Ecophysiological adaptation in a diploid-tetraploid complex of treefrogs (Hylidae)

ECOPHYSIOLOGlCAL ADAPTATION DIPLOID-TETRAPLOID COMPLEX TREEFROGS (HYLIDAE) DENNIS B. RALIN Department

of Biology, Millikin University, lllinois 62522, U.S.A.

Decatur,

Abstract--l.

Sympatric populations of the cryptic treefrog species Hylu chrysoscelis (diploid) and HJ~IN (tetraploid) did not differ in body mass, water content or mean dehydration tolerance, but a population of H. wrsicoh from a higher rainfall locality was significantly less tolerant to desiccation. 2. There was no water content-mediated relationship between body mass and dehydration tolerance in either species. indicating that body size, percentage of body water and dehydration tolerance can vary independently of one another in different popuiations, as in other hyiid frogs. 3. The dipioid and tetraploid are capable of converging ecophysiologically when they occupy the same habitat. rvrsicohr

INTRODLICTION Anuran amphibians exhibit a spectrum of life histories ranging from entirely aquatic to nearly complete terrestrialism or arborealism. Physiological adjustments in water economy, coupled with behavioral responses to variations in abundance or distribution of water. have probably been the most important factors enabling anurans to occupy a wide variety of habitats. Numerous interspecific studies have correlated degree of terrestrialism with water economy parameters such as desiccation tolerance, water content and rate of water loss (Farrell & MacMahon, 1969; Hillman, 1980; Jameson, 1966; Main & Bentley, 1964; Pough et al.. 1977; Ralin & Rogers, 1972; Schmid. 1965; Thorson, 1955; Thorson & Svihla, 1943). Multipopulation studies carried out on hyhd frogs have revealed significant interpopulation variation in at least one water economy parameter in three of the four species examined (Jameson, 1966; Ralin & Rogers, 1972; Nevo, 1973). The differences between populations exceed differences between species and even genera found in earlier studies, and appear to be correlated with moisture differences between localities. The diploid-tetraploid treefrogs H. chr~soscelis and H. t~ersicolor are of interest from this point of view because they form a complex of populations occupying a variety of habitats in the eastern half of the United States and Canada (see provisional range map in Ralin & Selandcr. 1979). The two species are morphologically indistinguishable (Ralin & Rogers. 1979) and temperature-corrected mating call (Ralin, 1968, 1977) and karyotypic analysis (Bogart & Wasserman, 1972) remain as the most accurate and reliable means of species identification. They are also very similar at the ievel of the structural gene. Interspecific genetic similarities of populations from the same geographic region exceed interpopulation comparisons within other species and east-to-west clines in allele frequencies involve both species (Ralin & Selander, 1979). This suggests that the two species are capable of con-

vergent evolution when occupying the same or similar habitats. The most obvious east-to-west environmental trend in Texas is one of decreasing levels of available moisture (Blair, 1950). Nevo & Yang (1979) have suggested that climatic selection (particularly aridity) is the primary factor molding the spatial patterns of genetic variation seen among populations of ffyiu arborea sa~ig~~~~i in Israel. In this study the water economies of sympatric populations of H. chrp.sosceiis and H. oersico/or in central Texas and a population of H. umico/or from eastern Texas are compared with each other and with the water economies of populations of two other hyhds from comparable localities (Ralin & Rogers, 1972). MATERIALS AND METHODS Adult male frogs were collected at two localities in eastern and central Texas during April and May of 1968. The Sam Houston National Forest locality in Montgomery County received an average annual rainfall of 106.7 cm during the period 1958-1967. Only H. cle~s~~~~f~~ is present. Both H. nersicolor and H. chr~~scefis are present in Bastrop State Park, Bastrop County. which had an average annual rainfall of 91.4cm for the years 1958-1967. This locality is the western limit of the range of H. rersicolor in Texas and perhaps in North America. Populations of H. chrysosceiis extend approx 200 km. farther to the west. Acclimation and desiccation procedures that were used are described by Rahn & Rogers (1972). Specimens were kept in 3.8 1. jars with 6 mm of water on the bottom for 5 14 days before being tested. After elimination of bladder water, frogs were weighed and placed in wire mesh cages in an incubator at room temperature. The incubator contained pans of “Drierite” and a small fan that produced a barely perceptible flow of air of 40-509; relative humidity. At the Critical Activity Point (CAP), defined by Rabin & Rogers (1972) as loss of the righting response, each frog was weighed to the nearest milligram. Dry mass of each frog was then obtained by drying to constant weight at 105 ‘C in an oven. Percentage of body mass lost at the CAP, percentage of body water and percentage of body water lost at the CAP where then calculated.

175

176

DENNIS B. RAI 11 Table

Population

I. Mean parameters

(No.)

H. c~hr,wm~/i.s Bastrop (32) H. rrrsico/or H. rwtkolor

Bastrop (28) Sam Houston * Significantly

(28) different

of water economy

Body Mass (g) i2 SE

I’(, Body Water _t2 SE

3.943 & 02.54 4.133 * 0.280 4.019 f 0.312

70.x f 0.4 79.7 + 0.6 79.7 * 0.5

356 t ox 35 1 i: 0.x 32 3 + IO’

-iv-

RESULTS

Water economy parameters for all populations of both species are given in Table 1. There are no significant differences in mean body mass or body water content among the three populations. There is considerable individual variation in body weight and water content. For example. in the H. chrysoscelis population body mass ranges from 2.7 to 5.7 g and water content from 77 to 82”,,. There is a significant difference among populations with regard to the mean CAP, whether measured as percentage body mass lost or percentage of body water lost at the behavioral end point. By either measure, the Sam Houston population of H. ret-sic&r is significantly less tolerant to desiccation than are the Bastrop populations of H. versicolor and H. chrysoscelis (P < 0.001). Individual body mass CAPS ranged from 31 to 40.5”,,; body water CAPS ranged from 39 to 50” (I. The relationships between the following pairs of water economy parameters were examined in each population (Table 2): (I) body mass vs percentage of body water: (2) body mass vs percentage of body mass lost: (3) body mass vs percentage of body water lost; (4) percentage of body water vs percentage of body mass lost; (5) percentage of body water vs percentage of body water lost and (6) percentage of body water lost vs percentage body mass lost.

coefficients

between

4O.h1 I I *

As expected all populations demonstrate a consistently high positive correlation between the percentage of body mass lost CAP and the percentage of body water lost CAP. There is also a consistent negative relationship between body mass and percentage of body water in all three populations (Table 2). However, the highest correlation. that in the Bastrop [I. tlersicolor population. accounts for less than 50”,, of the variation in percentage of body water (R’ = 0.482). The only other significant correlations are positive ones between percentage of body water and percentage of body mass lost in the two populations of H. rersicolor. However. the best correlation accounts for only a small portion of the variation in percentage of body mass lost (R2 = 0.23). In no instance is there a significant correlation between body mass and either measure of dehydration tolerance. Caged frogs initially attempted to escape after introduction into the desiccation chamber. However. all specimens of both species stopped moving and assumed the posture shown in the photographs (Fig. I) between the 1st and 2nd hr after introduction into the chamber. This posture was maintained and even exaggerated during the course of the desiccation process. At the CAP the snout and urostyle were more ventrally directed and the limbs were drawn up closer to the body than illustrated in Fig, I. At the CAP. specimens would resume this posture if the limbs were forcibly extended away from the body. even though the righting response had been lost. The effect of this posture was that at the CAP and beyond all specimens of both species were nearly hemispherical in configuration.

water economy

Population

parameters

‘I,, Body water

in each popularIon

‘I,, Body mass lost

‘I,, Bodq water lost

H. chr~,.w.w~/i.\Bastrop

Body Mass “,, Body Water “,, Body Mass Lost

~ 0.630*

0. I60 0.274

0.324 0.03 I 0.974*

H. wrtidor

Bastrop

Body Mass “,, Body Water “,, Body Mass Lost

- 0.694’

-0.178 0.446*

0.064 0.064 0.963*

If. rcrcidor

Sam Houston

Body Mass ‘IOBody Water IJo Body Mass Lost

- 0.472*

0.05 I 0.480*

0.162 0.295 0.972*

* Significant

at P < 0.01.

II

.!.I i * (I.‘)

at P < 0.001.

Analysis of variance was used to test for interpopulation differences of means in the above parameters. Correlations between desiccation parameters were calculated for each population.

Table 2. Correlation

for three HJ,/‘~ population\

Desiccation

Fig. 1. Dorsal

in treefrogs

(top), lateral (middle) and ventral (bottom) views of a specimen of Hyla approx 90 min after being introduced into a desiccation chamber.

chrysoscelis

I 7x

DENNIS B. RALIS

The three studies that have dealt with the water economy of two or more species of North American hylids have all used different criteria for the end point of the desiccation process (Farrell & MacMahon. 1969; Ralin & Rogers, 1972: Schmid, 1965), making comparisons difficult. However, the procedures and criteria of Ralin & Rogers (1972) were identical to (&~se used here and the Auk crepitans and Pseudtui.\ ,strcdwi were collected from localities that were the same as or very close to, the localities sampled here. In terms of water economy the two species of .&ris are the most aquatic North American hylids (Farrell & MacMahon, 1969; Ralin & Rogers, 1972). Thus far, P. streckeri. which is fossorial, has proved to be the most terrestrial North American hylid examined in terms of water economy (Ralin & Rogers, 1972). The two species of Hula are considered terrestrial arboreal (Farrell & MacMahon. 1969) in water economy. The populations of Hdu examined here show neither inter-specific or intraspecific differences in \hatcr content (Table I). Both species are intermediate i[I water content with respect to populations of A. uq~itcu~s and P. streckeri from approximately the same range of habitats (Ralin & Rogers, 1972). Populations of the latter two species had significantly different mean water contents ranging respectively from 77.2 to 78.9”,, (A. crepituns) and from 81.7 to 83.O”i; (P. strwkeri); intraspecific water content increased with increasing habitat aridity (Ralin & Rogers, 1972). The mean CAPS of 32.3%35.6”,; (body mass lost) found here for H. wrsicolor and H. chrvsoscelis are also intermediate with respect to A. cre&ans (23.1-29.9”;) tr~r/ P. ,streckeri (44.3--14.8”~“) populations (Ralin & Rogers, 1972). Within H. rwsicolor the higher mean CAP is found in the population from the more arid habitat (Table 1). Although .4. uepituns populations differed significantly. there was no pattern consistent with rainfall differences among the localities sampled (Rahn & Rogers. 19721. Sampling populations from a much larger geographic area. Nevo (1973) was able to demonstrate that higher mean desiccation tolerances wcrc correlated with lower moisture levels in A. uepifilJl\.

Within H. rusir~olor. the population from the more arid locality is significantly more tolerant to desiccation and does not differ significantly from the sympatrlc population of H. chry.sosce/is. The two species are therefore capable of ecophysiological convergence: that is, responding physiologically in similar ways to the same environmental variables. This would seem to favor the hypothesis (Ralin, 1977) that the observed greater behavioral (Ralin, 1977), morphological (Ralin & Rogers. 1979) and genetic interspecific resembl.tnces (Rahn & Selander, 1979; Ralin et trl., 1980) of northeastern H. rersico/or (tetraploid) and eastern H. c~/rr~~.wscdis (diploid) populations relative to Texas populations of both species are the result of convergent evolution following a single central origin of H. rcvGo/or from H. c~hr~~sosc~elis. Four of five hylid species in which two or more populations have been examined exhibit significant interpopulation variability of water economy parameters. Furthermore. the pattern seems to vary from

species to species. This raises \otnr tnterestlng questions with regard to correlations of water economy and terrestrialism in interspecific surveys (Thorson & Svihla, 1943; Main & Bentie!. 1964: Schmtd. 196.5: Farrell & MacMahon, 1969). In diRerent studies the same species have exhibited different relali\c tolerantes to desiccation (Farrell & MacMuhon. 1969; Schmid, 1965). Ralin & Rogers (1972) poInted out that differences in mean CAPS of -1. crc,pircm\ populntions from Texas were great enough so that one pop~1lation fell within the aquatic Gt-ottp I of I-arrcll & MacMahon (A. urpirmx ami 1 qrdh~) .~td IIIC‘ others fell within theit- \cmlaquatic Lerrc\triai OI semiaquatic-arboreal Group II tl’. r~r,~,r’itr/~ f[-on] Kentucky. Hdtr uw&.~. from ()hio and H \,/tr ~mwt~ and Hldrc squireiltr from Florida). Populations of H ~~er.sicolor from Louihlana and H dtr qlr.,rtio.w from Florida were considered to hc terrestrial arboreal species (Group III. Farrell & 1LlacMahon. 1969). In this study (Table 1I 111~‘ diffcrencc in mean (-‘AI’ hetwecn the t&O population\ of H. I ~,r\i~.o/or I, greater than the differences hctwcen specie5 within any of the three ecological groupings proposed h! Farrell & MacMahon ( 1969). Despite the intraspecific Ldr-lation. the present study does support the conclusion of Farrell & MacMahon (1969) that extremes of terrcstrialism are discernible in the North American hylid fauna (aquatic forms like Act-is and terrestrial forms like P. mwkeriL However, there are a number of reasons for questioning the suggestion that the similar mean CAPS of the four species in Group II of Farrell & MacMahon (1969) reflect similarities in microhabitat. First. these species are very different in habitat preferences and geographic distributions. Second. the species populations compared were frotn direrent geographic regions and thus similar microhabitats may not even be available to the populations m question. Third. the C.4P varies geographically (Ralin & Rogers. 1972: Nevo. 1973; Table 1I. Fourth. the CAP i\ not the only water cconom! pat-ametel- that tna,y ,be in\c)lved in adaptation to \arymg degree\ of artdlty (popul;~tions) or varying degrees of terre~tricdism (species). The rate at which amphibian\ loxc Mater ix an important water economy factar and is determined primarily by the surface area \olumc ratio rather than absolute physiological difference5 between species. The surface area volume ratio in turn is J function ~)f three factors: (1) size:mass of the species (Schmid. 1965; Farrell & MacMahon. 1969): (2) surface C’O~V figuration (Spight, 1968 ; Heatwole et ctl.. l9hY) and (31 activity patterns (Heatwole c~ftrl.. 1969). Larger specimens lose water at a slower rate. so in theory larger body size would be advantageous in a population inhabiting a more arid environment or in ;I species with a more terrestrial ecology. However. Thorson (1955) suggested that. other things being equal. the advantage in water economy gained by increased body size and a resultant decrease in the rate of &siccation would be offset h) ;I decrcasc 111tolerimce to desiccation mediated throueh dccrc,~>ed h<~l! \r;ttcr content. In this studv thcrccia no \ignificatl( trclationship between body
Desiccation in treefrogs some of the same species used by Thorson (Schmid, 1965; Farrell & MacMahon, 1969; Ralin & Rogers, 1972). Thus the CAP is apparently free to vary independently of body size in different populations and larger body size could be an adaptation to decrease the rate of desiccation and extend the time to the CAP in stressed populations (Nevo, 1973). This may be why the Bastrop population of H. uersicolor is slightly larger on the average than the Sam Houston population (Table 1). In 1969 collections H. chrysoscelis from Bastrop State Park and nearby localities have a mean snout-vent length of 39.6 f 1.21 mm. (+2 SE); a population from Fredericksburg, a more arid locality on the western extremity of the range, is significantly larger (42.3 & 1.26 mm). Even when size/mass is controlled, small differences in rates of desiccation exist among amphibian species (Cohen, 1952; Schmid, 1965; Spight, 1968; Thorson, 1955). Stockier, more compact species tend to lose water more slowly than slender species of the same mass. The posture assumed and maintained by H. chrysoscelis and H. uersicolor during the desiccation process obviously minimizes the surface area to volume ratio of the individual (Fig. 1). With the venter pressed against the substrate (a tree limb, for example), the rate of water loss would therefore be minimized. Neither A. crepitans or P. streckeri (Ralin & Rogers, 1972) exhibit the behavior or posture seen in the Hyla. Both species remain active until shortly before the CAP and at the CAP there is no discernible pattern to the posture. It appears that A. crepiruns and P. streckeri lack the behavioral mechanism for in situ water conservation of the Hyla. The postural adjustments of the Hyla may enable them to survive dehydrating conditions until their water content can be replenished from free water sources like dew and rainfall, whereas the other two species may adjust behaviorally by seeking free water (A. crepiruns) or seeking a more favorable saturation deficit (P. streckeri).

Populations of H. chrysoscelis range as far to the west as P. streckeri. It is possible that these populations will prove to have higher mean CAPS than central Texas populations of H. chrysoscelis, but since the maximum individual CAP exhibited by H. chrysoscelis is 41”” (body mass lost), it seems unlikely that these populations could ever attain mean CAPS as high as those of P. streckeri (4&45°~$. The ability of H. chrysoscelis to extend as far to the west as P. streckeri probably involves a combination of factors: its generally larger body size (Table 1; Ralin & Rogers, 1972); the behavioral adjustment to desiccation stress; its increased body size at localities with lower moisture levels and possibly an increase in mean CAP at localities with lower moisture levels. Acl\norzledgemenrs-I thank Martis Ballinger for taking the photographs used to make Fig. 1. A. A. Burbidge provided technical assistance and advice.

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