Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: A review

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 182, Issue 8, 2012, Pages 997-1014

  McNamara, John Campbell ^a   Faria, Samuel Coelho ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Decapod Crustacea; Evolutionary physiology; Osmoregulation

Indexed keywords

ANIMAL; COMPARATIVE STUDY; DECAPODA (CRUSTACEA); ECOSYSTEM; ELECTROLYTE BALANCE; EVOLUTION; GENETICS; GILL; HEMOLYMPH; METABOLISM; REVIEW; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL EVOLUTION; BIOLOGICAL TRANSPORT; DECAPODA (CRUSTACEA); ECOSYSTEM; GILLS; HEMOLYMPH; WATER-ELECTROLYTE BALANCE;

CRUSTACEA; DECAPODA (CRUSTACEA); PALAEMONIDAE;

EID: 84870352459     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-012-0665-8     Document Type: Review

References (162)

1. Ahearn GA, Duerr JM, Zhuang Z, Brown RJ, Aslamkhan A, Killebrew DA (1999) Ion transport processes of crustacean epithelial cells. Physiol Biochem Zool 72: 1-18.
2. Ahearn GA, Mandal PK, Mandal A (2004) Calcium regulation in crustaceans during the molt cycle: a review and update. Comp Biochem Physiol 137A: 247-257.
3. Antelman SM, Caggiula AR (1980) Stress-induced behavior: chemotherapy without drugs. In: Davidson JM, Davidson RJ (eds) The psychobiology of consciousness. Plenum Press, New York, pp 65-104.
4. Augusto A, Greene LJ, Laure HJ, McNamara JC (2007a) Adaptive shifts in osmoregulatory strategy and the invasion of freshwater by brachyuran crabs: evidence from Dilocarcinus pagei (Trichodactylidae). J Exp Zool 307A: 688-698.
5. Augusto A, Greene LJ, Laure HJ, McNamara JC (2007b) The ontogeny of isosmotic intracellular regulation in the diadromous, freshwater palaemonid shrimps, Macrobrachium amazonicum and M. olfersi (Decapoda). J Crustac Biol 27: 626-634.
6. Augusto A, Pinheiro AS, Greene LJ, Laure HJ, McNamara JC (2009) Evolutionary transition of freshwater by ancestral marine palaemonids: evidence from osmoregulation of in a tide pool shrimp. Aquat Biol 7: 113-122.
7. Ax P (1996) Multicellular animals. A new approach to the phylogenetic order in nature. Springer, New York.
8. +-ATPase activity and epithelial interfaces in gills of the freshwater shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). Comp Biochem Physiol 152A: 431-439.
9. Bentley PJ, Lee AK, Main AR (1958) Comparison of dehydration and hydration of two genera of frogs (Heleioporus and Neobatrachus) that live in areas of varying aridity. J Exp Biol 35: 677-684.
10. Blomberg SP, Garland T (2002) Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J Evol Biol 15: 899-910.
11. Blomberg SP, Garland T Jr, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57: 717-745.
12. Bracken HD, De Grave S, Felder DL (2009) Phylogeny of the infraorder Caridea based on mitochondrial and nuclear genes (Crustacea: Decapoda). In: Martin JW, Felder DL, Crandall KA (eds) Decapod crustacean phylogenetics. Crustacean issues 18. CRC Press, Boca Raton, pp 281-305.
13. Brusca R, Brusca G (2003) Invertebrates, 2nd edn. Sinauer Associates, Inc., Sunderland.
14. Burggren WW, McMahon BR (1988) Biology of the land crabs. Cambridge University Press, Cambridge.
15. Castille FL, Lawrence AL (1981) The effect of salinity on the osmotic, sodium, and chloride concentrations in the hemolymph of the freshwater shrimps, Macrobrachium ohione smith and Macrobrachium rosenbergii de man. Comp Biochem Physiol 70A: 47-52.
16. Charmantier G, Anger K (2010) Ontogeny of osmoregulatory patterns in the South American shrimp Macrobrachium amazonicum: loss of hypo-regulation in a land-locked population indicates phylogenetic separation from estuarine ancestors. J Exp Mar Biol Ecol 396: 89-98.
17. Charmantier G, Charmantier-Daures M, Towle D (2009) Osmotic and ionic regulation in aquatic arthropods. In: Evans DH (ed) Osmotic and ionic regulation: cells and animals. CRC Press, Boca Raton, pp 165-230.
18. Crane J (1975) Fiddler crabs of the world. Princeton University Press, New Jersey.
19. +-ATPase and osmoregulation in the sand fiddler crab, Uca pugilator. Physiol Zool 58: 364-373.
20. Denne LB (1968) Some aspects of osmotic and ionic regulation in the prawns Macrobrachium australiense (Holthuis) and M. equidens (Dana). Comp Biochem Physiol 26: 17-30.
21. Díaz-Uriarte R, Garland T Jr (1996) Testing hypotheses of correlated evolution using phylogenetically independent contrasts: sensitivity to deviations from Brownian motion. Syst Biol 45: 27-47.
22. Diesel R, Schubart CD, Schuh M (2000) A reconstruction of the invasion of land by Jamaican crabs (Grapsidae: Sesarminae). J Zool 250: 141-160.
23. Diniz-Filho JAF (2000) Métodos filogenéticos comparativos. Holos, Ribeirão Preto.
24. Dobkin S, Manning RS (1964) Osmoregulation in two species of Palaemonetes (Crustacea: Decapoda) from Florida. Bull Mar Sci Gulf Carib 14: 149-157.
25. Evans DH (2009) Osmotic and ionic regulation: cells and animals. Taylor & Francis Group, CRC Press, Boca Raton.
26. Evans DH, Piermarini PM, Potts WTW (1999) Ionic transport in the fish gill epithelium. J Exp Zool 283: 641-652.
27. +- and V-ATPase activities and transporter mRNA expression during osmoregulatory acclimation in the cinnamon shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). J Exp Biol 213: 3894-3905.
28. Faria SC, Augusto AS, McNamara JC (2011) Intra- and extracellular osmotic regulation in the hololimnetic Caridea and Anomura: a phylogenetic perspective on the conquest of fresh water by the decapod Crustacea. J Comp Physiol 181B: 175-186.
29. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125: 1-15.
30. Ferraris JD, Fauchald K, Kensley B (1994) Physiological responses to fluctuation in temperature or salinity in invertebrates. Adaptations of Alpheus viridari (Decapoda, Crustacea), Terebellides parva (Polychaeta) and Golfinigia cylindrata (Sipunculida) to the mangrove habitat. Mar Biol 120: 397-406.
31. Firmino KC, Faleiros RO, Masui DC, McNamara JC, Furriel RP (2011) Short- and long-term, salinity-induced modulation of V-ATPase activity in the posterior gills of the true freshwater crab, Dilocarcinus pagei (Brachyura, Trichodactylidae). Comp Biochem Physiol 160B: 24-31.
32. Freire CA, McNamara JC (1995) Fine structure of the gills of the freshwater shrimp Macrobrachium olfersii (Decapoda): effect of acclimation to high salinity medium and evidence for involvement of the lamellar septum in ion uptake. J Crustac Biol 15: 103-116.
33. Freire CA, Cavassin F, Rodrigues EM, Torres AH, McNamara JC (2003) Adaptive patterns of osmotic and ionic regulation, and the invasion of fresh water by the palaemonid shrimps. Comp Biochem Physiol 136: 771-778.
34. Freire CA, Onken H, McNamara JC (2008) A structure-function analysis of ion transport in crustacean gills and excretory organs. Comp Biochem Physiol 151A: 272-304.
35. +-ATPase driven ion transport in posterior gills of the true freshwater crab, Dilocarcinus pagei (Decapoda, Trichodactylidae). J Exp Zool 313A: 508-523.
36. Futuyma DJ (2009) Evolution. Sinauer Associates Inc., Sunderland.
37. Garland T Jr, Ives AR (2000) Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am Nat 155: 346-364.
38. Garland T Jr, Martin KLM, Díaz-Uriarte R (1997) Reconstructing ancestral trait values using squared-change parsimony: plasma osmolarity at the origin of amniotes. In: Sumida SS, Martin KLM (eds) Amniote origins. Academic Press, London, pp 425-501.
39. Garland T Jr, Bennett AF, Rezende EL (2005) Phylogenetic approaches in comparative physiology. J Exp Biol 208: 3015-3035.
40. - exchanger in electrogenic ion transport across the gills of the euryhaline crab Chasmagnathus granulatus. Comp Biochem Physiol 142A: 362-369.
41. Gilles R (1979) Mechanisms of osmoregulation in animals. Wiley, New York.
42. Gilles R, Péqueux A (1986) Physiological and ultrastructural studies of NaCl transport in crustacean gills. Boll Zool 53: 173-182.
43. Gittleman JL, Anderson CG, Kot M, Luh HK (1996) Phylogenetic lability and rates of evolution: a comparison of behavioral, morphological and life history traits. In: Martins EP (ed) Phylogenies and the comparative method in animal behavior. Oxford University Press, Oxford, pp 166-205.
44. González-Ortegón E, Pascual E, Cuesta JA, Drake P (2006) Field distribution and osmoregulatory capacity of shrimps in a temperate European estuary (SW Spain). Estuar Coast Shelf Sci 67: 293-302.
45. Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc Royal Soc Lond 205B: 581-598.
46. Grafen A (1989) The phylogenetic regression. Philos T Roy Soc B 326: 119-157.
47. Greenaway P (1998) Physiological diversity and the colonization of land. In: Schram FR, von Vaupel Klein JC (eds) Crustaceans and the biodiversity crisis. Brill, Leiden, pp 823-842.
48. Greenberg N, Carr JA, Summers CH (2002) Causes and consequences of stress. Integr Comp Biol 42: 508-516.
49. Greenburg G, Hay ED (1986) Cytodifferentiation and tissue phenotype change during transformation of embryonic lens epithelium to mesenchyme-like cells in vitro. Dev Biol 115: 363-379.
50. Gross WJ (1955) Aspects of osmotic regulation in crabs showing the terrestrial habitat. Am Nat 89: 205-222.
51. Gross L (2006) Bridging the gap between theory and ecology in evolutionary models. PLoS Biol 4: e405. doi: 10. 1371/journal. pbio. 0040405.
52. Haas M, Forbush B (2000) The Na-K-Cl cotransporter of secretory epithelia. Annu Rev Physiol 62: 515-534.
53. Hansen TF, Martins EP (1996) Translating between microevolutionary process and macroevolutionary patterns: the correlation structure of interspecific data. Evolution 50: 1404-1417.
54. Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. In: Oxford series in ecology and evolution. Oxford University Press, Oxford.
55. Hay ED (1984) Cell-matrix interaction in the embryo: cell shape, cell surface, cell skeletons, and their role in differentiation. In: Trelstad RL (ed) The role of extracellular matrix in development. Alan Liss, New York, pp 379-409.
56. Hengeveld R, Fedonkin MA (2004) Causes and consequences of eukaryotization through mutualistic endosymbiosis and compartmentalization. Acta Biotheor 52: 105-154.
57. Hennig W (1966) Phylogenetic systematics. University Illinois Press, Urbana.
58. Henry RP (2001) Environmentally mediated carbonic anhydrase induction in the gills of euryhaline crustaceans. J Exp Biol 204: 991-1002.
59. +-ATPase activity in the euryhaline crab, Carcinus maenas, in response to low salinity exposure. J Exp Zool 292: 595-603.
60. Henry RP, Gehnrich S, Weihrauch D, Towle DW (2003) Salinity-mediated carbonic anhydrase induction in the gills of the euryhaline green crab, Carcinus maenas. Comp Biochem Physiol 136A: 243-258.
61. Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, New York.
62. Hull DL (1988) Science as a process: an evolutionary account of the social and conceptual development of science. University of Chicago Press, Chicago.
63. Hull DL, Ruse M (1998) The philosophy of biology. Oxford University Press, New York.
64. Huong DT, Wang T, Bayley M, Phuong NT (2010) Osmoregulation, growth and moulting cycles of the giant freshwater prawn (Macrobrachium rosenbergii) at different salinities. Aquac Res 41: 35-143.
65. Ivanis G, Esbaugh AJ, Perry SF (2008) Branchial expression and localization of SLC9A2 and SLC9A3 sodium/hydrogen exchangers and their possible role in acid-base regulation in freshwater rainbow trout (Oncorhynchus mykiss). J Exp Biol 211: 2467-2477.
66. +-ATPase alpha-subunit in the euryhaline shore crab Pachygrapsus marmoratus: sequence variants and promoter structure. J Exp Biol 210: 2070-2081.
67. Kandel ER, Schwartz JH, Jessel TM (2000) Principles of neural science. McGraw-Hill, New York.
68. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge.
69. Kirschner LB (2004) The mechanism of sodium chloride uptake in hyperregulating aquatic animals. J Exp Biol 207: 1439-1452.
70. Knowlton RE, Kirby DF (1984) Salinity tolerance and sodium balance in the prawn Palaemonetes pugio Holthuis, in relation to other Palaemonetes species. Comp Biochem Physiol 77A: 425-430.
71. Knowlton RE, Schoen RH (1984) Salinity tolerance and sodium balance in the prawn Palaemonetes vulgaris compared with P. pugio. Comp Biochem Physiol 79: 519-524.
72. Krebs HA (1975) The August Krogh principle: for many problems there is an animal on which it can be most conveniently studied. J Exp Zool 194: 221-226.
73. Krogh A (1929) The progress of physiology. Am J Physiol 90: 243-251.
74. Leinen R (1982a) Sodium regulation in a freshwater prawn-I. Tissue electrolyte composition. Comp Biochem Physiol 73A: 315-319.
75. Leinen R (1982b) Sodium regulation in a freshwater prawn-II. Sodium fluxes. Comp Biochem Physiol 73A: 321-326.
76. Lin HC, Su YC, Su SH (2002) A comparative study of osmoregulation in four fiddler crabs (Ocypodidae, Uca). Zool Sci 19: 643-650.
77. Little C (1983) The colonization of land. Cambridge University Press, London.
78. Little C (1990) The terrestrial invasion. Cambridge University Press, New York.
79. Lockwood APM (1962) The osmoregulation of Crustacea. Biol Rev 37: 257-305.
80. Lowy RJ, Dawson DC, Ernst SA (1989) Mechanism of ion transport by avian salt gland primary cell cultures. Am J Physiol 256: R1184-R1191.
81. Lucu C (1990) Ionic regulatory mechanisms in crustacean gill epithelia. Comp Biochem Physiol 97A: 297-306.
82. Lucu C (1993) Ion transport in the gill epithelium of aquatic Crustacea. J Exp Zool 265: 378-386.
83. 2+ exchange activities in gills of hyperregulating Carcinus maenas. Am J Physiol 276: R490-R499.
84. Luquet CM, Pellerano G, Rosa G (1997) Salinity-induced changes in the fine structure of the gills of the semiterrestrial estuarine crab Uca uruguayensis (Nobili, 1901) (Decapoda, Ocypodidae). Tissue Cell 29: 495-501.
85. Luquet CM, Genovese G, Rosa GA, Pellerano GN (2002a) Ultrastructural changes in the gill epithelium of the crab Chasmagnathus granulatus (Decapoda: Grapsidae) in diluted and concentrated seawater. Mar Biol 141: 753-760.
86. + flux in isolated perfused gills of the crab Chasmagnathus granulatus (Grapsidae) acclimated to hyper and hypo-salinity. J Exp Biol 205: 71-77.
87. Luquet CM, Weihrauch D, Senek M, Towle DW (2005) Induction of branchial ion transporter mRNA expression during acclimation to salinity change in the euryhaline crab Chasmagnathus granulatus. J Exp Biol 208: 3627-3636.
88. Maciel CR, Valenti WC (2009) Biology, fisheries, and aquaculture of the Amazon River prawn Macrobrachium amazonicum: a review. Nauplius 17: 61-79.
89. Maddison DR (1994) Phylogenetic methods for inferring the evolutionary history and process of change in discretely valued characters. Annu Rev Entomol 39: 267-292.
90. Maddison WP (1995) Calculating the probability distributions of ancestral states reconstructed by parsimony on phylogenetic trees. Syst Biol 44: 474-481.
91. Maddison WP, Maddison DR (2010) Mesquite: a modular system for evolutionary analysis. Version 2. 73. http://mesquiteproject. org.
92. Maina JN (1990) The morphology of the gills of the African freshwater crab Potamon niloticus Ortmann (Crustacea: Brachyura: Potamonidae): a scanning and transmission electron microscopic study. J Zool 221: 499-515.
93. Mantel LH (1967) Asymmetry potentials, metabolism, and sodium fluxes in gills of the blue crab, Callinectes sapidus. Comp Biochem Physiol 20: 743-753.
94. Mantel LH, Farmer LL (1983) Osmotic and ionic regulation. In: Bliss DE (ed) The biology of Crustacea, volume 5: internal anatomy and physiological regulation. Academic Press, New York, pp 53-159.
95. Martelo MJ, Zanders IP (1986) Modifications of gill ultrastructure and ionic composition in the crab Goniopsis cruentata acclimated to various salinities. Comp Biochem Physiol 84A: 383-389.
96. Martinez CBR, Harris RR, Santos MCF (1998) Transepithelial potential differences and sodium fluxes in isolated perfused gills of the mangrove crab Ucides cordatus. Comp Biochem Physiol 120A: 227-237.
97. + ATPase activity in gill microsomes from the blue crab, Callinectes danae, acclimated to low salinity: novel perspectives on ammonia excretion. Comp Biochem Physiol 153A: 141-148.
98. McNamara JC, Lima AG (1997) The route of ion and water movements across the gill epithelium of the fresh water shrimp Macrobrachium olfersii (Decapoda, Palaemonidae): evidence from ultrastructural changes induced by acclimation to saline media. Biol Bull 192: 321-331.
99. +-ATPase activity and effects of high salinity acclimation in gill and renal epithelia of the freshwater shrimp Macrobrachium olfersii (Crustacea, Decapoda). J Exp Biol 284: 617-628.
100. McNamara JC, Greene LJ, Rosa JC, Augusto A (2004) Adjustment of free amino acid pools in different tissues and hemolymph of the freshwater shrimp Macrobrachium olfersii (Crustacea, Decapoda) during salinity acclimation. Mar Fresh Behav Physiol 37: 193-208.
101. Moreira GS, McNamara JC, Shumway SE, Moreira PS (1983) Osmoregulation and respiratory metabolism in Brazilian Macrobrachium (Decapoda, Palaemonidae). Comp Biochem Physiol 74A: 57-62.
102. Morris PJ (1993) The developmental role of the extracellular matrix suggests a monophyletic origin of the kingdom Animalia. Evolution 47: 152-165.
103. Morris S (2001) Neuroendocrine regulation of osmoregulation and the evolution of air-breathing in decapod crustaceans. J Exp Biol 204: 979-989.
104. Murphy NP, Austin CM (2005) Phylogenetic relationships of the globally distributed freshwater prawn genus Macrobrachium (Crustacea: Decapoda: Palaemonidae): biogeography, taxonomy and the convergent evolution of abbreviated larval development. Zool Scr 34: 187-197.
105. + antiporter cDNA from the blue crab Callinectes sapidus. Bull Mt Desert Isl Biol Lab 35: 19-21.
106. Nielsen C (2001) Animal evolution. Oxford University Press, Oxford.
107. Onken H, McNamara JC (2002) Hyperosmoregulation in the red freshwater crab Dilocarcinus pagei (Brachyura, Trichodactylidae): structural and functional asymmetries of the posterior gills. J Exp Biol 205: 167-175.
108. - absorption across the gills of Eriocheir sinensis. J Exp Biol 198: 767-774.
109. Onken H, Riestenpatt S (1998) NaCl absorption across split gill lamellae of hyperregulating crabs: transport mechanisms and their regulation. Comp Biochem Physiol 119A: 883-893.
110. - uptake across the posterior gills of the Chinese crab (Eriocheir sinensis): voltage-clamp and microelectrode studies. J Comp Physiol 161B: 293-301.
111. Onken H, Graszynski K, Johannsen A, Putzenlechner M, Riestenpatt S, Schirmer C, Siebers D, Zeiske W (1995) How to overcome osmotic stress? Marine crabs conquer freshwater. New insights from modern electrophysiology. Helgoländer Meeresunters 49: 715-725.
112. Onken H, Tresguerres M, Luquet CM (2003) Active NaCl absorption across posterior gills of hyperosmoregulating Chasmagnathus granulatus. J Exp Biol 206: 1017-1023.
113. Panikkar NK (1941) Osmoregulation in some palaemonid prawns. J Mar Biol Assoc UK 25: 317-359.
114. Parry G, Potts WTW (1965) Sodium balance in the freshwater prawn, Palaemonetes antennarius. J Exp Biol 42: 415-421.
115. Péqueux A (1995) Osmotic regulation in crustaceans. J Crust Biol 15: 1-60.
116. Pereira G (1997) A cladistic analysis of the freshwater shrimps of the family Palaemonidae (Crustacea, Decapoda, Caridea). Acta Biol Venezuel 17: 1-69.
117. Pileggi LG, Mantelatto FL (2010) Molecular phylogeny of the freshwater prawn genus Macrobrachium (Decapoda, Palaemonidae), with emphasis on the relationships among selected American species. Invert Syst 24: 194-208.
118. Prosser CL (1973) Comparative animal physiology. Saunders, Philadelphia.
119. Pullikuth AK, Filippov V, Gill SS (2003) Phylogeny and cloning of ion transporters in mosquitoes. J Exp Biol 206: 3857-3868.
120. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
121. Richter S, Møller OS, Wirkner CS (2009) Advances in crustacean phylogenetics. Arthropod Syst Phylogeny 67: 275-286.
122. - across the gill epithelium of the shore crab Carcinus maenas: voltage-clamp and ion-flux studies. J Exp Biol 199: 1545-1554.
123. Riordan JR, Forbush B III, Hanrahan JW (1994) The molecular basis of chloride transport in shark rectal gland. J Exp Biol 196: 405-418.
124. Russell JM (2000) Sodium-potassium-chloride cotransport. Physiol Rev 80: 211-276.
125. Sáez AG, Lozano E, Zaldívar-Riverón A (2009) Evolutionary history of Na, K-ATPases and their osmoregulatory role. Genetica 136: 479-490.
126. Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge.
127. Schubart CD, Diesel R (1998) Osmoregulatory capacities and penetration into terrestrial habitats: a comparative study of Jamaican crabs of the genus Armases Abele, 1992 (Brachyura: Grapsidae: Sesarminae). Bull Mar Sci 62: 743-752.
128. Schultz TR, Cocroft RB, Churchill GA (1996) The reconstruction of ancestral states. Evolution 50: 504-511.
129. Siebers D, Winkler A, Lucu C, Thedens G, Weichart D (1985) Na-K-ATPase generates an active transport potential in the gills of the hyperregulating shore crab Carcinus maenas. Mar Biol 87: 185-192.
130. Sober E, Orzack SH (2003) Common ancestry and natural selection. Brit J Philos Sci 54: 423-437.
131. Taylor HH, Taylor EW (1992) Gills and lungs: the exchange of gases and ions. In: Harrison FW, Humes AG (eds) Microscopic anatomy of invertebrates, decapod Crustacea, vol 10. Wiley-Liss, New York, pp 203-293.
132. Thurman CL (2002) Osmoregulation in six sympatric fiddler crabs (genus Uca) from the northwestern Gulf of Mexico. Mar Ecol 23: 269-284.
133. 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.
134. Thurman Cl (2005) A comparison of osmoregulation among subtropical fiddler crabs (Uca) from Southern Florida and California. Bull Mar Sci 77: 83-100.
135. Thurman C, Hanna J, Bennett C (2010) Ecophenotypic physiology: osmoregulation by fiddler crabs (Uca spp.) from the northern Caribbean in relation to ecological distribution. Mar Fresh Behav Physiol 43: 339-356.
136. Torres AH Jr (2006) Um estudo eletrofisiológico e ultraestrutural do transporte iônico transepitelial em camarões e caranguejos (Crustacea, Decapoda). Ph. D. thesis, University of São Paulo.
137. +-ATPase in gill epithelium of two osmoregulating crabs, Callinectes sapidus and Carcinus maenas. J Exp Zool 239: 311-318.
138. Towle DW, Weihrauch D (2001) Osmoregulation by gills of euryhaline crabs: molecular analysis of transporters. Am Zool 41: 770-780.
139. Towle DW, Rushton ME, Heidysch D, Magnani JJ, Rose MJ, Amstutz A, Jordan MK, Shearer DW, Wu WS (1997) Sodium/proton antiporter in the euryhaline crab Carcinus maenas molecular cloning, expression and tissue distribution. J Exp Biol 200: 1003-1014.
140. +-ATPase in gills of the blue crab Callinectes sapidus: cDNA sequencing and salinity related expression of alpha-subunit mRNA and protein. J Exp Biol 204: 4005-4012.
141. Towle DW, Henry RP, Terwilliger NB (2011) Microarray-detected changes in gene expression in gills of green crabs (Carcinus maenas) upon dilution of environmental salinity. Comp Biochem Physiol 6D: 115-125.
142. +-ATPase in the gills of 13 euryhaline crabs during salinity acclimation. J Exp Biol 210: 620-627.
143. Tyler S (2003) Epithelium: the primary building block for metazoan complexity. Integr Comp Biol 43: 55-63.
144. Valentine JW (2004) On the origin of phyla. University of Chicago Press, Chicago.
145. von Sternberg R, Cumberlidge N, Rodríguez G (1999) On the marine sister groups of the freshwater crabs (Crustacea: Decapoda: Brachyura). J Zool Syst Evol Res 37: 19-38.
146. Webb DA (1940) Ionic regulation in Carcinus maenas. Proc Royal Soc London 129: 107-136.
147. Weber RE, Spaargaren DH (1970) On the influence of temperature on the osmoregulation of Crangon crangon and its significance under estuarine conditions. Nether J Sea Res 5: 108-120.
148. --cotransporter are expressed in gills of the euryhaline Chinese crab Eriocheir sinensis. Comp Biochem Physiol 126: S158-S158.
149. +-ATPase (β-subunit) in gills of euryhaline crabs and its physiological role in osmoregulatory ion uptake. J Exp Biol 204: 25-37.
150. Weihrauch D, McNamara JC, Towle DW, Onken H (2004a) Ion-motive ATPases and active, transbranchial NaCl uptake in the red freshwater crab, Dilocarcinus pagei (Decapoda, Trichodactylidae). J Exp Biol 207: 4623-4631.
151. Weihrauch D, Morris S, Towle DW (2004b) Ammonia excretion in aquatic and terrestrial crabs. J Exp Biol 207: 4491-4504.
152. Wheatly MG, Gao Y (2004) Molecular biology of ion motive proteins in comparative models. J Exp Biol 207: 3253-3263.
153. Wheatly MG, Zanotto FP, Hubbard MG (2002) Calcium homeostasis in crustaceans: subcellular Ca dynamics. Comp Biochem Physiol 132B: 163-178.
154. Wiley EO (1975) Karl R. Popper, systematics and classification: a reply to Walter Bock and other evolutionary taxonomists. Syst Zool 24: 233-243.
155. Wilmer PG (1982) Microclimate and environmental physiology of insects. Adv Insect Physiol 16: 1-57.
156. Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Ann Rev Biochem 46: 573-639.
157. Wood TG (1971) The distribution and abundance of Folsomides deserticula (Collembola, Isotomidae) and other microarthropods in arid and semi-arid soils in southern Australia, with a note on nematode populations. Pedobiologia 11: 446-468.
158. Wowor D, Muthu V, Meier R, Balke M, Cai Y, Ng PKL (2009) Evolution of life history traits in Asian freshwater prawns of the genus Macrobrachium (Crustacea: Decapoda: Palaemonidae) based on multilocus molecular phylogenetic analysis. Mol Phylogenet Evol 52: 340-350.
159. +-ATPase in the sailfin molly correlates with hypoosmoregulatory endurance. J Comp Physiol 181B: 953-964.
160. +-ATPase, and V-ATPase in the freshwater crayfish Cherax destructor (Crustacea: Parastacidae). Comp Biochem Physiol 119A: 739-745.
161. + channels: amiloride-induced current-noise in crab gill. Biochim Biophys Acta 1105: 245-252.
162. Zetino AM, Kirschner LB, Harvey M (2001) On the mechanism of sodium-proton exchange in crayfish. Comp Biochem Physiol 128A: 863-872.