Abstract
During tidal cycles, fiddler crabs undergo alternating periods of submersion and desiccation. We compare physiological and biochemical adjustments to submersion and desiccation challenge in two gelasminids from the Galapagos archipelago: the indigenous Leptuca helleri, and Minuca galapagensis. We examine population distributions and habitat characteristics; survival and hemolymph osmolality after 6 h submersion at several salinities, and after 6 or 12 h desiccation; and oxidative stress responses in the hepatopancreas and gills, accompanying glutathione enzyme antioxidant activities, and lipid peroxidation. We provide an integrated biomarker response index based on oxidative stress in each tissue, condition and species. Leptuca helleri occupies a restricted intertidal niche while M. galapagensis is supralittoral. Burrow density in M. galapagensis declined with increasing salinity and decreasing substrate moisture; L. helleri burrow density showed no correlation. After 6 h submersion, L. helleri survived only at 21‰S while M. galapagensis survived from 0 to 42 ‰S. After 6 h desiccation, hemolymph osmolality decreased markedly in L. helleri but increased in M. galapagensis. Antioxidant enzyme activities and lipid peroxidation in the hepatopancreas and gills showed tissue- and species-specific responses to submersion and desiccation challenge. The integrated biomarker response indexes for L. helleri were highest in control crabs, driven by oxidative stress. In M. galapagensis, submersion was the determining factor in both tissues. Minuca galapagensis is a generalist species while Leptuca helleri occupies a more restricted intertidal habitat. The species’ respective physiological limitations and flexibilities provide insights into how fiddler crabs might respond to environmental change on semi-arid islands.
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Data are available on request to Prof John C. McNamara.
References
Allen BJ, Levinton JS (2014) Sexual selection and the physiological consequences of habitat choice by a fiddler crab. Oecologia 176:25–34. https://doi.org/10.1007/s00442-014-3002-y
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 438:93–99. https://doi.org/10.1016/j.jembe.2012.09.009
Araújo MB, Luoto M (2007) The importance of biotic interactions for modelling species distributions under climate change. Glob Ecol Biogeogr 16:743–753
Baldwin GF, Kirschner LB (1976) Sodium and chloride regulation in Uca adapted to 10% sea water. Physiological Zoology 49:172–180
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 Linnean Soc 81:23–87. https://doi.org/10.1111/j.1096-3642.1984.tb02558.x
Beebe W (1924) Galápagos: World’s End. GP Putnam’s Sons, GP
Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21:1316–1322
Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative Stress and Antioxidant Defense. World Allergy Organ J 5:9–19. https://doi.org/10.1097/WOX.0b013e3182439613
Bonjoch NP, Tamayo PR (2001) Protein Content Quantification by Bradford Method. In: Reigosa Roger MJ (ed) Handbook of Plant Ecophysiology Techniques. Springer, Netherlands, Dordrecht, pp 283–295
Boone L (1927) Crustacea from tropical East American Seas: scientific results of the first oceanographic expedition of the “Pawnee” 195. Bingham Oceanograph Collect 5:9
Borecka A, Janas U, Kendzierska H (2016) The combined effect of temperature and salinity changes on osmoregulation and haemocyanin concentration in Saduria entomon (Linnaeus, 1758). Marine Biol Res 12:316–322. https://doi.org/10.1080/17451000.2016.1142092
Capparelli MV, Abessa DM, McNamara JC (2016) Effects of metal contamination in situ on osmoregulation and oxygen consumption in the mudflat fiddler crab Uca rapax (Ocypodidae, Brachyura). Biochem Physiol Toxicol Pharmacol 185–186:102–111. https://doi.org/10.1016/j.cbpc.2016.03.004
Capparelli MV, McNamara JC, Grosell M (2017) Effects of waterborne copper delivered under two different exposure and salinity regimes on osmotic and ionic regulation in the mudflat fiddler crab, Minuca rapax (Ocypodidae, Brachyura). Ecotoxicol Environ Saf 143:201–209
Capparelli MV, Gusso-Choueri PK, Abessa DM, McNamara JC (2019) Seasonal environmental parameters influence biochemical responses of the fiddler crab Minuca rapax to contamination in situ. Comp Biochem Physiol Toxicol Pharmacol 216:93–100. https://doi.org/10.1016/j.cbpc.2018.11.012
Chapman MG, Underwood AJ (1996) Influences of tidal conditions, temperature and desiccation on patterns of aggregation of the high-shore periwinkle, Littorina unifasciata, in New South Wales, Australia. J Exp Mar Biol Ecol 196:213–237. https://doi.org/10.1016/0022-0981(95)00131-X
Costa TM, Soares-Gomes A (2015) Secondary production of the fiddler crab Uca rapax from mangrove areas under anthropogenic eutrophication in the Western Atlantic, Brazil. Mar Pollut Bull 101:533–538. https://doi.org/10.1016/j.marpolbul.2015.10.061
Crane J (2015) Fiddler crabs of the world: Ocypodidae: genus Uca. Princeton University Press, Princeton
Cuellar-Gempeler C, Munguia P (2013) Fiddler crabs (Uca thayeri, Brachyura: Ocypodidae) affect bacterial assemblages in mangrove forest sediments. Commun Ecol 14:59–66. https://doi.org/10.1556/ComEc.14.2013.1.7
D’Orazio SE, Holliday CW (1985) Gill Na, K-ATPase and osmoregulation in the sand fiddler crab, Uca pugilator. Physiol Zool 58:364–373
Díaz H, Rodríguez G (1977) The branchial chamber in terrestrial crabs: a comparative study. Biol Bull 153:485–504
Dillard CJ, Tappel AL (1989) Lipid peroxidation products in biological tissues. Free Radical Biol Med 7:193–196. https://doi.org/10.1016/0891-5849(89)90014-2
Garth JS, Murphy RC (1948) The Brachyura of the “Askoy” expedition: with remarks on carcinological collecting in the panama bight. Bull Am Museum Nat History 92:1
Halliwell B, Chirico S (1993) Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr 57:715S-725S. https://doi.org/10.1093/ajcn/57.5.715S
Helmuth B, Harley CDG, Halpin PM, O’Donnell M, Hofmann GE, Blanchette CA (2002) Climate change and latitudinal patterns of intertidal thermal stress. Science 298:1015–1017. https://doi.org/10.1126/science.1076814
Jones LL (1941) Osmotic regulation in several crabs of the Pacific coast of North America. J Cell Comp Physiol 18:79–92
Keeling PL, Smith LL (1982) Relevance of NADPH depletion and mixed disulphide formation in rat lung to the mechanism of cell damage following paraquat administration. Biochem Pharmacol 31:3243–3249. https://doi.org/10.1016/0006-2952(82)90557-3
Keen JH, Habig WH, Jakoby WB (1976) Mechanism for the several activities of the glutathione S-transferases. J Biol Chem 251:6183–6188
Landstorfer RB, Schubart CD (2010) A phylogeny of Pacific fiddler crabs of the subgenus Minuca (Crustacea, Brachyura, Ocypodidae: Uca) with the description of a new species from a tropical gulf in Pacific Costa Rica. J Zool Syst Evol Res 48:213–218. https://doi.org/10.1111/j.1439-0469.2009.00554.x
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 469:57–62. https://doi.org/10.1016/j.jembe.2015.04.010
Liu C, Chang VWC, Gin KYH (2013) Environmental toxicity of PFCs: an enhanced integrated biomarker assessment and structure–activity analysis. Environ Toxicol Chem 32:2226–2233. https://doi.org/10.1002/etc.2306
Livingstone DR, Lemaire P, Matthews A, Peters L, Bucke D, Law RJ (1993) Pro-oxidant, antioxidant and 7-ethoxyresorufin O-deethylase (EROD) activity responses in liver of Dab (Limanda limanda) exposed to sediment contaminated with hydrocarbons and other chemicals. Mar Pollut Bull 26:602–606. https://doi.org/10.1016/0025-326X(93)90498-9
Martínez-Álvarez RM, Morales AE, Sanz A (2005) Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fisheries 15:75–88. https://doi.org/10.1007/s11160-005-7846-4
McFarland VA, Inouye LS, Lutz CH, Jarvis AS, Clarke JU, McCant DD (1999) Biomarkers of oxidative stress and genotoxicity in livers of field-collected brown bullhead, ameiurus nebulosus. Arch Environ Contam Toxicol 37:236–241. https://doi.org/10.1007/s002449900510
McGuinness KA (1994) The climbing behaviour of Cerithidea anticipata (Mollusca: Gastropoda): the roles of physical and biological factors. Aust J Ecol 19:283–289. https://doi.org/10.1111/j.1442-9993.1994.tb00491.x
Moity N, Delgado B, Salinas-de-León P (2019) Mangroves in the Galapagos islands: distribution and dynamics. PLoS ONE 14:e0209313. https://doi.org/10.1371/journal.pone.0209313
Morris S, Oliver S (1999) Respiratory gas transport, haemocyanin function and acid–base balance in Jasus edwardsii during emersion and chilling: simulation studies of commercial shipping methods. Comp Biochem Physiol Mol Integr Physiol 122:309–321. https://doi.org/10.1016/S1095-6433(99)00004-5
Munguia P, Backwell PRY, Darnell MZ (2017) Thermal constraints on microhabitat selection and mating opportunities. Anim Behav 123:259–265. https://doi.org/10.1016/j.anbehav.2016.11.004
Nobbs M (2003) Effects of vegetation differ among three species of fiddler crabs (Uca spp.). J Exp Mar Biol Ecol 284:41–50. https://doi.org/10.1016/S0022-0981(02)00488-4
Oliveira UO, da Rosa Araújo AS, Belló-Klein A, Silva RSM, Kucharski LC (2005) Effects of environmental anoxia and different periods of reoxygenation on oxidative balance in gills of the estuarine crab Chasmagnathus granulata. Comp Biochem Physiol Biochem Mol Biol 140:51–57. https://doi.org/10.1016/j.cbpc.2004.09.026
Paital B (2013) Antioxidant and oxidative stress parameters in brain of Heteropneustes fossilis under air exposure condition; role of mitochondrial electron transport chain. Ecotoxicol Environ Saf 95:69–77. https://doi.org/10.1016/j.ecoenv.2013.05.016
Paital B, Chainy GBN (2010) Antioxidant defenses and oxidative stress parameters in tissues of mud crab (Scylla serrata) with reference to changing salinity. Comp Biochem Physiol Toxicol Pharmacol 151:142–151. https://doi.org/10.1016/j.cbpc.2009.09.007
Peck SB (1994) Diversity and zoogeography of the non-oceanic Crustacea of the Galápagos Islands, Ecuador (excluding terrestrial Isopoda). Can J Zool 72:54–69. https://doi.org/10.1139/z94-009
Perussolo MC, Guiloski IC, Lirola JR, Fockink DH, Corso CR, Bozza DC, Prodocimo V, Mela M, Ramos LP, Cestari MM, Acco A, Silva de Assis HC (2019) Integrated biomarker response index to assess toxic effects of environmentally relevant concentrations of paracetamol in a neotropical catfish (Rhamdia quelen). Ecotoxicol Environ Saf 182:109438. https://doi.org/10.1016/j.ecoenv.2019.109438
Powers LW, Cole JF (1976) Temperature variation in fiddler crab microhabitats. J Exp Mar Biol Ecol 21:141–157. https://doi.org/10.1016/0022-0981(76)90035-6
Principe SC, Augusto A, Costa TM (2018) Differential effects of water loss and temperature increase on the physiology of fiddler crabs from distinct habitats. J Therm Biol 73:14–23. https://doi.org/10.1016/j.jtherbio.2018.02.004
Rabalais NN, Cameron JN (1985) The effects of factors important in semi-arid environments on the early development of Uca subcylindrica. Biol Bull 168:147–160
Rathbun MJ (1902) Papers from the Hopkins Stanford Galápagos Expedition, 1898–1899. VIII. Brachyura and Macrura. In, Proceedings of the Washington Academy of Sciences (Vol. 4, pp. 275–292). Washington Academy of Sciences.
Reed DJ (1986) Defense mechanisms of normal and tumor cells. Internat J Radiation Oncol Biol Phys 12:1457–1461. https://doi.org/10.1016/0360-3016(86)90194-X
Sies H (1993) Strategies of antioxidant defense. Eur J Biochem 215:213–219. https://doi.org/10.1111/j.1432-1033.1993.tb18025.x
Smith WK, Miller PC (1973) The thermal ecology of two south Florida fiddler crabs: Uca rapax smith and U. pugilator Bosc. Physiol Zool 46:186–207
Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr Comp Biol 42:780–789. https://doi.org/10.1093/icb/42.4.780
Saintilan N, Wilson NC, Rogers K, Rajkaran A, Krauss KW (2014) Mangrove expansion and salt marsh decline at mangrove poleward limits. Glob Change Biol 20(1):147–157
Tan KH, Meyer DJ, Coles B, Gillies N, Ketterer B (1987) Detoxication of peroxidized DNA by glutathione transferases. Biochem Soc Trans 15:628–629. https://doi.org/10.1042/bst0150628
Taylor HH, Greenaway P (1979) The structure of the gills and lungs of the arid-zone crab, Holthuisana (Austrothelphusa) transversa (Brachyura: Sundathelphusidae) including observations on arterial vessels within the gills. J Zool 189:359–384
Teal JM (1959) Respiration of crabs in georgia salt marshes and its relation to their ecology. Physiol Zool 32:1–14
Teal JM, Carey FG (1967) The metabolism of marsh crabs under conditions of reduced oxygen pressure. Physiol Zool 40:83–91. https://doi.org/10.1086/physzool.40.1.30152440
Thurman CL (1998) Evaporative water loss, corporal temperature and the distribution of sympatric fiddler crabs (Uca) from South Texas. Comp Biochem Physiol Mol Integr Physiol 119:279–286. https://doi.org/10.1016/S1095-6433(97)00424-8
Thurman CL (2003) Osmoregulation by six species of fiddler crabs (Uca) from the Mississippi delta area in the Northern Gulf of Mexico. J Exp Mar Biol Ecol 291:233–253. https://doi.org/10.1016/S0022-0981(03)00138-2
Thurman CL (2005) A comparison of osmoregulation among subtropical fiddler crabs (Uca) from Southern Florida and California. Bull Mar Sci 77:83–100
Thurman C, Hanna J, Bennett C (2010) Ecophenotypic physiology: osmoregulation by fiddler crabs (spp.) from the northern Caribbean in relation to ecological distribution. Marine Freshw Behav Physiol 43(5):339–356
Thurman CL, Faria SC, McNamara JC (2013) The distribution of fiddler crabs (Uca) along the coast of Brazil: implications for biogeography of the western Atlantic Ocean. Marine Biodiversity Records. https://doi.org/10.1017/S1755267212000942
Thurman CL, Faria SC, McNamara JC (2017) Geographical variation in osmoregulatory abilities among populations of ten species of fiddler crabs from the Atlantic coast of Brazil: a macrophysiological analysis. J Exp Mar Biol Ecol 497:243–253. https://doi.org/10.1016/j.jembe.2017.07.007
Timperley CM, Abdollahi M, Al-Amri AS, Baulig A, Benachour D, Borrett V, Cariño FA, Geist M, Gonzalez D, Kane W, Kovarik Z, Martínez-Álvarez R, Fusaro Mourão NM, Neffe S, Raza SK, Rubaylo V, Suárez AG, Takeuchi K, Tang C, Trifirò F, van Straten FM, Vanninen PS, Vučinić S, Zaitsev V, Zafar-Uz-Zaman M, Zina MS, Holen S, Forman JE, Alwan WS, Suri V (2019) Advice on assistance and protection by the scientific advisory board of the organisation for the prohibition of chemical weapons: Part 2. on preventing and treating health effects from acute, prolonged, and repeated nerve agent exposure, and the identification of medical countermeasures able to reduce or eliminate the longer term health effects of nerve agents. Toxicology 413:13–23. https://doi.org/10.1016/j.tox.2018.11.009
Urbina MA, Paschke K, Gebauer P, Cumillaf JP, Rosas C (2013) Physiological responses of the southern king crab, Lithodes santolla (Decapoda: Lithodidae), to aerial exposure. Comp Biochem Physiol Mol Integr Physiol 166:538–545. https://doi.org/10.1016/j.cbpa.2013.08.006
Von Hagen H-O (1968) Studien an peruanischen Winkerkrabben (Uca). Zoologische Jahrbücher. Abteilung für Systematik Ökologie und Geographie der Tiere 95:395–468
Wilson RJ, Gutiérrez D, Gutiérrez J, Martínez D, Agudo R, Monserrat VJ (2005) Changes to the elevational limits and extent of species ranges associated with climate change. Ecol Lett 8:1138–1146. https://doi.org/10.1111/j.1461-0248.2005.00824.x
Withers PC (1992) Comparative animal physiology. Saunders College Publications, Philadelphia, pp 542–545
Zanders IP, Rojas WE (1996) Salinity effects on cadmium accumulation in various tissues of the tropical fiddler crab Uca rapax. Environ Pollut 94:293–299. https://doi.org/10.1016/S0269-7491(96)00095-4
Acknowledgements
We wish to express our appreciation to the staff of the regional offices of the Ministerio del Ambiente de Ecuador (MAE) for supporting this research (MAE-DNB-CM-2017-0062-IKIAM), and in particular, we thank Galo Quezada and Jeniffer Suarez (Galapagos National Park, Isla Santa Cruz, Permit #083-2019 DPNG). During fieldwork, we were graciously assisted by Angel Cajas (Ikiam), Alexandra Kler Lago (Galapagos National Park) and Mara Anais Espinoza Buitrón (Galapagos National Park). MVC received no financial support towards the costs of this investigation. The University of Northern Iowa (UNI) Study Abroad Program, and Information Technology Services, provided travel support for CLT. JCM received an Excellence in Research scholarship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil (CNPq 303613/2017-3) which defrayed travel and accommodation costs. PKG-C thanks the Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil, for financial support (FAPESP #2017/04970-5). We are also grateful to Dr. Gabriel Massaine Moulatlet (Ikiam) for the preparation of the study area map and Figure 3.
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MVC: conceptualization, methodology, validation, formal analysis, investigation, resources, writing—original draft, writing—review and editing, supervision, and project administration. CLT: methodology, resources, writing—review and editing, and funding acquisition. PGC: validation and writing—review and editing. DMA: validation, resources, and writing—review and editing. MKF: validation, and writing—review and editing. CRN: software, formal analysis, and writing—review and editing. JCM: methodology, validation, formal analysis, investigation, resources, data curation, writing—original draft, writing—review and editing, supervision, project administration, and funding acquisition.
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Capparelli, M.V., Thurman, C.L., Choueri, P.G. et al. Survival strategies on a semi-arid island: submersion and desiccation tolerances of fiddler crabs from the Galapagos Archipelago. Mar Biol 168, 8 (2021). https://doi.org/10.1007/s00227-020-03807-6
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DOI: https://doi.org/10.1007/s00227-020-03807-6