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Marine Biology

, 165:28 | Cite as

Color change in the Sargassum crab, Portunus sayi: response to diel illumination cycle and background albedo

Original paper

Abstract

Floating mats of Sargassum macroalgae provide a model system for studying multiple aspects of animal coloration. The endemic crab Portunus sayi has heterogeneous yellow and brown patterning, which matches its algal background. We show that by fluctuating the chromatophores underneath its transparent carapace, the crab can alter its coloration within hours in response to diel variability in the ambient light field and to changes in background reflectance. Held in a naturalistic illumination and temperature regime, P. sayi displayed a distinct diel cycle of coloration, being pale at night and darker during the day. Individuals under constant illumination showed a modified cycle, retaining their nocturnal shading but becoming significantly paler during day time. On monochromatic black, grey, and white surfaces, crabs showed an ability to change coloration in response to their backgrounds, as integrated reflectance (ΣR) of crabs generally followed background albedo. This study expands on earlier work which revealed that P. sayi utilizes a distinct camouflage strategy from other cryptic Sargassum crabs to achieve background color matching in the view of predators. Dynamic color change in this species may play roles including photoprotection and enhancing camouflage in a unique marine environment.

Notes

Acknowledgements

We wish to thank the staff of Keys Marine Lab in providing facilities, vessel support, and collection assistance, as well as an anonymous reviewer for suggestions to improve an earlier version of this manuscript.

Funding

This work was funded by the Office of Naval Research Multi-University Research Initiative (N000140911054), and by a pre-doctoral award from the University of Connecticut Department of Marine Sciences.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human/animal rights statement

All applicable national, state, and University of Connecticut ethical standards regarding the use of animals were observed. Only invertebrates were used in this study. All care was taken to ensure humane treatment of animals.

Supplementary material

227_2018_3287_MOESM1_ESM.pdf (426 kb)
Supplementary material 1 (PDF 426 kb)

References

  1. Abramowitz AA (1935) Color changes in cancroid crabs of Bermuda. Proc Natl Acad Sci USA 21:677CrossRefGoogle Scholar
  2. Abramowitz AA (1937) The chromatophorotropic hormone of the Crustacea: standardization, properties and physiology of the eye-stalk glands. Biol Bull 72:344.  https://doi.org/10.2307/1537694 CrossRefGoogle Scholar
  3. Baldwin J, Johnsen S (2012) The male blue crab, Callinectes sapidus, uses both chromatic and achromatic cues during mate choice. J Exp Biol 215:1184–1191.  https://doi.org/10.1242/jeb.067512 CrossRefGoogle Scholar
  4. Ballance L, Pitman R (1999) S34. 4: foraging ecology of tropical seabirds. In: Proceedings of the 22nd international ornithological congress, Durban. Citeseer, pp 2057–2071Google Scholar
  5. Barnwell FH (1968) Comparative aspects of the chromatophoric responses to light and temperature in fiddler crabs of the genus Uca. Biol Bull 134:221.  https://doi.org/10.2307/1539598 CrossRefGoogle Scholar
  6. Brooks WR, Hutchinson KA, Tolbert MG (2007) Pelagic Sargassum mediates predation among symbiotic fishes and shrimps. Gulf Mex Sci 2:144–152Google Scholar
  7. Brown FA (1933) The controlling mechanism of chromatophores in Palaemonetes. Proc Natl Acad Sci 19:327–329CrossRefGoogle Scholar
  8. Brown FA (1939) The coloration and color changes of the gulf-weed shrimp, Latreutes fucorum. Am Nat 73:564–568CrossRefGoogle Scholar
  9. Brown FA (1950) Studies on the physiology of Uca red chromatophores. Biol Bull 98:218.  https://doi.org/10.2307/1538669 CrossRefGoogle Scholar
  10. Brown FA, Sandeen MI (1948) Responses of the chromatophores of the fiddler crab, Uca, to light and temperature. Physiol Zool 21:361–371CrossRefGoogle Scholar
  11. Brown FA, Fingerman M, Sandeen MI, Webb HM (1953) Persistent diurnal and tidal rhythms of color change in the fiddler crab, Uca pugnax. J Exp Zool 123:29–60CrossRefGoogle Scholar
  12. Butler JN, Morris BF, Cadwallader J, Stoner AW (1983) Studies of Sargassum and the Sargassum community, vol 22. Bermuda Biological Station Research, Bermuda, 307pGoogle Scholar
  13. Chace FA (1951) The oceanic crabs of the genera Planes and Pachygrapsus. Proc US Natl Mus 101:65–103CrossRefGoogle Scholar
  14. Coohill TP, Fingerman M (1975) Relative effectiveness of ultraviolet and visible light in eliciting pigment dispersion in melanophores of the fiddler crab, Uca pugilator, through the secondary response. Physiol Zool 48:57–63CrossRefGoogle Scholar
  15. Coohill TP, Fingerman M (1976) Comparison of the effects of illumination on the melanophores of intact and eyestalkless fiddler crabs, Uca pugilator, and inhibition of the primary response by cytochalasin B. Experientia 32:569–570CrossRefGoogle Scholar
  16. Coohill TP, Bartell CK, Fingerman M (1970) Relative effectiveness of ultraviolet and visible light in eliciting pigment dispersion directly in melanophores of the fiddler crab, Uca pugilator. Physiol Zool 43:232–239CrossRefGoogle Scholar
  17. Coston-Clements L, Settle LR, Hoss DE, Cross FA (1991) Utilization of the Sargassum habitat by marine invertebrates and vertebrates—a review. NOAA Tech Mem NMFS-SEFSC-296Google Scholar
  18. Crane J (1944) On the color changes of fiddler crabs in the field. Zoologica 29:161–168Google Scholar
  19. Crozier WJ (1918) Note on the coloration of Planes minutus. Am Nat 52:262–263CrossRefGoogle Scholar
  20. Darnell MZ (2012) Ecological physiology of the circadian pigmentation rhythm in the fiddler crab Uca panacea. J Exp Mar Biol Ecol 426–427:39–47.  https://doi.org/10.1016/j.jembe.2012.05.014 CrossRefGoogle Scholar
  21. De Robertis A (2002) Size-dependent visual predation risk and the timing of vertical migration: an optimization model. Limnol Oceanogr 47:925–933CrossRefGoogle Scholar
  22. Detto T (2007) The fiddler crab Uca mjoebergi uses colour vision in mate choice. Proc R Soc B Biol Sci 274:2785–2790.  https://doi.org/10.1098/rspb.2007.1059 CrossRefGoogle Scholar
  23. Detto T, Backwell PR, Hemmi JM, Zeil J (2006) Visually mediated species and neighbour recognition in fiddler crabs (Uca mjoebergi and Uca capricornis). Proc R Soc B Biol Sci 273:1661–1666.  https://doi.org/10.1098/rspb.2006.3503 CrossRefGoogle Scholar
  24. Detto T, Hemmi JM, Backwell PRY (2008) Colouration and colour changes of the fiddler crab, Uca capricornis: a descriptive study. PLoS One 3:e1629.  https://doi.org/10.1371/journal.pone.0001629 CrossRefGoogle Scholar
  25. Dierssen HM, Chlus A, Russell B (2015) Hyperspectral discrimination of floating mats of seagrass wrack and the macroalgae Sargassum in coastal waters of Greater Florida Bay using airborne remote sensing. Remote Sens Environ 167:247–258.  https://doi.org/10.1016/j.rse.2015.01.027 CrossRefGoogle Scholar
  26. Emery CJ (1984) The ecological impact of near ultraviolet radiation on Daphnia pulex. Master’s, University of WindsorGoogle Scholar
  27. Endler JA (1978) A predator’s view of animal colour patterns. Evol Biol 11:319–364Google Scholar
  28. Fingerman M (1955) Persistent daily and tidal rhythms of color change in Callinectes sapidus. Biol Bull 109:255–264CrossRefGoogle Scholar
  29. Fingerman M (1956a) Phase difference in the tidal rhythms of color change of two species of fiddler crab. Biol Bull 110:274.  https://doi.org/10.2307/1538833 CrossRefGoogle Scholar
  30. Fingerman M (1956b) Physiology of the black and red chromatophores of Callinectes sapidus. J Exp Zool 133:87–105CrossRefGoogle Scholar
  31. Fingerman M (1963) The control of chromatophores. Macmillan, New YorkGoogle Scholar
  32. Fingerman M (1965) Chromatophores. Physiol Rev 45:296–339CrossRefGoogle Scholar
  33. Fingerman M, Tinkle DW (1956) Responses of the white chromatophores of two species of prawns (Palaemonetes) to light and temperature. Biol Bull 110:144–152CrossRefGoogle Scholar
  34. Fingerman M, Lowe ME, Mobberly WC (1958) Environmental factors involved in setting the phases of tidal rhythm of color change in the fiddler crabs Uca pugilator and Uca minax. Limnol Oceanogr 3:271–282CrossRefGoogle Scholar
  35. Fingerman M, Nagabhushanam R, Philpott L (1961) Physiology of the melanophores in the crab Sesarma reticulatum. Biol Bull 120:337–347CrossRefGoogle Scholar
  36. Gouveia GR, Lopes TM, Neves CA, Nery LEM, Trindade GS (2004) Ultraviolet radiation induces dose-dependent pigment dispersion in crustacean chromatophores. Pigment Cell Res 17:545–548CrossRefGoogle Scholar
  37. Granato FC, Tironi TS, Maciel FE, Rosa CE, Vargas MA, Nery LEM (2004) Circadian rhythm of pigment migration induced by chromatrophorotropins in melanophores of the crab Chasmagnathus granulata. Comp Biochem Physiol A Mol Integr Physiol 138:313–319.  https://doi.org/10.1016/j.cbpb.2004.04.009 CrossRefGoogle Scholar
  38. Green JP (1964a) Morphological color change in the fiddler crab, Uca pugnax (S. I. Smith). Biol Bull 127:239.  https://doi.org/10.2307/1539223 CrossRefGoogle Scholar
  39. Green JP (1964b) Morphological color change in the Hawaiian ghost crab, Ocypode ceratophthalma (Pallas). Biol Bull 126:407.  https://doi.org/10.2307/1539309 CrossRefGoogle Scholar
  40. Hacker SD, Madin LP (1991) Why habitat architecture and color are important to shrimps living in pelagic Sargassum: use of camouflage and plant-part mimicry. Mar Ecol Prog Ser 70:143–155CrossRefGoogle Scholar
  41. Haney JC (1986) Seabird patchiness in tropical oceanic waters: the influence of Sargassum “reefs”. Auk 103:141–151Google Scholar
  42. Hemmi JM, Marshall J, Pix W, Vorobyev M, Zeil J (2006) The variable colours of the fiddler crab Uca vomeris and their relation to background and predation. J Exp Biol 209:4140–4153.  https://doi.org/10.1242/jeb.02483 CrossRefGoogle Scholar
  43. Herreid CF, Mooney SM (1984) Color change in exercising crabs: evidence for a hormone. J Comp Physiol B 154:207–212CrossRefGoogle Scholar
  44. Hervey R (2011) Hervey RV, US DOC, NOAA, NWS, National Data Buoy Center (2011) Meteorological and oceanographic data collected from the National Data Buoy Center Coastal-Marine Automated Network (C-MAN) and moored (weather) buoys during 2011-06 (NODC accession 0074384). version 2.2. National Oceanographic Data Center, NOAA. DatasetGoogle Scholar
  45. Hitchcock HB (1941) The coloration and color changes of the gulf-weed crab, Planes minutus. Biol Bull 80:26–30CrossRefGoogle Scholar
  46. Horst MN, Freeman JA (1993) The crustacean integument: morphology and biochemistry. CRC Press, Boca RatonGoogle Scholar
  47. Hultgren KM, Mittelstaedt H (2015) Color change in a marine isopod is adaptive in reducing predation. Curr Zool 6:739–748CrossRefGoogle Scholar
  48. Hultgren KM, Stachowicz JJ (2008) Alternative camouflage strategies mediate predation risk among closely related co-occurring kelp crabs. Oecologia 155:519–528.  https://doi.org/10.1007/s00442-007-0926-5 CrossRefGoogle Scholar
  49. Iampietro PJ (1999) Distribution, diet, and pigmentation of the northern kelp crab, Pugettia producta (Randall) in central California kelp forests. Master’s, California State University, StanislausGoogle Scholar
  50. Jensen GC, Egnotovich MS (2015) A whiter shade of male: color background matching as a function of size and sex in the yellow shore crab Hemigrapsus oregonensis (Dana, 1851). Curr Zool 61:729–738CrossRefGoogle Scholar
  51. Jobe CF, Brooks WR (2009) Habitat selection and host location by symbiotic shrimps associated with Sargassum communities: the role of chemical and visual cues. Symbiosis 49:77–85.  https://doi.org/10.1007/s13199-009-0017-y CrossRefGoogle Scholar
  52. Kolwalkar DG, Rangnekar PV (1979) Morphological color change in the marine crab Portunus pelagicus. J Bombay Nat Hist Soc 76:540–543Google Scholar
  53. Korínek V, Frey DG (eds) (2013) Biology of Cladocera. In: Proceedings of the second international symposium on Cladocera, Tatranska Lomnica, Czechoslovakia, 13–20, September 1989. Springer, NetherlandsGoogle Scholar
  54. Kronstadt SM, Darnell MZ, Munguia P (2013) Background and temperature effects on Uca panacea color change. Mar Biol 160:1373–1381.  https://doi.org/10.1007/s00227-013-2189-5 CrossRefGoogle Scholar
  55. Morris BF, Mogelberg DD (1973) Identification manual to the pelagic Sargassum fauna. Bermuda Biological Station for Research, St Georges, p 22Google Scholar
  56. Munguia P, Levinton JS, Silbiger NJ (2013) Latitudinal differences in thermoregulatory color change in Uca pugilator. J Exp Mar Biol Ecol 440:8–14.  https://doi.org/10.1016/j.jembe.2012.11.010 CrossRefGoogle Scholar
  57. Oro D, Martínez-Abraín A (2005) Ecology and behavior of seabirds. In: Duarte CM, Lota A (eds) Marine ecology, encyclopedia of life support systems (EOLSS). Eolss Publishers-UNESCO, OxfordGoogle Scholar
  58. Powell BL (1962) The responses of the chromatophores of Carcinus maenas (L., 1758) to light and temperature. Crustaceana 4:93–102CrossRefGoogle Scholar
  59. Rooker JR, Turner JP, Holt SA (2006) Trophic ecology of Sargassum-associated fishes in the Gulf of Mexico determined from stable isotopes and fatty acids. Mar Ecol Prog Ser 313:249–259CrossRefGoogle Scholar
  60. Russell BJ, Dierssen HM (2015) Use of hyperspectral imagery to assess cryptic color matching in Sargassum associated crabs. PLoS One 10:e0136260CrossRefGoogle Scholar
  61. Russell B, Dierssen H, LaJeunesse T, Hoadley K, Warner M, Kemp D, Bateman T (2016) Spectral reflectance of Palauan reef-building coral with different symbionts in response to elevated temperature. Remote Sens 8:164.  https://doi.org/10.3390/rs8030164 CrossRefGoogle Scholar
  62. Shih H-T, Mok H-K, Chang H-W, Lee S-C (1999) Morphology of Uca formosensis (Rathbun, 1921) (Crustacea: Decapoda: Ocypodidae), an endemic fiddler crab from Taiwan, with notes on its ecology. Zool Stud Taipei 38:164–177Google Scholar
  63. Silbiger N, Munguia P (2008) Carapace color change in Uca pugilator as a response to temperature. J Exp Mar Biol Ecol 355:41–46.  https://doi.org/10.1016/j.jembe.2007.11.014 CrossRefGoogle Scholar
  64. Stachowicz JJ, Lindquist N (1997) Chemical defense among hydroids on pelagic Sargassum: predator deterrence and absorption of solar UV radiation by secondary metabolites. Mar Ecol Prog Ser 155:115–126CrossRefGoogle Scholar
  65. Stachowicz JJ, Lindquist N (2000) Hydroid defenses against predators: the importance of secondary metabolites versus nematocysts. Oecologia 124:280–288CrossRefGoogle Scholar
  66. Stevens M (2016) Color change, phenotypic plasticity, and camouflage. Front Ecol Evol.  https://doi.org/10.3389/fevo.2016.00051 Google Scholar
  67. Stevens M, Merilaita S (eds) (2011) Animal camouflage: mechanisms and function. Cambridge University Press, CambridgeGoogle Scholar
  68. Stevens M, Rong CP, Todd PA (2013) Colour change and camouflage in the horned ghost crab Ocypode ceratophthalmus. Biol J Linn Soc 109:257–270CrossRefGoogle Scholar
  69. Stevens M, Lown AE, Wood LE (2014a) Camouflage and individual variation in shore crabs (Carcinus maenas) from different habitats. PLoS One 9:e115586.  https://doi.org/10.1371/journal.pone.0115586 CrossRefGoogle Scholar
  70. Stevens M, Lown AE, Wood LE (2014b) Color change and camouflage in juvenile shore crabs Carcinus maenas. Front Ecol Evol.  https://doi.org/10.3389/fevo.2014.00014 Google Scholar
  71. Thurman CL (1988) Rhythmic physiological color change in Crustacea: a review. Comp Biochem Physiol Part C Comp Pharmacol 91:171–185.  https://doi.org/10.1016/0742-8413(88)90184-3 CrossRefGoogle Scholar
  72. Thurman CL (1990) Adaptive coloration in Texas fiddler crabs (Uca). In: Wickstein M (ed) Adaptive coloration in invertebrates. Texas A&M University Press, Texas, pp 109–126Google Scholar
  73. Umbers KDL, Fabricant SA, Gawryszewski FM, Seago AE, Herberstein ME (2014) Reversible colour change in Arthropoda: Arthropod colour change. Biol Rev 89:820–848.  https://doi.org/10.1111/brv.12079 CrossRefGoogle Scholar
  74. Welsh JH (1938) Diurnal rhythms. Q Rev Biol 13:123–139CrossRefGoogle Scholar
  75. White TE, Dalrymple RL, Noble DWA, O’Hanlon JC, Zurek DB, Umbers KDL (2015) Reproducible research in the study of biological coloration. Anim Behav 106:51–57.  https://doi.org/10.1016/j.anbehav.2015.05.007 CrossRefGoogle Scholar
  76. Wilkens JL, Fingerman M (1965) Heat tolerance and temperature relationships of the fiddler crab, Uca pugilator, with reference to body coloration. Biol Bull 128:133–141CrossRefGoogle Scholar
  77. Zeil J, Hofmann M (2001) Signals from “crabworld”: cuticular reflections in a fiddler crab colony. J Exp Biol 204:2561–2569Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Marine ScienceUniversity of ConnecticutGrotonUSA
  2. 2.Department of GeographyUniversity of ConnecticutStorrsUSA

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