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Ph and Temperature in Ectothermic Vertebrates Number 18 De~ember 1,1996 pH and Temperature in Ectothermic Vertebrates Life Histories of Noturus baileyi and N. flavipinnis (Pisces: Ictaluridae), Two Rare Madtom Catfishes in Citico Creek, Monroe County, Tennessee BULLETIN ALABAMA MUSEUM OF NATURAL HISTORY The scientific publication of the Alabama Museum of Natural History. Richard L. Mayden, Editor, John C. Hall, Managing Editor. BULLETIN ALABAMA MUSEUM OF NATURAL HISTORY is published by the Alabama Museum of Natural History, a unit of The University of Alabama Museums. The BULLETIN succeeds its predecessor, the MUSEUM PAPERS, which was terminated in 1961 upon the transfer of the Museum to the University from its parent organization, the Geological Survey of Alabama. The BULLETIN is devoted primarily to scholarship and research concerning the natural history of Alabama and the Southeast. It appears twice yearly in consecu­ tively numbered issues. Communication concerning manuscripts, style, and editorial policy should be addressed to: Editor, BULLETIN ALABAMA MUSEUM OF NATURAL HIS­ TORY, The University of Alabama, Box 870340, Tuscaloosa, Alabama 35487- 0340; telephone (205) 348-7550. Prospective authors should examine the Notice to Authors inside the back cover. Orders and requests for general information should be addressed to BULLETIN ALABAMA MUSEUM OF NATURAL HISTORY, at the above address. Yearly subscriptions (two issues) are $15.00 for individuals, $20.00 for corporations and institutions. Numbers may be purchased individually. Payment should accom­ pany orders and subscriptions and checks should be made out to "The University of Alabama." Library exchanges should be handled through: Exchange Librar­ ian, The University of Alabama, Box 870266, Tuscaloosa, Alabama 35487-0340. When citing this publication, authors are requested to use the following abbre­ viation: Bull. Alabama Mus. Nat. Hist. ISSN: 0196-1039 Copyright 1996 by The Alabama Museum of Natural History ))~(( .~ ...:-.~ »0((w ALABAMA MUSEUM of Natural History Number 18 December 1, 1996 pH and Temperature in Ectothermic Vertebrates by Gordon R. Ultsch and Donald C. Jackson Life Histories of Noturus baileyi and N. flavipinnis (Pisces: Ictaluridae), Two Rare Madtom Catfishes in Citico Creek, Monroe County, Tennessee by Gerald R. Dinkins and Peggy W. Shute THE UNIVERSITY OF ALABAMA TUSCALOOSA, ALABAMA December 1, 1996 pH and Temperature in Ectothermic Vertebrates Gordon R. Ultsch Departmen t of Biological Sciences University of Alabama Tuscaloosa, AL ~5487 (FAX 205-~4R-178(j, e-mail Guitsch@biolob,)'.as.ua.edu) Donald C. Jackson Departmen t of Physiolob,)' Brown University Providence, RI 02912 ABSTRACT: Ultsch, Gordon R. and Jackson, Donald C. 1996. pH and Temperature in Ecothermic Verte­ brates. Bulletin Alabama Museum of Natural History, Number 18: 1-42, 13 tables. We have compiled data from a large number of studies of ectothermic vertebrates relating to temperature-acid-base relations. We have documented and analyzed the inverse relationship between both blood pH (pHb) and tissue pH (pHi) with temperature and have evaluated the agreement between these data, both ell masse and in selected subgroupings of species, with the theoretical constructs of Reeves (alphas tat regulation) and Rabn (constant relative alkalinity). In general the experimental data agree with these hypotheses, especially alphas tat regulation, but the changes in pHb (arterial blood pH) with temperature are consistently less than predicted by theory. The slope of the curve for 207 pHb-temperature points (each point an average of up to 36 studies), representing 81 species, is -0.016. When large data sets are considered, significant intergroup differences in the plasma pH-temperature relationship emerge related to the elevation (or y-intercept) of the linear regression relating pH to temperature, but not to its slope. Marine fishes, for example, have lower pHb values than do freshwater fishes, and reptiles have a lower pHb than do freshwater fishes and amphibians. The underlying bases for these differences are unknown. The observed fall in pHb with temperature of air-breathers is achieved principally by increases in PC02, similar to the behavior of blood equilibrated ill vitro, as has been previously noted. The regulatory mechanisms associated with temperature-dependent pHb changes in fishes are less certain, but may involve adjustments in both PC02 and [HCOs·]' We caution that "deviations" from the overall ectotherm slope of certain species or smaller taxonomic groups are in many cases based on relatively few studies, and that more extensive data are needed, particularly within the normal temperature range in which a species operates, before such deviations are accepted as real and therefore requiring an explanation. Bull. Alabama Mus. Nat. Hist. 18:1- 41 Decem ber 1, 1996 2 BULLETIN 18 December 1,1996 Introduction however, demonstrated that the pattern of pH" change HISTORICAL ASPECTS-I t is well established that the pH of was similar among ectothermic species but that the values blood (pHb) and other body fluids of ectothermic verte­ of related acid-base variables were often quite different brates decreases with increasing body temperature. Al­ (Howell et aI., 1970; Rahn and Garey, 1973). For PCO" though this phenomenon was reported several times early and [HC03-], prominent interspecific differences can b~ in this cen tury (Austin et aI., 1927; Henderson, 1928; Dill readily explained by habitat and respiratory mode (Rahn, et aI., 1935; Dill and Edwards, 1935), it only gained wide­ 1966). Water-breathers achieve a particular pH" with low spread attention in more recent times after the study of -], values of both PC02 and [HCOg whereas air-breathers Robin on turtles (1962), followed by detailed investiga­ at the same pH" and temperature have proportionately tions by Rahn, Reeves, and their co-workers (e.g., Rahn, -] . elevated values of both PC02 and [HCOg Systematic 1966; Howell et aI., 1970; Reeves, 1972). The latter work­ differences among species in pHb at a particular tempera­ ers not only added to the growing body of data on the ture, on the other hand, have not been generally recog­ subject, but they also attempted to deduce general laws nized and have not been examined in a comprehensive governing the collected data. manner. The integrative hypotheses of constant relative alkalin­ THEORETICAL CONCEPTS-Rahn (1966) in troduced the con­ ity and alphastat regulation, in particular the latter, have cept of "constant relative alkalinity," based on the similar­ become the operative paradigms in the comparative acid­ ity benveen the temperature dependence of pH" and of base field, and much subsequent work has been carried the neutral pH of pure water (pN). He noted that pH" out to test their validity. The central issues of alphastat and pNw both varied with temperature with a slope of regulation concern the satisfaction of two key properties: about -0.017 U 1°C, but that pHb was 0.4-0.6 U on the first, that pHb decreases with an overall slope of about alkaline side of neutrality. From a regulatory point of view, -0.018 U;oC bet\Veen 0 and 40°C (Reeves, 1976) and, Rahn proposed that the animals were maintaining a con­ second, that total plasma or extracellular CO" concentra­ stant [OH-] / [H+] ratio. An alternative interpretation of tion remains constant over this range. These-conditions, the pH,,-temperature relationship, developed by Reeves in short, require that blood in vivo behave like blood in (1972, 1977), is that the observed pHb changes conform vitro. The failure of collected data to satisfy these ideal to the temperature-dependence of the pK values of pro­ conditions set forth in the Rahn or Reeves hypotheses has tein buffers in the blood and intracellular fluid and that led some workers to question their validity (Heisler, 1986; these changes serve to maintain a constant net electrical Cameron, 1989). Heisler (1986), for example, assembled charge, and thereby a constant degree of dissociation and data from a variety of vertebrate ectotherms in which the a consistent tertiary structure, of proteins within these pH,,-temperature slope was consistently less than -0.018, fluids. The principal buffer group involved is the imida­ leading him to challenge the alphastat hypothesis. In zole moiety of the amino acid histidine. Reeves (1972) addition, Heisler presented intracellular data from his suggested that the animals were regulating the imidazole own and other laboratories that departed in both direc­ dissociation state, or alpha-imidazole (aIm)' and coined tions from the ideal pH,,-temperature slope. Cameron the term alphastat to describe the defended variable asso­ (1989) also criticized the alphastat idea because of the ciated with the inverse pH" change with temperature. The uncertainty of assigning a single value, or of confidently potential importance of alphastat regulation for intracel­ ascribing any value, to the pK of intracellular imidazole lular protein functions has been analyzed by White and groups, because of the very different rnicroenvironments Somero (1982). these groups experience in their host proteins. The issue A striking related observation, originally made on Im­ of intracellular alphastat regulation is complicated fur­ man and laboratory animal blood by Rosenthal (1948), is ther by the pH heterogeneity ofthe intracellular compart­ that the pH of blood subjected to temperature change in ment (White and Somero, 1982), by the diversity of cell vitro at constant gas content exhibits a temperature de­ and tissue
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