, Beehner JC (2019) Temperature alters chest redness in male geladas. In: 88th Annual Meeting of the American Association for Physical Anthropologists [Poster session]. Cleveland, OH, USA
Deschner T, Heistermann M, Hodges K, Boesch C (2004) Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Horm Behav 46:204–215. https://doi.org/10.1016/j.yhbeh.2004.03.013
Douglas PH, Hohmann G, Murtagh R, Thiessen-Bock R, Deschner T (2016) Mixed messages: wild female bonobos show high variability in the timing of ovulation in relation to sexual swelling patterns. BMC Evol Biol 16:140. https://doi.org/10.1186/s12862-016-0691-3
Dubuc C, Brent LJN, Accamando AK, Gerald MS, MacLarnon A, Semple S, Heistermann M, Engelhardt A (2009) Sexual skin color contains information about the timing of the fertile phase in free-ranging Macaca mulatta. Int J Primatol 30:777–789. https://doi.org/10.1007/s10764-009-9369-7
Dubuc C, Winters S, Allen WL, Brent LJN, Cascio J, Maestripieri D, Ruiz-Lambides AV, Widdig A, Higham JP (2014a) Sexually selected skin colour is heritable and related to fecundity in a non-human primate. Proc Biol Sci 281:20141602. https://doi.org/10.1098/rspb.2014.1602
Dubuc C, Allen WL, Maestripieri D, Higham JP (2014b) Is male rhesus macaque red color ornamentation attractive to females? Behav Ecol Sociobiol 68:1215–1224. https://doi.org/10.1007/s00265-014-1732-9
Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc Lond 41:315–352. https://doi.org/10.1111/j.1095-8312.1990.tb00839.x
Exnerová A, Landová E, Štys P, Fuchs R, Prokopová M, Cehláriková P (2003) Reactions of passerine birds to aposematic and non-aposematic firebugs (Pyrrhocoris apterus; Heteroptera). Biol J Linn Soc Lond 78:517–525. https://doi.org/10.1046/j.0024-4066.2002.00161.x
Gamer M, Lemon J, Fellows I, Singh P (2019) irr: Various coefficients of interrater reliability agreement. R package version 0.84.1. https://CRAN.R-project.org/package=irr
Gerald MS (2001) Primate colour predicts social status and aggressive outcome. Anim Behav 61:559–566. https://doi.org/10.1006/anbe.2000.1648
Gesquiere LR, Wango EO, Alberts SC, Altmann J (2007) Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons. Horm Behav 51:114–125. https://doi.org/10.1016/j.yhbeh.2006.08.010
Gestich CC, Caselli CB, Setz EZF (2014) Behavioural thermoregulation in a small neotropical primate. Ethology 120:331–339. https://doi.org/10.1111/eth.12203
Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17:509–528. https://doi.org/10.1017/S0952523800174036
Grueter CC, Zhu P, Allen WL, Higham JP, Ren B, Li M (2015a) Sexually selected lip colour indicates male group-holding status in the mating season in a multi-level primate society. R Soc Open Sci 2:150490. https://doi.org/10.1098/rsos.150490
Grueter CC, Isler K, Dixson BJ (2015b) Are badges of status adaptive in large complex primate groups? Evol Hum Behav 36:398–406. https://doi.org/10.1016/j.evolhumbehav.2015.03.003
Hallgren KA (2012) Computing inter-rater reliability for observational data: an overview and tutorial. Tutor Quant Methods Psychol 8(1):23–24. https://doi.org/10.20982/tqmp.08.1.p023
Hanya G, Kiyono M, Hayaishi S (2007) Behavioral thermoregulation of wild Japanese macaques: comparisons between two subpopulations. Am J Primatol 69:802–815. https://doi.org/10.1002/ajp.20397
Hayes JP (1989) Field and maximal metabolic rates of deer mice (Peromyscus maniculatus) at low and high altitudes. Physiol Zool 62:732–744. https://doi.org/10.1086/physzool.62.3.30157924
Heinonen I, Brothers RM, Kemppainen J, Knuuti J, Kalliokoski KK, Crandall CG (2011) Local heating, but not indirect whole body heating, increases human skeletal muscle blood flow. J Appl Physiol 111:818–824. https://doi.org/10.1152/japplphysiol.00269.2011
Hendershott R, Hu G, Groves C, Behie A (2019) Natal-to-juvenile pelage change in free-living François’ (Trachypithecus francoisi) and Cat Ba langurs (T. poliocephalus). Viet JPrimatol 3: 41–54. http://hdl.handle.net/1885/207918
Higham JP (2006) The reproductive ecology of female olive baboons (Papio hamadryas anubis), at Gashaka-Gumti National Park, Nigeria. PhD thesis. Roehampton University: London.
Higham JP, Heistermann M, Saggau C, Agil M, Perwitasari-Farajallah D, Engelhardt A (2012) Sexual signalling in female crested macaques and the evolution of primate fertility signals. BMC Evol Biol 12:89. https://doi.org/10.1186/1471-2148-12-89
Higham JP, Pfefferle D, Heistermann M, Maestripieri D, Stevens M (2013) Signaling in multiple modalities in male rhesus macaques: sex skin coloration and barks in relation to androgen levels, social status, and mating behavior. Behav Ecol Sociobiol 67:1457–1469. https://doi.org/10.1007/s00265-013-1521-x
Hou R, Chapman CA, Jay O, Guo S, Li B, Raubenheimer D (2020) Cold and hungry: combined effects of low temperature and resource scarcity on an edge-of-range temperate primate, the golden snub-nose monkey. Ecography 43:1672–1682. https://doi.org/10.1111/ecog.05295
Houde A (2019) Sex, color, and mate choice in guppies. Princeton University Press
Jablonski NG, Chaplin G (2010) Human skin pigmentation as an adaptation to UV radiation. Proc Natl Acad Sci USA 107(Supplement 2):8962–8968. https://doi.org/10.1073/pnas.0914628107
Jacobs GH, Deegan JF 2nd (1999) Uniformity of colour vision in Old World monkeys. Proc Biol Sci 266:2023–2028. https://doi.org/10.1098/rspb.1999.0881
Johnson JM (1986) Nonthermoregulatory control of human skin blood flow. J Appl Physiol 61:1613–1622. https://doi.org/10.1152/jappl.1986.61.5.1613
Kamilar JM, Bradley BJ (2011) Interspecific variation in primate coat colour supports Gloger’s rule. J Biogeogr 38:2270–2277. https://doi.org/10.1111/j.1365-2699.2011.02587.x
Kassambara A (2020) ggpubr: ‘ggplot2’ based publication ready plots. R package version 0.4.0. https://CRAN.R-project.org/package=ggpubr
Kelley EA, Jablonski NG, Chaplin G, Sussman RW, Kamilar JM (2016) Behavioral thermoregulation in Lemur catta: the significance of sunning and huddling behaviors. Am J Primatol 78:745–754. https://doi.org/10.1002/ajp.22538
Kenney WL, Johnson JM (1992) Control of skin blood flow during exercise. Med Sci Sports Exerc 24:303–312. https://doi.org/10.1249/00005768-199203000-00005
Keyser AJ, Hill GE (2000) Structurally based plumage coloration is an honest signal of quality in male blue grosbeaks. Behav Ecol 11:202–209. https://doi.org/10.1093/beheco/11.2.202
Kingdon JS (2010) The role of visual signals and face patterns in African forest monkeys (guenons) of the genus Cercopithecus. Trans Zool Soc Lond 35:425–475. https://doi.org/10.1111/j.1096-3642.1980.tb00062.x
Kitchen DM, Seyfarth RM, Fischer J, Cheney DL (2003) Loud calls as indicators of dominance in male baboons (Papio cynocephalus ursinus). Behav Ecol Sociobiol 53:374–384. https://doi.org/10.1007/s00265-003-0588-1
Kuze N, Malim TP, Kohshima S (2005) Developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus): possible signals in visual communication. Am J Primatol 65:353–376. https://doi.org/10.1002/ajp.20121
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82(13):1–26. https://doi.org/10.18637/jss.v082.i13
Lev-Yadun S (2001) Aposematic (warning) coloration associated with thorns in higher plants. J Theor Biol 210:385–388. https://doi.org/10.1006/jtbi.2001.2315
Lindstedt C, Lindström L, Mappes J (2009) Thermoregulation constrains effective warning signal expression. Evolution 63:469–478. https://doi.org/10.1111/j.1558-5646.2008.00561.x
Marty JS, Higham JP, Gadsby EL, Ross C (2009) Dominance, coloration, and social and sexual behavior in male drills Mandrillus leucophaeus. Int J Primatol 30:807–823. https://doi.org/10.1007/s10764-009-9382-x
Maynard Smith J (1982) Evolution and the theory of games. Cambridge University Press, Cambridge
McFarland R, Fuller A, Hetem RS, Mitchell D, Maloney SK, Henzi SP, Barrett L (2015) Social integration confers thermal benefits in a gregarious primate. J Anim Ecol 84:871–878. https://doi.org/10.1111/1365-2656.12329
McGraw KO, Wong SP (1996) Forming inferences about some intraclass correlation coefficients. Psychol Methods 1(1):30–46. https://doi.org/10.1037/1082-989X.1.1.30
Milledge JS, West JB, Schoene RB (2007) High altitude medicine and physiology. CRC Press
Mourthe I, Trindade RA, Aguiar LM, Trigo TC, Bicca-Marques JC, Bonatto SL (2019) Hybridization between neotropical primates with contrasting sexual dichromatism. Int J Primatol 40:99–113. https://doi.org/10.1007/s10764-017-0011-9
Osorio D, Vorobyev M (2005) Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proc Biol Sci 272:1745–1752. https://doi.org/10.1098/rspb.2005.3156
Osorio D, Vorobyev M (2008) A review of the evolution of animal colour vision and visual communication signals. Vision Res 48:2042–2051. https://doi.org/10.1016/j.visres.2008.06.018
Pappano DJ, Beehner JC (2014) Harem-holding males do not rise to the challenge: androgens respond to social but not to seasonal challenges in wild geladas. R Soc Open Sci 1:140081. https://doi.org/10.1098/rsos.140081
Parr LA, Winslow JT, Hopkins WD, de Waal FB (2000) Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). J Comp Psychol 114:47–60. https://doi.org/10.1037/0735-7036.114.1.47
Patricelli GL, Hebets EA (2016) New dimensions in animal communication: the case for complexity. Curr Opin in Behav Sci 12:80–89. https://doi.org/10.1016/j.cobeha.2016.09.011
Penn DJ, Számadó S (2019) The Handicap Principle: how an erroneous hypothesis became a scientific principle. Biol Rev Camb Philos Soc. https://doi.org/10.1111/brv.12563
Potash AD, Greene DU, Foursa GA, Mathis VL, Conner LM, McCleery RA (2020) A comparison of animal color measurements using a commercially available digital color sensor and photograph analysis. Curr Zool 66:601–606. https://doi.org/10.1093/cz/zoaa016
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, URL https://www.R-project.org/
Rettenmeyer CW (1970) Insect mimicry. Annu Rev Entomol 15:43–74. https://doi.org/10.1146/annurev.en.15.010170.000355
Rhodes L, Argersinger ME, Gantert LT, Friscino BH, Hom G, Pikounis B, Hess DL, Rhodes WL (1997) Effects of administration of testosterone, dihydrotestosterone, oestrogen and fadrozole, an aromatase inhibitor, on sex skin colour in intact male rhesus macaques. J Reprod Fertil 111:51–57. https://doi.org/10.1530/jrf.0.1110051
Rigaill L, Higham JP, Winters S, Garcia C (2019) The redder the better? Information content of red skin coloration in female Japanese macaques. Behav Ecol Sociobiol. https://doi.org/10.1007/s00265-019-2712-x
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Setchell JM, Dixson AF (2001) Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Horm Behav 39:177–184. https://doi.org/10.1006/hbeh.2000.1628
Setchell JM, Wickings EJ, Knapp LA (2006) Signal content of red facial coloration in female mandrills (Mandrillus sphinx). Proc Biol Sci 273:2395–2400. https://doi.org/10.1098/rspb.2006.3573
Siddiqi A, Cronin TW, Loew ER, Vorobyev M, Summers K (2004) Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. J Exp Biol 207:2471–2485. https://doi.org/10.1242/jeb.01047
Snyder-Mackler N, Beehner JC, Bergman TJ (2012a) Defining higher levels in the multilevel societies of geladas (Theropithecus gelada). Int J Primatol 33:1054–1068. https://doi.org/10.1007/s10764-012-9584-5
Snyder-Mackler N, Alberts SC, Bergman TJ (2012b) Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups. Proc R Soc B 279:3788–3795. https://doi.org/10.1098/rspb.2012.0842
Stephen ID, Coetzee V, Law Smith M, Perrett DI (2009) Skin blood perfusion and oxygenation colour affect perceived human health. PLoS ONE 4:e5083. https://doi.org/10.1007/s10764-009-9380-z
Stevens M, Merilaita S (2011) Animal camouflage: mechanisms and function. Cambridge University Press
Stevens M, Párraga CA, Cuthill IC, Partridge JC, Troscianko TS (2007) Using digital photography to study animal coloration. Biol J Linn Soc Lond 90:211–237. https://doi.org/10.1111/j.1095-8312.2007.00725.x
Terrien J, Perret M, Aujard F (2011) Behavioral thermoregulation in mammals: a review. Front Biosci 16:1428–1444. https://doi.org/10.2741/3797
Tinsley Johnson E, Snyder-Mackler N, Lu A, Bergman TJ, Beehner JC (2018) Social and ecological drivers of reproductive seasonality in geladas. Behav Ecol 29:574–588. https://doi.org/10.1093/beheco/ary008
Troscianko J, Stevens M (2015) Image calibration and analysis toolbox–a free software suite for objectively measuring reflectance, colour and pattern. Methods Ecol Evol 6:1320–1331. https://doi.org/10.1111/2041-210X.12439
Uy JAC, Moyle RG, Filardi CE, Cheviron ZA (2009) Difference in plumage color used in species recognition between incipient species is linked to a single amino acid substitution in the melanocortin-1 receptor. Am Nat 174:244–254. https://doi.org/10.1086/600084
van den Berg CP, Troscianko J, Endler JA, Marshall NJ, Cheney KL (2020) Quantitative colour pattern analysis (QCPA): a comprehensive framework for the analysis of colour patterns in nature. Methods Ecol Evol 11:316–332. https://doi.org/10.1111/2041-210X.13328
Waitt C, Gerald MS, Little AC, Kraiselburd E (2006) Selective attention toward female secondary sexual color in male rhesus macaques. Am J Primatol 68:738–744. https://doi.org/10.1002/ajp.20264
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Wickings EJ, Dixson AF (1992) Testicular function, secondary sexual development, and social status in male mandrills (Mandrillus sphinx). Physiol Behav 52:909–916. https://doi.org/10.1016/0031-9384(92)90370-H
Winters S, Allen WL, Higham JP (2020) The structure of species discrimination signals across a primate radiation. Elife 9:47428. https://doi.org/10.7554/eLife.47428
Acknowledgements
We are grateful to the Ethiopian Wildlife Conservation Authority for granting us permission to conduct this research. We also want to thank the many staff and wardens (Berhanu Gebre, Maru Biadglegn, Abebaw Azanaw Haile) of the Simien Mountains National Park, our Ethiopian staff (Esheti Jejaw, Ambaye Fanta, Setey Girmay, Yeshi Dessie, Dereje Bewket, Atirsaw Aduga, Tariku W/Aregay, Shifarew Asrat), our research assistants in the field (Clay Wilton, Julie Jarvey, Levi Morris, Tara Regan, Caitlin Hawley, Peter Clark, Evan Sloan, Megan Gomery, Laura Morrissey, Emily Downey, Eddy Wild, Liz Babbitt, Maddie Melton, Anna Cryer). We thank Jeanne Altmann from the Amboseli Baboon Project for loaning us the Raytek MX6 PhotoTemp Infrared Thermometer.
Funding
This work was supported by the National Science Foundation (BCS-2041542, BCS-0715179, BCS-1732231, BCS-1723237, BCS-2010309, BCS-1723228, IOS-1255974, IOS-1854359), the Leakey Foundation (AWD015438), the Leakey Foundation Baldwin Award (AWD012312), the National Geographic Society (NGS-8100–06, NGS-8989–11, NGS-1242, and NGS-50409R-18), the Fulbright Scholars Program, Nacey Maggioncalda Foundation, Sigma Xi, the University of Michigan, Arizona State University, and Stony Brook University.
Author information
Authors and Affiliations
Contributions
Conceptualization, data curation, formal analysis, investigation, visualization: PMD, RFP, JCB, TJB; data collection: PMD, RFP, SS, ISC, KLC, AL, FA, NSM, JCB, TJB; writing—original draft: PMD, RFP, JCB, TJB; writing—review and editing: all the authors; supervision: JCB, TJB. All the authors reviewed the results and approved the final version of the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
On behalf of all the authors, the corresponding author states that there is no conflict of interest.
Data availability
Data and code are available at https://github.com/GeladaResearchProject/DeLacey_Perlman_et_al_chest_color_2022.
Additional information
Handling editors: Scott Y.S. Chui and Leszek Karczmarski.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliation'.
This article is a contribution to the special issue on “Individual Identification and Photographic Techniques in Mammalian Ecological and Behavioural Research – Part 1: Methods and Concepts” — Editors: Leszek Karczmarski, Stephen C.Y. Chan, Daniel I. Rubenstein, Scott Y.S. Chui and Elissa Z. Cameron.
Supplementary Information was updated.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
DeLacey, P.M., Perlman, R.F., Sen, S. et al. Assessing male gelada chest patches: color measurement and physiological mechanisms. Mamm Biol 102, 751–763 (2022). https://doi.org/10.1007/s42991-021-00211-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42991-021-00211-5