Reproductive biology of anurans of the arid Southwest, with emphasis on adaptation of embryos to temperature. Bulletin of the AMNH ; v. 140, article 1

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New York : [American Museum of Natural History]
"Nine species of anuran amphibians inhabit desert-grassland and semiarid uplands of southeastern Arizona and adjacent New Mexico in the vicinity of the Chiricahua Mountains. Embryos of eight of these were raised under constant temperature conditions in order to determine rates of development and upper and lower temperatures limiting for normal development. The species most tolerant of high temperatures is Scaphiopus couchii, early embryos of which can develop normally at a constant temperature of 34° C. Rana pipiens, with an upper limiting temperature of 31.5° C., may be least tolerant of high temperatures, although the limit for Hyla arenicolor may be even lower. Greater differences exist with respect to low temperatures. Bufo debilis may be least able to withstand low temperatures, but its lower limit was not established with precision. Bufo cognatus is unable to develop normally below 16° C., and B. punctatus probably has approximately the same limit. In contrast, Rana pipiens probably can develop at a temperature as low as 12° C., and the limit for Scaphiopus hammondii may be even lower. The temperatures limiting embryonic development correlate with conditions in the breeding sites. Scaphiopus couchii, with the highest upper limiting temperature, breeds in temporary desert rain pools that are the warmest aquatic habitats. Rana pipiens and Hyla arenicolor, both tolerant of cool waters, inhabit mountain streams. The situation is by no means clear-cut, however, and other factors in addition to temperature tolerance figure importantly in the selection of breeding sites. Rates of embryonic development differ greatly among the eight species. The three species of Scaphiopus exhibit rapid rates at all temperatures, but S. couchii develops more rapidly at high temperatures, and S. hammondii and S. bombifrons develop faster at low temperatures. The three species of Bufo and Hyla arenicolor all show similar rates, markedly slower than those of Scaphiopus. Rana pipiens is by far the slowest of all except at temperatures approaching the minimum tolerated by Bufo, at which pipiens develops at a similar or slightly more rapid rate. The effect of change in temperature on developmental rate (the slope of the rate curve) differs in the same fashion. A given change in temperature has roughly the same effect on the three species of Scaphiopus, and on Bufo and Hyla (most on S. couchii, least on H. arenicolor), and the least effect on Rana pipiens. An increase of 10° in temperature, from 19° to 29° C., increases the rate of development of most of the species about three to four times, but only doubles that of pipiens. The most rapid embryonic development is found in the three species of Scaphiopus that breed in temporary desert rain pools. The species of Bufo and those of Hyla have less rapid rates of development and normally utilize breeding sites where the water supply is more lasting but not necessarily permanent. The slowest developer, Rana pipiens, apparently breeds only in permanent waters. Thus there is a correlation between rate of development and water supply. Rapid development may be particularly advantageous to frogs breeding in warmer habitats because of the increase in the range of temperature tolerance of the embryos that accompanies development. The upper limiting temperatures of embryos of Scaphiopus bombifrons and S. hammondii are rather low early in development, but development is so rapid that the most heat-sensitive stage is likely to be passed before the morning sun warms the ponds to dangerously high levels. Scaphiopus couchii, with an initially high level of temperature tolerance and even more rapid development, is perhaps the best adapted to high temperature among all species studied. Other features of the embryonic stages that may reflect adaptation to temperature include the color and size of the ovum, the form of the egg mass, and the stage of development of the embryo when it hatches. To a considerable extent these features are interrelated. A compact mass of dark eggs exposed to sunlight becomes warmer than surrounding still water, an advantage under cool conditions but disadvantageous in warm water. Embryos in cool water, even in a compact mass, are likely to be exposed to a higher oxygen tension than those in warm water and can develop to a later stage, at which the demand for oxygen increases greatly, before hatching. Among the species studied, only Rana pipiens lays dark eggs in a compact mass from which the embryos hatch at a late stage of development. The remaining species vary greatly in the manner in which the eggs are deposited, but, whether they are arranged singly, in long strings, or in small masses, the eggs are well exposed to the water. Presumably this reduction or lack of clumping is necessary in the low oxygen tension of warm water, and also avoids the concentration of dark pigment that presumably is partly responsible for the differential heating of a compact mass. Other factors may be of greater importance than adaptation to temperature in influencing the form of the egg mass. Eggs deposited singly may have greater survival value in a running-water habitat (less likely to be dislodged, or less conspicuous to predators). Both Bufo punctatus and Hyla arenicolor breed in running water, or where pools may suddenly be scoured by floods, and both produce eggs singly, at least part of the time. The long strings of eggs produced by most species of Bufo, but only by B. cognatus in the study area, evidently are well adapted both to cool and warm still-water habitats. If dark coloration of an ovum promotes absorption of heat, lighter eggs might be anticipated in species adapted to warm-water conditions. Dark pigment, however, may also be of importance in protecting the embryo from injury by ultraviolet radiation, so the relationship is not simple. Related species breeding in the same pond at the same time (Scaphiopus couchii and S. hammondii) have eggs that differ noticeably in the amount of dark pigment. Rana pipiens and Hyla arenicolor hatch relatively late in development (stage 20), usually after the gills have started to function. Such late hatching in species adapted to relatively cool conditions agrees with the presumption that the greater oxygen supply in cool water permits a longer period of development within the egg membranes. Similarly, Scaphiopus couchii hatches earlier (stage 18) than S. bombifrons or S. hammondii (late stage 19 or stage 20) and is adapted to warmer temperature than the last two. Bufo cognatus and B. punctatus conform to the usual Bufo mode of hatching at a very early stage (stage 16 or stage 17), regardless of other indications of adaptation to temperature, whereas Bufo debilis hatches rather late (stage 19). Therefore, although there are indications of correlation between stage at hatching and adaptation to temperature, the relationship is not a critical one. For the most part, there are no strong correlations between the geographic distribution of the species studied and the adaptations of their embryos to temperature. A possible relationship of temperature tolerance to distribution is seen in the species Scaphiopus couchii and S. hammondii. The former ranges eastward from Arizona into the hot desert of southeastern California but does not occur on the Pacific coast. Scaphiopus hammondii does not occur in the California deserts but is present in coastal California. Rainfall in the coastal region is almost totally limited to winter and early spring, when temperatures are suitable for the relatively cold-tolerant hammondii but too low for the early embryos of couchii. These spadefoot toads are not restricted to breeding at any one time of the year, but are limited to breeding in temporary rain pools. This inflexibility of their breeding habits may give temperature a more important role in determining the distribution of Scaphiopus than is the case in other species that can vary both breeding season and habitat to some extent. To summarize, the adaptation of frog embryos to temperature takes a variety of courses. Basically, each embryo in its earliest stages of development is capable of tolerating temperatures within a range characteristic of the species or at least of the population. Typically, this range differs from species to species. The range of tolerance expands as the embryo develops, and a rapid rate of embryonic development may be regarded in part as an adaptation to temperature. Features adaptive to high temperature include laying eggs in small masses and hatching at a relatively early stage of development; conversely, very dark eggs in large masses absorb heat more readily and are thus adapted to cooler waters. Superimposed upon the adaptations of the embryos are adaptive aspects of the breeding habits of the frogs, notably habitat selection and variation in time of breeding. The interactions of these various features permit the coexistence of species that differ from one another, in some cases markedly, in one or more aspects of adaptation to temperature"--P. 60-61.
64 p., 2 p. of plates : ill. ; 27 cm.
Includes bibliographical references (p. 62-64).