Skip to main content
Log in

Resolving tradeoffs among crypsis, escape behavior, and microhabitat use in sexually dichromatic species

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

Abstract

Variation in color pattern between populations of cryptic animals is common and typically attributed to selection pressures from visual predators combined with variation in substrate composition. However, little is known about how cryptic color pattern relates to varied rates of predation, and few studies simultaneously analyze patterns of escape behavior and microhabitat use along with variation in color pattern, even though these traits evolve in tandem. Here, we use a combination of calibrated photographs and spectrometry to examine the influence of spatial heterogeneity in rates of predation on dorsal brightness in the Florida scrub lizard (Sceloporus woodi), a cryptic and sexually dimorphic species. Simultaneously, we analyze patterns of escape behavior and microhabitat use measured in the field. The results of this study indicate that populations inhabiting environments of increased predation have less color variation and more closely match the color of local substrate than populations sampled in environments of relaxed predation. Populations exposed to increased predation also show more pronounced escape behavior and are more selective in their use of microhabitat. Interestingly, geographic variation of dorsal brightness, escape behavior, and microhabitat use were greater for females than for males. Our results not only provide empirical evidence for theories of adaptive coloration, but suggest that sexual dichromatism can be maintained by selection pressures related to predation.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ahnesjo J, Forsman A (2006) Differential habitat selection by pygmy grasshopper color morphs; interactive effects of temperature and predator avoidance. Evol Ecol 20:235–257

    Google Scholar 

  • Badyaev AV, Hill GE (2003) Avian sexual dichromatism in relation to phylogeny and ecology. Annu Rev Ecol Evol Syst 34:27–49

    Google Scholar 

  • Bond AB (2007) The evolution of color polymorphism: crypticity searching images, and apostatic selection. Annu Rev Ecol Evol Syst 38:489–514

    Google Scholar 

  • Bowmaker JK, Heath LA, Wilkie SE, Hunt DM (1997) Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vis Res 37:2183–2194

    CAS  PubMed  Google Scholar 

  • Brodie ED (1992) Correlational selection for color pattern and antipredator behavior in the garter snake thamnophis ordinoides. Evolution 46:1284–1298

    PubMed  Google Scholar 

  • Brown JL, Maan ME, Cummings ME, Summers K (2010) Evidence for selection on coloration in a Panamanian poison frog: a coalescent-based approach. J Biogeogr 37:891–901

    Google Scholar 

  • Bulova SJ (1994) Ecological correlates of population and individual variation in antipredator behavior of two species of desert lizards. Copeia 1994(4):980–992

    Google Scholar 

  • Burkey TV (1993) Edge effects in seed and egg predation at two neotropical rainforest sites. Biol Conserv 66:139–143

    Google Scholar 

  • Calsbeek R, Irschick DJ (2007) The quick and the dead: correlational selection on morphology, performance, and habitat use in island lizards. Evolution 61:2493–2503

    PubMed  Google Scholar 

  • Campbell HW, Christman SP (1982) The herpetological components of Florida sandhill and sand pine scrub associations. Herpetol Communities 13:163–171

    Google Scholar 

  • Castella B, Golay J, Monney JC, Golay P, Mebert K, Dubey S (2013) Melanism, body condition and elevational distribution in the asp viper. J Zool 290:273–280

    Google Scholar 

  • Chunco AJ, Mckinnon JS, Servedio MR (2007) Microhabitat variation and sexual selection can maintain male color polymorphisms. Evolution 61:2504–2515

    PubMed  Google Scholar 

  • Cooper WE (2003) Effect of risk on aspects of escape behavior by a lizard, Holbrookia propinqua, in relation to optimal escape theory. Ethology 109:617–626

    Google Scholar 

  • Cott HB (1940) Adaptive coloration in animals. Methuen, London

    Google Scholar 

  • Cowles RB, Bogert CM (1944) A preliminary study of the thermal requirements of desert reptiles. Bull Am Mus Nat Hist 83:263–296

    Google Scholar 

  • Cox RM, Skelly SL, Leo A, John-Alder HB (2005) Testosterone regulates sexually dimorphic coloration in the eastern fence lizard, Sceloporus undulatus. Copeia 2005(3):597–608

    Google Scholar 

  • Creer DA (2005) Correlations between ontogenetic change in color pattern and antipredator behavior in the racer, Coluber constrictor. Ethology 111:287–300

    Google Scholar 

  • Cuthill IC, Stevens M, Sheppard J, Maddocks T, Parraga CA, Troscianko TS (2005) Disruptive coloration and background pattern matching. Nature 434:72–74

    CAS  PubMed  Google Scholar 

  • Delucchi KL (1993) On the use and misuse of chisquare. In: Keren G, Lewis C (eds) A handbook for data analysis in the behaviroal sciences. Lawrence Erlbaum, Hillsdale, pp 294–319

    Google Scholar 

  • Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91

    PubMed  Google Scholar 

  • Endler JA (1995) Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol Evol 10:22–29

    CAS  PubMed  Google Scholar 

  • Endler JA, Mielke PW (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc 86:405–431

    Google Scholar 

  • Enge KM, Bentzien MM, Percival HF (1986) Florida scrub lizard status survey. Technical Report No. 26, US Fish and Wildlife Service, Jacksonville, Florida, USA

  • Finch VA, Bennett I, Holmes C (1984) Coat colour in cattle: effect on thermal balance, behaviour and growth, and relationship with coat type. J Agric Sci 102:141–147

    Google Scholar 

  • Forsman A (1995) Opposing fitness consequences of colour pattern in male and female snakes. J Evol Biol 8:53–70

    Google Scholar 

  • Forsman A (2000) Some like it hot: intra-population variation in behavioral thermoregulation in color-polymorphic pygmy grasshoppers. Evol Ecol 14:25–38

    Google Scholar 

  • Forsman A, Appelqvist S (1998) Visual predators impose correlational selection on prey color pattern and behavior. Behav Ecol 9:409–413

    Google Scholar 

  • Gomez D (2006) AVICOL, a program to analyse spectrometric data. Last updated Oct 2011. Free program available at http://sites.google.com/site/avicolprogram/ or from the author at dodogomezyahoo.fr

  • Greenberg CH, Neary DG, Harris LD (1994) Effect of high-intensity wildfire and silvicultural treatments on herpetofaunal communities in sand pine scrub. Conserv Biol 8:1047–1057

    Google Scholar 

  • Hagen DW, Gilbertson LG (1973) Selective predation and intensity of selection acting upon lateral plates of threespine sticklebacks. Heredity 30:273–287

    Google Scholar 

  • Hart NS, Vorobyev M (2005) Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors. J Comp Physiol A 191:381–392

    Google Scholar 

  • Harvey DS, Weatherhead PJ (2006) A test of the hierarchical model of habitat selection using eastern massasauga rattlesnakes (Sistrurus c. catenatus). Biol Conserv 130:206–216

    Google Scholar 

  • Hayter AJ (1984) A proof of the conjecture that the Tukey–Kramer multiple comparisons procedure is conservative. Ann Stat 12:61–75

    Google Scholar 

  • Hoekstra HE, Krenz JG, Nachman MW (2005) Local adaptation in the rock pocket mouse (Chaetodipus intermedius): natural selection and phylogenetic history of populations. Heredity (Edinb) 94:217–228

    CAS  Google Scholar 

  • Houde AE, Endler JA (1990) Correlated evolution of female mating preferences and male color patterns in the guppy Poecilia reticulata. Science 248:1405–1408

    CAS  PubMed  Google Scholar 

  • Huey RB, Hertz PE (1984) Effects of body size and slope on acceleration of a lizard (Stellio stellio). J Exp Biol 110:113–123

    Google Scholar 

  • Jormalainen V, Merilaita S, Tuomi J (1995) Differential predation on sexes affects colour polymorphism of the isopod Idotea baltica. Biol J Linn Soc 55:45–68

    Google Scholar 

  • Kaunert MD, Mcbrayer LD (2015) Population density of the Florida scrub lizard (Sceloporus woodi) in managed Florida scrub and longleaf pine sandhill habitats. Herpetol Conserv Biol 10:883–893

    Google Scholar 

  • Kettlewell HB (1973) The evolution of melanism: a study of a recurring necessity. Oxford University Press, Oxford

    Google Scholar 

  • Kramer CY (1956) Extension of multiple range tests to group means with unequal numbers of replications. Biometrics 12:307–310

    Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    PubMed  Google Scholar 

  • Langkilde T, Boronow KE (2010) Color as a signal: the relationship between coloration and morphology in male eastern fence lizards, Sceloporus undulatus. J Herpetol 44:261–271

    Google Scholar 

  • Lewis TH (1949) Dark coloration in the reptiles of the Tularosa Malpais, New Mexico. Copeia 1949:181–184

    Google Scholar 

  • Lind O, Kelber A (2011) The spatial tuning of achromatic and chromatic vision in budgerigars. J Vis 11(7):2. https://doi.org/10.1167/11.7.2

    Article  PubMed  Google Scholar 

  • Losos JB (1990) Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: an evolutionary analysis. Ecol Monogr 60:369–388

    Google Scholar 

  • Maan ME, Eshuis B, Haesler MP, Schneider MV, Van Alphen JJM, Seehausen O (2008) Color polymorphism and predation in a Lake Victoria cichlid fish. Copeia 2008(3):621–629

    Google Scholar 

  • Maia R, Eliason CM, Bitton PP, Doucet SM, Shawkey MD (2013) Pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol Evol 4(10):609–613

    Google Scholar 

  • Marshall KL, Stevens M (2014) Wall lizards display conspicuous signals to conspecifics and reduce detection by avian predators. Behav Ecol 25(6):1325–1337

    PubMed  PubMed Central  Google Scholar 

  • Marshall KL, Philpot KE, Damas-Moreira I, Stevens M (2015a) Intraspecific colour variation among lizards in distinct island environments enhances local camouflage. PLoS ONE 10:e0135241

    PubMed  PubMed Central  Google Scholar 

  • Marshall KL, Philpot KE, Stevens M (2015b) Conspicuous male coloration impairs survival against avian predators in aegean wall lizards, Podarcis erhardii. Ecol Evol 5:4115–4131

    PubMed  PubMed Central  Google Scholar 

  • Marshall KL, Philpot KE, Stevens M (2016) Microhabitat choice in island lizards enhances camouflage against avian predators. Sci Rep 6:19815

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martín J, López P (1995) Escape behaviour of juvenile Psammodromus algirus lizards: constraint of or compensation for limitations in body size? Behaviour 132:181–192

    Google Scholar 

  • McBrayer LD, Parker SE (2018) Variation in habitat management alters risk aversion behavior in lizards. Behav Ecol Sociobiol 72:149

    Google Scholar 

  • McGraw KJ, Hill GE (2004) Plumage color as a dynamic trait: carotenoid pigmentation of male house finches (Carpodacus mexicanus) fades during the breeding season. Can J Zool 82:734–738

    Google Scholar 

  • Merilaita S, Tuomi J, Jormalainen V (1999) Optimization of cryptic coloration in heterogeneous habitats. Biol J Linn Soc 67:151–161

    Google Scholar 

  • Miles DB, Sinervo B, Frankino WA (2000) Reproductive burden, locomotor performance, and the cost of reproduction in free ranging lizards. Evolution 54:1386–1395

    CAS  PubMed  Google Scholar 

  • Moodie GEE (1972) Predation, natural selection and adaptation in an unusual threespine stickleback. Heredity 28:155–167

    Google Scholar 

  • Murcia C (1995) Edge effects in fragmented forests: implications for conservation. Trends Ecol Evol 10:58–62

    CAS  PubMed  Google Scholar 

  • Myers RL, Ewel JJ eds (1990) Ecosystems of Florida. University of Central Florida Press, Orlando

    Google Scholar 

  • Neel LK, McBrayer LD (2018) Habitat management alters thermal opportunity. Funct Ecol. https://doi.org/10.1111/1365-2435.12123

    Article  Google Scholar 

  • Norris KS, Lowe CH (1964) Analysis of background color-matching in amphibians and reptiles. Ecology 45:565

    Google Scholar 

  • Orton RW, McElroy EJ, McBrayer LD (2018) Predation and cryptic coloration in a managed landscape. Evol Ecol 32:1–17

    Google Scholar 

  • Osorio D (1999) Colour vision in domestic chicks. Perception 28:22

    Google Scholar 

  • Osorio D, Miklosi A, Gonda Z (1999a) Visual ecology and perception of coloration patterns by domestic chicks. Evol Ecol 13:673–689

    Google Scholar 

  • Osorio D, Vorobyev M, Jones CD (1999b) Colour vision of domestic chicks. J Exp Biol 202:2951–2959

    CAS  PubMed  Google Scholar 

  • Pearson OP (1977) The effect of substrate and of skin color on thermoregulation of a lizard. Comp Biochem Physiol A Physiol 58:353–358

    Google Scholar 

  • Poulton EB (1890) The colors of animals, their meaning and use, especially considered in the case of insects. Kegan Paul, Trench, Trubner and Co., London

    Google Scholar 

  • Pröhl H, Ostrowski T (2011) Behavioural elements reflect phenotypic colour divergence in a poison frog. Evol Ecol 25:993–1015

    Google Scholar 

  • Rand AS (1964) Inverse relationship between temperature and shyness in the lizard Anolis lineatopus. Ecology 45:863

    Google Scholar 

  • Rice W (1989) The sequential Bonferroni test. Evolution 43:223–225

    PubMed  Google Scholar 

  • Rowell CHF (1971) The variable coloration of the Acridoid grasshoppers. Adv Insect Physiol 8:145–198

    Google Scholar 

  • Rohde K, Papiorek S, Lunau K (2013) Bumblebees (Bombus terrestris) and honeybees (Apis mellifera) prefer similar colours of higher spectral purity over trained colours. J Comp Physiol A 199:197–210. https://doi.org/10.1007/s00359-012-0783-5

    Article  Google Scholar 

  • Rosenblum EB (2006) Convergent evolution and divergent selection: lizards at the white sands ecotone. Am Nat 167:1–15

    PubMed  Google Scholar 

  • Salvador A, Veiga JP, Martin J, Lopez P, Abelenda M, Puerta M (1996) The cost of producing a sexual signal: testosterone increases the susceptibility of male lizards to ectoparasitic infestation. Behav Ecol 7:145–150

    Google Scholar 

  • Sherbrooke WC, Castrucci AMD, Hadley ME (1994) Temperature effects on in vitro skin darkening in the mountain spiny lizard, Sceloporus jarrovi—a thermoregulatory adaptation. Physiol Zool 67:659–672

    Google Scholar 

  • Shine R (1980) Costs of reproduction in reptiles. Oecologia 46:92–100

    PubMed  Google Scholar 

  • Shine R (2003) Effects of pregnancy on locomotor performance: an experimental study on lizards. Oecologia 136:450–456

    PubMed  Google Scholar 

  • Shine R (2006) Is increased maternal basking an adaptation or a pre-adaptation to viviparity in lizards? J Exp Zool Part A Comp Exp Biol 305A:524–535

    Google Scholar 

  • Sinervo B, Miles DB, Frankino WA, Klukowski M, Denardo DF (2000) Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Horm Behav 38:222–233

    CAS  PubMed  Google Scholar 

  • Skaar P, Richter A, Lederberg J (1957) Correlated selection for motility and sex-incompatibility in Escherichia coli k12. Proc Natl Acad Sci 43:329–333

    CAS  PubMed  Google Scholar 

  • Skelhorn J, Ruxton GD (2011) Mimicking multiple models: polyphenetic masqueraders gain additional benefits from crypsis. Behav Ecol 22:60–65

    Google Scholar 

  • Slatkin Montgomery (1984) Ecological causes of sexual dimorphism. Evolution 38:622–630

    PubMed  Google Scholar 

  • Stevens M, Parraga CA, Cuthill IC, Partridge JC, Troscianko TS (2007) Using digital photography to study animal coloration. Biol J Linn Soc 90:211–237

    Google Scholar 

  • Stiller RB, Mcbrayer LD (2013) The ontogeny of escape behavior, locomotor performance, and the hind limb in Sceloporus woodi. Zoology 116:175–181

    PubMed  Google Scholar 

  • Stoddard MC, Prum RO (2008) Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of new world buntings. Am Nat 171(6):755–776

    PubMed  Google Scholar 

  • Storfer A, Cross J, Rush V, Caruso J (1999) Adaptive coloration and gene flow as a constraint to local adaptation in the streamside salamander, Ambystoma barbouri. Evolution 53:889–898

    PubMed  Google Scholar 

  • Strugariu A, Zamfirescu SR (2011) Population characteristics of the adder (Vipera berus berus) in the Northern Romanian Carpathians with emphasis on colour polymorphism: is melanism always adaptive in vipers? Anim Biol 61:457–468

    Google Scholar 

  • Stuart-Fox D, Moussalli A (2009) Camouflage, communication and thermoregulation: lessons from colour changing organisms. Philos Trans R Soc Lond B Biol Sci 364:463–470

    PubMed  Google Scholar 

  • Stuart-Fox DM, Ord TJ (2004) Sexual selection, natural selection and the evolution of dimorphic coloration and ornamentation in agamid lizards. Proc R Soc B Biol Sci 271:2249–2255

    Google Scholar 

  • Stuart-Fox D, Moussalli A, Whiting MJ (2008) Predator-specific camouflage in chameleons. Biol Lett 4:326–329

    PubMed  PubMed Central  Google Scholar 

  • Thresher RE (1977) Eye ornamentation of Caribbean reef fishes. Ethology 43:152–158

    Google Scholar 

  • Tiebout HM, Anderson RA (1997) A comparison of corridors and intrinsic connectivity to promote dispersal in transient successional landscapes. Conserv Biol 11:620–627

    Google Scholar 

  • Tiebout HM, Anderson RA (2001) Mesocosm experiments on habitat choice by an endemic lizard: implications for timber management. J Herpetol 35:173–185

    Google Scholar 

  • Tukey J (1953) Multiple comparisons. J Am Stat Assoc 48:624–625

    Google Scholar 

  • Van Den Brink V, Dolivo V, Falourd X, Dreiss AN, Roulin A (2011) Melanic color-dependent antipredator behavior strategies in barn owl nestlings. Behav Ecol 23:473–480

    Google Scholar 

  • Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc B Biol Sci 265:351–358

    CAS  Google Scholar 

  • Wells BW (1928) Plant communities of the coastal plain of North Carolina and their successional relations. Ecology 9:230–242

    Google Scholar 

  • Wiens JJ, Kuczynski CA, Arif S, Reeder TW (2010) Phylogenetic relationships of phrynosomatid lizards based on nuclear and mitochondrial data, and a revised phylogeny for Sceloporus. Mol Phylogenet Evol 54:150–161

    PubMed  Google Scholar 

  • Willink B, Brenes-Mora E, Bolaños F, Pröhl H (2013) Not everything is black and white: color and behavioral variation reveal a continuum between cryptic and aposematic strategies in a polymorphic poison frog. Evolution 67:2783–2794

    PubMed  Google Scholar 

  • Wilson-Aggarwal JK, Troscianko JT, Stevens M, Spottiswoode CN (2016) Escape distance in ground-nesting birds differs with individual level of camouflage. Am Nat 188:231–239

    PubMed  Google Scholar 

  • Winters EA, Stevens M, Mitchell C, Blomberg PS, Blount JD (2014) Maternal effects and warning signal honesty in eggs and offspring of an aposematic ladybird beetle. Funct Ecol 28:1187–1196

    Google Scholar 

Download references

Acknowledgements

We owe a debt of gratitude to Christine Bedore’s sensory ecology laboratory at Georgia Southern University for aid with spectrophotometric measurements and analyses. We would also like to thank Lauren K. Neel and Chase T. Kinsey for their help in the field collecting lizards. Research in the Ocala National Forest was conducted with permission from the USDA Forest Service (USFS permit # SEM540). All applicable international, international and/or institutional guidelines for the care and use of animals were followed under protocol with the Institutional Animal Care and Use Committee (IACUC permit # I15011). Funding for this research was provided by a Graduate Student Professional Development grant from the College of Graduate Studies at Georgia Southern University, as well as a research grant through Sigma Xi’s GIAR.

Author information

Authors and Affiliations

Authors

Contributions

RWO and LDM conceived, designed, and performed this experiment. Additionally, RWO and LDM analyzed the data used for statistical analyses and wrote the manuscript.

Corresponding author

Correspondence to Lance D. McBrayer.

Additional information

Communicated by Jean-François Le Galliard.

Student highlight: This work evaluates a rarely tested hypothesis and demonstrates that predation intensity contributes to sexual dichromatism, risk avoidance, and microhabitat use.

Electronic supplementary material

Below is the link to the electronic supplementary material.

442_2018_4301_MOESM1_ESM.docx

Supplemental Figure 1. Comparisons between habitat type (F(1, 21) = 0.92; P = 0.3479) and sex (F(1, 21) = 3.77; P = 0.0663) of dorsal hue from the perspective of an avian predator taken from spectral data. (DOCX 103 kb)

442_2018_4301_MOESM2_ESM.docx

Supplemental Figure 2. Comparisons between habitat type (F(1,21) = 1.27; P = 0.274) and sex (F(1,21) = 1.32; P = 0.264) of dorsal saturation from the perspective of an avian predator taken from spectral data. (DOCX 140 kb)

442_2018_4301_MOESM3_ESM.docx

Supplemental Figure 3. Comparisons between habitat type (F(1,21) = 3.77; P = 0.00125) and sex (F(1, 21) = 2.00; 0.0573) of dorsal brightness from the perspective of an avian predator taken from spectral data. Note that spectral data of dorsal brightness mirror RGB data. (DOCX 135 kb)

442_2018_4301_MOESM4_ESM.docx

Supplemental Figure 4. Relationship between brightness from spectrometry data and brightness measured from calibrated photographs. Gray cloud surrounding line represents ± one SEM (ρ = 0.96, P < 0.001). (DOCX 1346 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Orton, R.W., McBrayer, L.D. Resolving tradeoffs among crypsis, escape behavior, and microhabitat use in sexually dichromatic species. Oecologia 189, 91–104 (2019). https://doi.org/10.1007/s00442-018-4301-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-018-4301-5

Keywords

Navigation