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Marine Biology

, 165:26 | Cite as

Geographic variation in thermal tolerance and morphology in a fiddler crab sister-species pair

  • M. Zachary Darnell
  • Kelly M. Darnell
Original paper

Abstract

Temperature-adaptive physiological and morphological variation plays a large role in determining species’ geographic ranges and responses to climate change. We examined critical thermal maximum (CTmax) and two thermally relevant morphological traits across multiple populations of two species of fiddler crabs, Leptuca panacea and Leptuca pugilator, spanning a latitudinal thermal gradient from South Padre Island, Texas (26.0850°N) to Long Island, New York (40.9357°N). CTmax was measured on crabs collected in 2015, while morphology was measured on crabs collected between 2012 and 2015. CTmax differed among populations and was greatest in populations experiencing a warmer thermal regime. CTmax did not differ between the two species at the site where they overlapped and experienced identical thermal regimes. These results indicate that large-scale (latitudinal) thermal gradients can shape thermally relevant physiological characteristics. Geographic patterns of the two morphological measurements (carapace width and relative claw length) were not consistent between the two species, and often ran counter to our expectations. Thermoregulatory ability is optimized by large body size and a large claw, and we thus hypothesized that carapace width and claw length would be positively correlated with environmental temperature. Carapace width exhibited a positive relationship with environmental temperature in L. panacea, but conversely exhibited a negative relationship in L. pugilator. Claw length was negatively correlated with temperature in both species. These morphological results highlight the need to consider the multiple, presumed interacting selective pressures shaping morphological variation among populations and species.

Notes

Acknowledgements

The authors thank J. Levinton for providing lab space, assisting with fiddler crab collections in New York, and for providing valuable feedback on this manuscript; P. Munguia for providing lab space in Texas; and S. Hicks, S. Bergeron, and S. Rehage for technical assistance. This study benefited from early discussions with R.S. Greenberg on temperature-driven variation in fiddler crab claw size and sparrow bill size. Partial funding for this research was provided by the Nicholls State University Research Council.

Compliance with ethical standards

Human/animal rights statement

All animals used in the study were collected, treated, and handled following established protocols. As only invertebrates were used in experiments, IACUC approvals were not required.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

227_2017_3282_MOESM1_ESM.pdf (90 kb)
Supplementary material 1 (PDF 90 kb)
227_2017_3282_MOESM2_ESM.pdf (85 kb)
Supplementary material 2 (PDF 85 kb)

References

  1. Addo-Bediako A, Chown SL, Gaston KJ (2000) Thermal tolerance, climatic variability and latitude. Proc R Soc B 267:739–745CrossRefGoogle Scholar
  2. Allen BJ (2007) Costs of sexual selection in the sand fiddler crab, Uca pugilator. Dissertation, Stony Brook University, New YorkGoogle Scholar
  3. Allen BJ, Levinton JS (2007) Costs of bearing a sexually selected ornamental weapon in a fiddler crab. Funct Ecol 21:154–161CrossRefGoogle Scholar
  4. Allen BJ, Levinton JS (2014) Sexual selection and the physiological consequences of habitat choice by a fiddler crab. Oecologia 176:25–34CrossRefGoogle Scholar
  5. Allen BJ, Rodgers B, Tuan Y, Levinton JS (2012) Size-dependent temperature and desiccation constraints on performance capacity: implications for sexual selection in a fiddler crab. J Exp Mar Biol Ecol 438:93–99CrossRefGoogle Scholar
  6. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, OxfordCrossRefGoogle Scholar
  7. Araújo MB, Ferri-Yáñez F, Bozinovic F, Marquet PA, Valladares F, Chown SL (2013) Heat freezes niche evolution. Ecol Lett 16:1206–1219CrossRefGoogle Scholar
  8. Atkinson D (1994) Temperature and organism size—a biological law for ectotherms. Adv Ecol Res 25:1–58CrossRefGoogle Scholar
  9. Backwell PRY, Matsumasa M, Double M, Roberts A, Murai M, Keogh JS, Jennions MD (2007) What are the consequences of being left-clawed in a predominantly right-clawed fiddler crab? Proc R Soc B 274:2723–2729CrossRefGoogle Scholar
  10. Bakken GS, Angilletta MJ (2014) How to avoid errors when quantifying thermal environments. Funct Ecol 28:96–107CrossRefGoogle Scholar
  11. Barnwell FH (1966) Daily and tidal patterns of activity in individual fiddler crab (Genus Uca) from the Woods Hole Region. Biol Bull 130:1–17CrossRefGoogle Scholar
  12. Barnwell FH, Thurman CL (1984) Taxonomy and biogeography of the fiddler crabs (Ocypodidae: Genus Uca) of the Atlantic and Gulf coasts of eastern North America. Zool J Linn Soc 81:23–87CrossRefGoogle Scholar
  13. Blackburn TM, Gaston KJ, Loder N (1999) Geographic gradients in body size: a clarification of Bergmann’s rule. Divers Distrib 5:165–174CrossRefGoogle Scholar
  14. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  15. Callander S, Jennions MD, Backwell PRY (2012) The effect of claw size and wave rate on female choice in a fiddler crab. J Ethol 30:151–155CrossRefGoogle Scholar
  16. Castaneda LE, Lardies MA, Bozinovic F (2004) Adaptive latitudinal shifts in the thermal physiology of a terrestrial isopod. Evol Ecol Res 6:579–593Google Scholar
  17. Christy JH (1978) Adaptive significance of reproductive cycles in the fiddler crab Uca pugilator: a hypothesis. Science 199:453–455CrossRefGoogle Scholar
  18. Crane J (1975) Fiddler crabs of the world (Ocypodidae: genus Uca). Princeton University Press, PrincetonGoogle Scholar
  19. Darnell MZ, Munguia P (2011) Thermoregulation as an alternate function of the sexually dimorphic fiddler crab claw. Am Nat 178:419–428CrossRefGoogle Scholar
  20. Darnell MZ, Fowler KK, Munguia P (2013) Sex-specific thermal constraints on fiddler crab behavior. Behav Ecol 24:997–1003CrossRefGoogle Scholar
  21. Darnell MZ, Nicholson HS, Munguia P (2015) Thermal ecology of the fiddler crab Uca panacea: thermal constraints and organismal responses. J Therm Biol 52:157–165CrossRefGoogle Scholar
  22. Dayan T, Simberloff D (1994) Character displacement, sexual dimorphism, and morphological variation among British and Irish mustelids. Ecology 75:1063–1073CrossRefGoogle Scholar
  23. Edney EB (1961) The water and heat relationships of fiddler crabs (Uca spp.). Trans R Soc S Afr 36:71–91CrossRefGoogle Scholar
  24. Eggert A, Burger EM, Breeman AM (2003) Ecotypic differentiation in thermal traits in the tropical to warm-temperate green macrophyte Valonia utricularis. Bot Mar 46:69–81CrossRefGoogle Scholar
  25. Eklov P, Svanback R (2006) Predation risk influences adaptive morphological variation in fish populations. Am Nat 167:440–452CrossRefGoogle Scholar
  26. Faria SC, Faleiros RO, Brayner FA, Alves LC, Bianchini A, Romero C, Buranelli RC, Mantelatto FL, McNamara JC (2017) Macroevolution of thermal tolerance in intertidal crabs from Neotropical provinces: a phylogenetic comparative evaluation of critical limits. Ecol Evol 7:3167–3176CrossRefGoogle Scholar
  27. Gaston KJ, Chown SL (1999) Elevation and climatic tolerance: a test using dung beetles. Oikos 86:584–590CrossRefGoogle Scholar
  28. Gerald GW, Thiesen KE (2014) Locomotor hindrance of carrying an enlarged sexually selected structure on inclines for male fiddler crabs. J Zool 294:129–138CrossRefGoogle Scholar
  29. Gilchrist GW (1990) The consequences of sexual dimorphism in body size for butterfly flight and thermoregulation. Funct Ecol 4:475–487CrossRefGoogle Scholar
  30. Gouveia SF, Hortal J, Tejedo M, Duarte H, Cassemiro FAS, Navas CA, Diniz-Filho JAF (2014) Climatic niche at physiological and macroecological scales: the thermal tolerance–geographical range interface and niche dimensionality. Global Ecol Biogeogr 23:446–456CrossRefGoogle Scholar
  31. Greenberg R, Danner RM (2013) Climate, ecological release and bill dimorphism in an island songbird. Biol Lett 9:20130118CrossRefGoogle Scholar
  32. Helmuth BST (1998) Intertidal mussel microclimates: predicting the body temperature of a sessile invertebrate. Ecol Monogr 68:51–74CrossRefGoogle Scholar
  33. Helmuth B, Harley CDG, Halpin PM, O’Donnell M, Hofmann GE, Blanchette CA (2002) Climate change and latitudinal patterns of intertidal thermal stress. Science 298:1015–1017CrossRefGoogle Scholar
  34. Hertz PE, Huey RB, Stevenson RD (1993) Evaluating temperature regulation by field-active ectotherms: the fallacy of the inappropriate question. Am Nat 142:796–818CrossRefGoogle Scholar
  35. Hjelm J, Persson L, Christensen B (2000) Growth, morphological variation and ontogenetic niche shifts in perch (Perca fluviatilis) in relation to resource availability. Oecologia 122:190–199CrossRefGoogle Scholar
  36. Hochachka PW, Somero GN (1984) Biochemical adaptation. Princeton University Press, PrincetonCrossRefGoogle Scholar
  37. Huey RB, Berrigan D (2001) Temperature, demography, and ectotherm fitness. Am Nat 158:204–210CrossRefGoogle Scholar
  38. Huey RB, Stevenson RD (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am Zool 19:357–366CrossRefGoogle Scholar
  39. Hyatt GW, Salmon M (1978) Combat in fiddler crabs Uca pugilator and Uca pugnax: quantitative analysis. Behaviour 65:182–211CrossRefGoogle Scholar
  40. Kearney M, Shine R, Porter WP (2009) The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. Proc Natl Acad Sci USA 106:3835–3840CrossRefGoogle Scholar
  41. Klok CJ, Chown SL (2005) Inertia in physiological traits: Embryonopsis halticella caterpillars (Yponomeutidae) across the Antarctic Polar Frontal Zone. J Insect Physiol 51:87–97CrossRefGoogle Scholar
  42. Levinton J, Lord S, Higeshide Y (2015) Are crabs stressed for water on a hot sand flat? Water loss and field water state of two species of intertidal fiddler crabs. J Exp Mar Biol Ecol 469:57–62CrossRefGoogle Scholar
  43. Lonsdale DJ, Levinton JS (1985) Latitudinal differentiation in copepod growth: an adaptation to temperature. Ecology 66:1397–1407CrossRefGoogle Scholar
  44. Luther D, Greenberg R (2014) Habitat type and ambient temperature contribute to bill morphology. Ecol Evol 4:699–705CrossRefGoogle Scholar
  45. Lutterschmidt WI, Hutchison VH (1997) The critical thermal maximum: data to support the onset of spasms as the definitive end point. Can J Zool 75:1553–1560CrossRefGoogle Scholar
  46. Lynch M, Gabriel W (1987) Environmental tolerance. Am Nat 129:283–303CrossRefGoogle Scholar
  47. McLain DK, Logue J, Pratt AE, McBrayer LD (2015) Claw-pinching force of sand fiddler crabs in relation to activity and the lunar cycle. J Exp Mar Biol Ecol 471:190–197CrossRefGoogle Scholar
  48. Miller DC, Vernberg FJ (1968) Some thermal requirements of fiddler crabs of the temperate and tropical zones and their influence on geographic distribution. Am Zool 8:459–469CrossRefGoogle Scholar
  49. Munguia P, Levinton JS, Silbiger NJ (2013) Latitudinal differences in thermoregulatory color change in Uca pugilator. J Exp Mar Biol Ecol 440:8–14CrossRefGoogle Scholar
  50. Munguia P, Backwell PRY, Darnell MZ (2017) Thermal constraints on microhabitat selection and mating opportunities. Anim Behav 123:259–265CrossRefGoogle Scholar
  51. Pope DS (2000a) Testing function of fiddler crab claw waving by manipulating social context. Behav Ecol Sociobiol 47:432–437CrossRefGoogle Scholar
  52. Pope DS (2000b) Video playback experiments testing the function of claw waving in the sand fiddler crab. Behaviour 137:1349–1360CrossRefGoogle Scholar
  53. Powers LW, Cole JF (1976) Temperature variation in fiddler crab microhabitats. J Exp Mar Biol Ecol 21:141–157CrossRefGoogle Scholar
  54. PRISM Climate Group (2012) Oregon State University. http://prism.oregonstate.edu. Accessed 16 Aug 2017
  55. Roberts B, Espinosa J, Heilman K, Brodie R (2015) Southern males are bigger but northern males are more honest: latitudinal trends in male claw traits of the fiddler crab Uca pugnax. Integr Comp Biol 55:E321Google Scholar
  56. Rosenberg MS (2001) The systematics and taxonomy of fiddler crabs: a phylogeny of the genus Uca. J Crust Biol 21:839–869CrossRefGoogle Scholar
  57. Sanford E, Holzman SB, Haney RA, Rand DM, Bertness MD (2006) Larval tolerance, gene flow, and the northern geographic range limit of fiddler crabs. Ecology 87:2882–2894CrossRefGoogle Scholar
  58. Shepherd BL, Prange HD, Moczek AP (2008) Some like it hot: body and weapon size affect thermoregulation in horned beetles. J Insect Physiol 54:604–611CrossRefGoogle Scholar
  59. Shih HT, Ng PKL, Davie PJF, Schubart CD, Turkay M, Naderloo R, Jones D, Liu MY (2016) Systematics of the family Ocypodidae Rafinesque, 1815 (Crustacea: Brachyura), based on phylogenetic relationships, with a reorganization of subfamily rankings and a review of the taxonomic status of Uca Leach, 1814, sensu lato and its subgenera. Raffles Bull Zool 64:139–175Google Scholar
  60. Smith WK, Miller PC (1973) The thermal ecology of two South Florida fiddler crabs: Uca rapax Smith and U. pugilator Bosc. Physiol Zool 46:186–207CrossRefGoogle Scholar
  61. Somero G (2005) Linking biogeography to physiology: evolutionary and acclimatory adjustments of thermal limits. Front Zool 2:1CrossRefGoogle Scholar
  62. Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J Exp Biol 213:912–920CrossRefGoogle Scholar
  63. Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65CrossRefGoogle Scholar
  64. Sturmbauer C, Levinton JS, Christy J (1996) Molecular phylogeny of fiddler crabs: test of the hypothesis of increasing behavioral complexity in evolution. Proc Natl Acad Sci 93:10855–10857CrossRefGoogle Scholar
  65. Sunday JM, Bates AE, Dulvy NK (2011) Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc B 278:1823–1830CrossRefGoogle Scholar
  66. Sunday JM, Bates AE, Dulvy NK (2012) Thermal tolerance and the global redistribution of animals. Nat Clim Change 2:686–690CrossRefGoogle Scholar
  67. Sunday JM, Bates AE, Kearney MR, Colwell RK, Dulvy NK, Longino JT, Huey RB (2014) Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc Natl Acad Sci 111:5610–5615CrossRefGoogle Scholar
  68. Thurman CL (2004) Unraveling the ecological significance of endogenous rhythms in intertidal crabs. Biol Rhythm Res 35:43–67CrossRefGoogle Scholar
  69. Vernberg FJ (1959) Studies on the physiological variation between tropical and temperate zone fiddler crabs of the genus Uca. II. Oxygen consumption of whole organisms. Biol Bull 117:163–184CrossRefGoogle Scholar
  70. Vernberg FJ, Costlow JD Jr (1966) Studies on the physiological variation between tropical and temperate-zone fiddler crabs of the genus Uca. IV. Oxygen consumption of larvae and young crabs reared in the laboratory. Physiol Zool 39:36–52CrossRefGoogle Scholar
  71. Vernberg FJ, Tashian RE (1959) Studies on the physiological variation between tropical and temperate zone fiddler crabs of the genus Uca. I. Thermal death limits. Ecology 40:589–593CrossRefGoogle Scholar
  72. Vernberg FJ, Vernberg WB (1966a) Studies on the physiological variation between tropical and temperate zone fiddler crabs of the genus Uca. VII. Metabolic-temperature acclimation responses in southern hemisphere crabs. Comp Biochem Phys 19:489–524CrossRefGoogle Scholar
  73. Vernberg FJ, Vernberg WB (1966b) Studies on the physiological variation between tropical and temperate zone fiddler crabs of the genus Uca. VI. The rate of metabolic adaptation to temperature in tissues. J Elisha Mitchell Sci Soc 82:30–34Google Scholar
  74. Vernberg WB, Vernberg FJ (1966c) Studies on the physiological variation between tropical and temperate zone fiddler crabs of the genus Uca. V. Effect of temperature on tissue respiration. Comp Biochem Phys 17:363–374CrossRefGoogle Scholar
  75. Vernberg FJ, Vernberg WB (1967) Thermal lethal limits of southern hemisphere Uca crabs. Studies on the physiological variation between tropical and temperate zone fiddler crabs of the genus Uca. IX. Oikos 18:118–123CrossRefGoogle Scholar
  76. Vernberg WB, Vernberg FJ (1968a) Studies on the physiological variation between tropical and temperate zone fiddler crabs of the genus Uca. X. The influence of temperature on cytochrome-C oxidase activity. Comp Biochem Phys 26:499–508CrossRefGoogle Scholar
  77. Vernberg WB, Vernberg FJ (1968b) Studies on the physiological variation between tropical and temperate zone fiddler crabs of the genus Uca. VIII. The rate of metabolic adaptation to temperature in tissues of Uca rapax from the northern and southern hemispheres. J Exp Mar Biol Ecol 2:113–123CrossRefGoogle Scholar
  78. Wallace GT, Kim TL, Neufeld CJ (2014) Interpopulational variation in the cold tolerance of a broadly distributed marine copepod. Conserv Physiol 2:cou41.  https://doi.org/10.1093/conphys/cou041 CrossRefGoogle Scholar
  79. Wasserthal LT (1975) The role of butterfly wings in regulation of body temperature. J Insect Physiol 21:1921–1930CrossRefGoogle Scholar
  80. Willett CS (2010) Potential fitness trade-offs for thermal tolerance in the intertidal copepod Tigriopus californicus. Evolution 64:2521–2534CrossRefGoogle Scholar
  81. Winne CT, Keck MB (2005) Intraspecific differences in thermal tolerance of the diamondback watersnake (Nerodia rhombifer): effects of ontogeny, latitude, and sex. Comp Biochem Physiol A Mol Integr Physiol 140:141–149CrossRefGoogle Scholar
  82. Yoder JA, Tank JL, Rellinger EJ, Moore BE, Gribbins KM (2007) Differences in body size and water balance strategies between North Carolina and Florida populations of the sand fiddler crab, Uca pugilator. J Crust Biol 27:560–564CrossRefGoogle Scholar
  83. Zippay ML, Hofmann GE (2010) Physiological tolerances across latitudes: thermal sensitivity of larval marine snails (Nucella spp.). Mar Biol 157:707–714CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Division of Coastal Sciences, School of Ocean Science and TechnologyThe University of Southern MississippiOcean SpringsUSA
  2. 2.Department of Biological SciencesNicholls State UniversityThibodauxUSA
  3. 3.The Water Institute of the GulfBaton RougeUSA
  4. 4.Division of Coastal Sciences, School of Ocean Science and TechnologyThe University of Southern MississippiOcean SpringsUSA

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