Natural Hybridization among Distantly Related Toads (Bufo alvarius, Bufo cognatus, Bufo woodhousii) in Central Arizona

Natural Hybridization among Distantly Related Toads (Bufo alvarius, Bufo cognatus, Bufowoodhousii) in Central ArizonaAuthor(s): Erik W. A. Gergus, Keith B. Malmos and Brian K. SullivanSource: Copeia, Vol. 1999, No. 2 (May 7, 1999), pp. 281-286Published by: American Society of Ichthyologists and Herpetologists (ASIH)Stable URL: http://www.jstor.org/stable/1447473 .

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Copeia, 1999(2), pp. 281-286

Natural Hybridization among Distantly Related Toads

(Bufo alvarius, Bufo cognatus, Bufo woodhousii) in Central Arizona

ERIK W. A. GERGUS, KEITH B. MALMOS, AND BRIAN K. SULLIVAN

Putative hybrid toads of the genus Bufo were collected in central Arizona and identified using allozymes, qualitative and qalsntitative morphological characters, and release call characteristics. Data suggest one hybrid resulted from mating between Bufo cognatus and Bufo woodhousii, and the other three resulted from matings between Bufo alvarius and B. woodhousii. Natural hybridization between these taxa has not been previously reported. To date, B. woodhousii has been found to hybridize with four species of the Bufo americanus species group, of which B. woodhousii is a member, and five other species which represent three outgroups to the B. americanus group. Fossil evidence suggests some genomic compatability has been retained between B. alvarius and B. woodhousii despite at least 6 million years of independent evolution. Hybridization among members of Bufo may be due to alternative mating tactics of males, such as active searching, and by alteration of historical habitats in central Arizona.

WT EATHIIN the Bufo americanus group of North Aerica, six of nine recognized species

are syntopic with other members in the group, and in each case, natural hybridization has been documented (Blair, 1972a). Bufo woodhousii sen- su stricto (Sullivan et al., 1996), a member of the B. americanus group, is widely distributed

throughout the western United States and parts of western Canada and Mexico (Stebbins, 1985). Across its distribution, B. woodhousii hybridizes with members of the B. americanus

group, including B. americanus (Malmos, 1992), Bufo fowleri (Meacham, 1962), Bufo houstonensis (Hillis et al., 1984) and Bufo microscaphus (Sul- livan 1986, 1995). Hybridization also has been documented between B. woodhousii and more

distantly related species, including Bufo punctatus (Malmos et al., 1995), Bufo speciosus (Ballin- ger, 1966), and Bufo valliceps (Thornton, 1955). Although B. woodhousii is syntopic with Bufo alvarius and Bufo cognatus in the southwestern United States, hybridization has not been defin- itively recorded among these species (but see Bragg, 1940). These three species are not in the same species group (Blair, 1972a), but B. cognatus is a member of the group sister to the B. americanus group, whereas B. alvarius is more distantly related (Blair, 1972a; Graybeal, 1997).

Aquatic environments of the Sonoran Desert have been dramatically altered during the past century (Szaro, 1989). As a result of agricultural practices, temporary and permanent sources of water for amphibian reproduction are now plentiful in south central Arizona relative to his- toric conditions. Bufo alvarius, B. cognatus, and

B. woodhousii (Fig. 1) are all known to breed in artificial water bodies (e.g., canals, flood control

impoundments, reservoirs; Sullivan and Fernan- dez, in press), and as a result, the distributions and breeding habits of these species may have been recently altered in south central Arizona. Understanding the significance of such habitat alterations for hybridization among anurans is important both to conservation in the face of worldwide declines and to an evaluation of the evolutionary significance of hybridization.

Surveys of anurans in central Arizona during the past five years provide an opportunity to document hybridization within the genus Bufo. We describe undocumented Bufo hybrids from Maricopa County, Arizona, using morphology, allozymes, and release call characteristics. We discuss the relative merits of each character set in diagnosing hybrids, the evolution of genomic incompatability among Bufo and the significance of habitat disturbance and alteration on the breeding habits of Bufo in central Arizona.

MATERIALS AND METHODS

Putative hybrids (Fig. 2) were collected in the field on three separate dates. The 1994 hybrid was collected in an agricultural field in Mari- copa County, Arizona (Material Examined) on 17 July 1994. It was observed calling from the edge of a large, earthen canal and was identified by its atypical color pattern and odd advertisement calls. Small numbers of B. alvarius, B. cognatus, and B. woodhousi were also calling. Two 1995 hybrids were obtained from a flood control canal in Maricopa County, Arizona, on 12

? 1999 by the American Society of Ichthyologists and Herpetologists



COPEIA, 1999, NO. 2

Fig. 1. Bufo cognatus (A), B. alvarius (B), and B. woodhousii (C).

May 1995. These hybrids were first recognized by their atypical advertisement calls; about 15 B. woodhousii were calling within 50 m of the hybrids, and approximately seven B. cognatus also were heard calling in the vicinity. The 1997 hybrid was collected on 5 May 1997 while it for-

aged near the 1995 hybrid collection site. A fifth

hybrid was found deposited in the herpetologi- cal collections at Arizona State University. This 1959 hybrid was collected in Maricopa County, Arizona, on 29 June 1959.

Morphology of parental and hybrid toads was

compared qualitatively and quantitatively. Ap- parently fixed, diagnostic characters for B. al-

Fig. 2. 1995 hybrid (A), 1997 hybrid (B), and 1994 hybrid (C).

varius, B. cognatus, and B. woodhousii were as- sessed for the five hybrid toads. For B. alvarius, diagnostic characters included uniform brown or green coloration, enlarged poison glands on femur, mottled throat, and white, glandular wart at the angle of the jaw. For B. cognatus, di-

agnostic characters included keratinized boss

posterior to the nostrils and pigmented, thin, elastic vocal sac. For B. woodhousii, diagnostic characters included darkly pigmented vocal sac, and middorsal white stripe. Nine morphological measurements were taken on preserved specimens of B. alvarius (n = 25), B. cognatus (n =

31), B. woodhousii (n = 27), and the five hybrids

____ .. ___ ____ ___ ___. ___._

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using dial calipers (? 0.1 mm). Measurements included snout-vent length (SVL), head length (HL), head width (HW) measured at the angle of the jaw, parotoid gland length (PL), parotoid gland width (PW), anterior gland distance (AGS; straightline anterior distance between parotoid glands), posterior gland distance (PGS), tympanum diameter (TYMD), and tibia- fibula length (TL). For bilateral characters, only the sinistral feature was measured.

Release calls were recorded in the field or lab

by gently compressing the sides of a male toad held between thumb and forefinger directly above a microphone (following Brown and Lit-

tlejohn, 1972). Cloacal temperature was recorded with a Weber quick-recording thermometer within 5 sec of recording the release call series. For comparative purposes, release call data for B. alvarius (n = 21) were taken from Sullivan and Malmos (1994), because they surveyed populations located in north-central Maricopa County, Arizona, less than 30 km from the collection site of the 1959, 1995, and 1997 hybrids. Release calls of B. cognatus (n = 22) were obtained from three sites: Pima County, Arizona, approximately 110 km south of the collection site of the 1994 hybrid (n = 5); Rainbow Valley at the collection site of the 1994 hybrid (n =

9); and north-central Maricopa County, 30 km from the collection site of the other hybrids (n = 8). Release calls of B. woodhousii (n = 21) were obtained from a population in north-central Maricopa County, from the same location as the collection site of the 1995 and 1997 hybrids (n = 11), and from Sullivan (1989) who surveyed a population in central Maricopa County, Arizona, in the early 1980s (n = 10). Analog recordings of calls were digitized and analyzed in the manner of Sullivan et al. (1996) to obtain pulse rate (PR) and dominant frequency (DF) data.

Statistical methodology followed Sokal and Rohlf (1981) and Manly (1986). All analyses were performed using SYSTAT 5.2 for the Mac- intosh (Evanston, IL, 1992, unpubl.). We used univariate analyses to assess variation in release calls and intermediacy of hybrids. We used dis- criminant function analysis (DFA) to produce a linear function to discriminate among B. woodhousii, B. alvarius, and B. cognatus. Canonical co- efficients were standardized using sample (among groups) standard deviations. We standardized the nine variables measured for the five hybrids using the grand mean and grand standard deviation. These standardized mea- sures were then multiplied by their respective canonical coefficient for each factor variable to get CF1 and CF2 scores for each hybrid.

Four allozyme loci (Acoh-1, G3pdh, Idh-1, and Idh-2), previously found to exhibit fixed differ- ences between B. cognatus and B. woodhousii (Gergus, 1998), were assayed in the present analysis for allelic variation among B. alvarius (n = 10), B. cognatus (n = 13), B. woodhousii (n =

13), and the four hybrid toads we collected in the field. Liver and skeletal muscle extracts were

prepared and subjected to horizontal starch gel electrophoresis in the manner of Gergus (1998). Enzyme stains followed Murphy et al. (1990). Locus homologies were estimated by relative staining intensities and mobilities in

specific tissues. Electromorphs were labeled a, b, or c in order of decreasing anodal mobility.

RESULTS

The 1994 hybrid was the only hybrid with slight evidence of a boss and a vocal sac similar to B. cognatus, and a faint middorsal stripe as found in B. woodhousii; these data indicate the 1994 hybrid resulted from a B. cognatus X B. woodhousii cross. None of the five hybrids exhib- ited enlarged poison glands on the hind limbs, as found in B. alvarius. The white wart at the angle of the jaw, characteristic of B. alvarius, was faintly present in all but the 1994 hybrid. Simi- larly, all but the 1994 hybrid possessed pectoral and throat coloration most like B. woodhousii and B. alvarius but lacked any sign of a middorsal stripe or boss. These data indicate the 1959, 1995, and 1997 hybrids resulted from crosses between B. alvarius and B. woodhousii.

DFA discriminated among the parental species (Wilks' Lambda 0.007, F18,144 = 88.0, P <

0.001). The CF1 loadings (correlations between dependent variables and dependent canonical factors) were all positive and high, greater than 0.92, except PW (0.776). The CF2 loadings were nearly all negative, except HL, and low, less than 0.32. CF1 and CF2 scores of the hybrids suggested the 1994 hybrid resulted from a B. cognatus X B. woodhousii cross; the 1959 and 1995 hybrids resulted from B. woodhousii X B. alvarius crosses; and the 1997 hybrid resulted from either a B. woodhousii X B. alvarius or a B. cognatus X B. alvarius cross (Fig. 3).

Although no pulsatile substructure was evi- dent in the release calls of one of the 1995 hybrids, release call pulses of all other hybrids had a rapid onset, similar to the within pulse group pulsation of B. alvarius and B. cognatus but un- like toads of the B. americanus group, such as B. woodhousii. Release call PR (about 10 p/s) of B. cognatus was similar to B. alvarius (about 10 p/ s) but much lower than B. woodhousii (about 100 p/s; Table 1). PR of hybrids (about 75 p/s) were

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COPEIA, 1999, NO. 2

CM 04 O I- o

LL -J

z

z Z

o

+ 1959 hybrid ? 1994 hybrid * 1995 hybrids A 1997 hybrid

2.5

0 B. cognatus 1.5- O O

Q [ EA 0 : E ) 0.5 +O []

00

;:~~ ~ A^~ ~ ~~ 4~ ~B. alvanrius

-1.5- A4

B. woodhousii A

-2.5 I I a viu -2.5

Fig. 3. Plot the discriminan

similar to B.

shape. Given tures of the i ferences in b for variation i varius was lov release calls c

TABLE 2. GENOTYPES FOR PURE Bufo alvarius (n = 10), B. cognatus (n = 13), B. woodhousii (n = 13), AND FOUR PUTATIVE HYBRID TOADS AT FOUR ALLOZYME LOCI.

Buffer conditions for each locus are given below.

Locus Acoh-1* G3pdh** Idh-l*** Idh- Sample 2***

B. alvarius aa bb aa aa B. cognatus bb aa cc aa B. woodhousii cc bb bb bb 1994 hybrid bc ab bc ab 1995/1997 hybrids ac bb ab ab

* Amine-citrate (morpholine), pH 6.1; ** Tris-borate-EDTA I, pH 8.6; ** Triscitrate II, pH 8.0.

-1.5 -0.5 0.5 1.5 2.5 housii and either B. alvarius or B. cognatus. Com- CANONICAL FACTOR 1 pared to the 1995 and 1997 hybrids, the 1994

of canonical variables and 2 from hybrid displayed different genotypes at Acoh-1, of canonical variables 1 and 2 from . . t funcon analysis. See text for details. G3dh, and Idh-1. The Acoh-1 and Idh-1 loci both it function analysis. See text for details. P

unequivocally identified the 1994 hybrid as the result of a B. cognatus X B. woodhousii cross.

woodhousii in rate but not pulse G3pdh, however, equivocally supported either a the small range in body tempera- B. alvarius X B. woodhousii or B. cognatus X B. ndividuals sampled (Table 1), dif- woodhousii hybridization event. Thus, for most

ody temperature did not account loci scored, allozyme genotypes were those ex- in PR. DF of release calls of B. al- pected if 1995 and 1997 hybrids were B. alvarius r (below 1000 Hz), whereas DF of X B. woodhousii and the 1994 hybrid was B. cog- )f R cmnnatrus was hiorh (ahbot 2300 natus X B. woodhousii.

Hz). DF of release calls of B. woodhousii and the putative hybrids was intermediate: 1250-1750 Hz. In both PR and DF, release calls of hybrids were closest to B. woodhousii rather than strictly intermediate to any pair of parental forms.

Parental contributors to hybrids were deter- mined with four allozyme loci based on inferred genotypes of hybrid and nonhybrid toads (Ta- ble 2). Allozyme variation at two loci (Acoh-1 and Idh-1) indicated that the 1995 and 1997 hybrids resulted from crosses between B. alvarius and B. woodhousii, and the inferred genotypes at the G3pdh locus excluded B. cognatus as a parental contributor. For all hybrids, Idh-2 equivocally indicated hybridization between B. wood-

DISCUSSION

All putative hybrids possessed morphological, release call, and allozyme traits suggestive of hybrid parentage. In summary, data are concor- dant with the conclusion that the 1994 hybrid is a B. cognatus X B. woodhousii, the 1995 and 1997 hybrids are B. alvarius X B. woodhousii, and the 1959 hybrid is most likely a B. alvarius X B. woodhousii. These results are consistent with pre- vious observations that B. woodhousii is able to hybridize with relatively distantly related species (Thornton, 1955; Ballinger, 1966; Malmos et al., 1995); B. woodhousii hybridizes with four B. amer-

TABLE 1. MEAN ? SE FOR PULSE RATE (PR) AND DOMINANT FREQUENCY (DF) OF RELEASE CALLS, AND RANGES FOR SNOUT-VENT LENGTH (SVL) AND CLOACAL TEMPERATURE (CT) OF POTENTIAL PARENT SPECIES. Individual

values for each hybrid also are given.

n PR (p/s) DF (kHz) SVL (mm) CT (C)

Bufo alvarius 24 10.6 ? 1.9 0.994 ? 0.020 137-162 23-28.5 Bufo cognatus 21 10.3 ? 0.4 2.307 ? 0.047 69-81 22-31.9 Bufo woodhousii 22 95.2 ? 1.9 1.550 ? 0.125 77-93 21.8-23.2 1994 hybrid 1 67.9 1.638 81 22.5 1995 hybrid 1 - 1.304 92 21.8 1995 hybrid 1 74.4 1.230 106 22.0 1997 hybrid 1 78.9 1.191 105 27.6

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icanus group species and species of at least three

outgroups to the B. americanus group, including B. cognatus and B. speciosus of the B. cognatus group, B. punctatus, and B. alvarius and B. val-

liceps which are both members of an unnamed clade (Graybeal, 1997).

Blair (1972b) conducted artificial hybridization experments to hypothesize phylogenetic re-

lationships among members of Bufo. These crosses provided insights into the relative genomic compatability of B. alvarius, B. cognatus, and B. woodhousii. In crosses of female B. alvarius with males of five B. americanus group species, including B. woodhousii, hybrids failed as

gastrulae or neurulae (Blair, 1972b); artificial crosses were not conducted between male B. alvarius and female B. woodhousii. In artificial mat-

ings between female B. cognatus and male B. woodhousii, the embryos were lost as abnormal larvae or failed at earlier stages, whereas, when female B. woodhousii were crossed with male B.

cognatus, less than 80% of the larvae successfully metamorphosed (Blair, 1972b). These labora- tory experiments suggest limited genomic compatability between B. cognatus and B. woodhousii and limited to no genomic compatability between B. alvarius and B. woodhousii. Testes of hybrids we examined (1994, 1995, 1997) were similar in size and shape to those of typical males of the parental forms, and the 1995 and 1994 hybrids were producing advertisement calls when collected. Despite the presence of these secondary sexual characteristics, the reproductive competency of these hybrids may be com- promised; sperm may in fact be nonfunctional, and aberrant advertisment calls may serve little or no function in mate attraction.

Although relatively few fossils of Bufo have been discovered (Tihen, 1972), some fossils do provide a framework in geologic time for inter- preting the possible age of the B. americanus, B. cognatus, and B. alvarius species groups and the amount of time available for genomic incompatability to have evolved. Fossilized members of either the B. americanus or B. cognatus species groups have been reported from the end of the Miocene (Estes and Tihen, 1964). Bufo praevis, described from the late Lower Miocene, ap- pears to be a member of the clade including the B. debilis and B. americanus groups (Tihen, 1962). The discovery of B. praevis suggests the clade containing the B. americanus, B. cognatus, and B. debilis groups is at least six million years old. Bufo alvarius is a member of a clade more ancient to this (Graybeal, 1997). These data indicate limited genomic compatability between B. alvarius and B. woodhousii has been retained despite six million years since the clades to

which they belong diverged from their imme- diate common ancestor. Our observations suggest that some level of natural reproductive compatability of Bufo may be retained across nu- merous speciation events and for extraordinari- ly long periods of time.

Several proximate factors may account for hybridization of Bufo in Arizona. In southern Ari- zona, B. alvarius and B. cognatus principally breed during the summer rainy season (July and August) and generally are restricted to rel-

atively open, rain-formed pools in lowland desert environments. Bufo woodhousii generally breeds during the spring (although limited ac-

tivity can occur in the summer) and typically occurs in temporary or permanent sources of water associated with large riparian systems (e.g., the Gila and Salt Rivers). Agricultural practices of the past 100 years have altered lowland and riparian habitats, thereby increasing opportunities for hybridization. Also, some have

suggested variability in social structure (e.g., alternative mating tactics) can influence opportunities to hybridize. For example, frequent natural hybridization in the genus Bufo may be due in part to active searching by males for females (Haddad et al., 1990). Such mating tactics may influence the potential for hybridization, espe- cially if habitat disturbance is increasing the in- cidence of social interactions between species.

MATERIAL EXAMINED

Bufo alvarius: ASU 30518, 30639-30642, 30644-30645: AZ: Pima Co.; Highway 286 at "Vekol Wash." ASU 30646-30652, 30658, 30662, 30742: AZ: Maricopa Co.; Adobe Dam, 43rd Ave. loop south of Pinnacle Peak Rd. ASU 30745-30747, 30750-30752, 30754-30755: AZ: Maricopa Co.; Cave Creek, Cave Buttes, Jomax Rd. Bufo cognatus: ASU 30532, 30534, 30536- 30540: AZ: Maricopa Co.; Rainbow Valley, Chan- dler Heights Rd. east of Rainbow Valley Rd. ASU 30766-30768, 30770-30772: AZ: Maricopa Co.; Cave Creek, Cave Buttes, Jomax Rd. ASU 30777-30779, 30781-30795: AZ: Maricopa Co.; Skunk Creek at Adobe Dam. Bufo woodhousii: ASU 28834, 28836: AZ: Maricopa Co.; New Riv- er at Bell Rd. ASU 30356-30359, 30368: AZ: Maricopa Co.; Sun Valley Parkway, 6 mi. W. of the Agua Fria River on Bell Rd. ASU 30489, 30497, 30499-30503: AZ: Maricopa Co.; New River at Deer Valley Rd. crossing. ASU 30504- 30512, 30514-30515: AZ: Maricopa Co.; Canal SE of Thunderbird Rd. and 59th Ave. ASU 30541-30542: AZ: Maricopa Co.; Rainbow Val- ley, Chandler Heights Rd. E. of Rainbow Valley Rd. 1959 Hybrid: ASU 2601: AZ: Maricopa Co.;

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COPEIA, 1999, NO. 2

Paradise Valley, Thunderbird Academy N. of Scottsdale. 1994 Hybrid: ASU 30527: AZ: Mari-

copa Co.; Rainbow Valley, Chandler Heights Rd. E. of Rainbow Valley Rd. 1995 Hybrids and 1997

Hybrid: ASU 30740-30741, ASU 30821: AZ:

Maricopa Co.; Canal SE of Thunderbird Rd. and 59th Ave.

ACKNOWLEDGMENTS

R. Bowker, M. Demlong, and M. Flowers as- sisted with some observations. We thank three

anonymous reviewers for helpful comments. All work was conducted in accordance with an IA- CUC protocol, and specimens were collected under Arizona Game and Fish Department col-

lecting permits SLVN0000173 and SP593039.

LITERATURE CITED

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. 1972b. Evidence from hybridization, p. 196- 232. In: Evolution in the genus Bufo. W. F. Blair (ed.). Univ. of Texas Press, Austin.

BRAGG, A. N. 1940. Observations on the ecology and natural history of Anura. II. Habits, habitats, and

breeding behavior of Bufo woodhousii woodhousii (Gi- rard) in Oklahoma. Am. Midi. Nat. 24:306-321.

BROWN, L. E., AND M. J. LITTLEJOHN. 1972. Male release call in the Bufo americanus group, p. 310-323. In: Evolution in the genus Bufo. W. F. Blair (ed.). Univ. of Texas Press, Austin.

ESTES, R., AND J. A. TIHEN. 1964. Lower vertebrates from the Valentine Formation of Nebraska. Am. Midi. Nat. 72:453-472.

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HILLIS, D. M., A. M. HILLIS, AND R. F. MARTIN. 1984.

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MALMOS, K. B. 1992. Morphology, mating calls, and allozymes of Bufo a. americanus and Bufo w. woodhousii from a hybrid zone in eastern Nebraska and western Iowa. Unpubl. master's thesis, Univ. of Ne- braska, Omaha.

, R. REED, AND B. STARRETT. 1995. Hybridiza- tion between Bufo woodhousii and Bufo punctatus from the Grand Canyon region of Arizona. Great Basin Nat. 55:368-371.

MANLY, B. F.J. 1986. Multivariate statistical methods: a primer. Chapman and Hall Press, London.

MEACHAM, W. R. 1962. Factors affecting secondary intergradation between two allopatric populations in the Bufo woodhousei complex. Am. Midi. Nat. 67: 282-304.

MURPHY, R. W., J. W. SITES, JR., D. G. BUTH, AND C. H. HAUFLER. 1990. Proteins. I. Isozyme electrophoresis, p. 45-126. In: Molecular systematics. D. M. Hillis and C. Moritz (eds.). Sinauer Associates, Sun- derland, MA.

SOKAL, R. R., AND F. J. ROHLF. 1981. Biometery. W. H. Freeman and Company, New York.

STEBBINS, R. C. 1985. A field guide to western reptiles and amphibians. 2d ed. rev. Houghton Mifflin Co., Boston, MA.

SULLIVAN, B. K. 1986. Hybridization between the toads Bufo microscaphus and Bufo woodhousei in Ari- zona: morphological variation. J. Herpetol. 20:11- 21.

1989. Interpopulational variation in vocali- zations of Bufo woodhousii. Ibid. 23:368-373.

. 1995. Temporal stability in hybridization between Bufo microscaphus and Bufo woodhousii (Anura: Bufonidae): behavior and morphology. J. Evol. Biol. 8:233-247.

, AND P. S. FERNANDEZ. 1999. Breeding activity, estimated age-structure, and growth in Sonoran De- sert anurans. Herpetologica 55:xx-xx.

, AND K. B. MALMOS. 1994. Call variation in the Colorado River Toad (Bufo alvarius): behavioral and phylogenetic implications. Ibid. 50:146-156.

, AND M. F. GIVEN. 1996. Systematics of the Bufo woodhousii complex (Anura: Bufonidae): advertisement call variation. Copeia 1996:274-280.

SZARO, R. C. 1989. Riparian forest and scrubland

community types of Arizona and New Mexico. De- sert Plants 9:69-138.

THORNTON, W. A. 1955. Interspecific hybridization in

Bufo woodhousei and Bufo valliceps. Evolution 9:455- 468.

TIHEN, J. A. 1962. A review of New World fossil bu- fonids. Am. Midl. Nat. 68:1-50.

.1972. The fossil record, p. 8-13. In: Evolu- tion in the genus Bufo. W. F. Blair (ed.). Univ. of Texas Press, Austin.

(EG, KM) DEPARTMENT OF ZOOLOGY, ARIZONA STATE UNIVERSITY, TEMPE, ARIZONA 85287- 1501; AND (BS) DEPARTMENT OF LIFE SCIENC-

ES, ARIZONA STATE UNIVERSITY WEST, 4701 WEST THUNDERBIRD ROAD, PHOENIX, ARIZONA

85069-7100. E-mail: (EG) [email protected]. Send reprint requests to EG. Submitted: 6 April 1998. Accepted: 24 Nov. 1998. Section editor: A. H. Price.

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Documents

Natural Hybridization among Distantly Related Toads (Bufo alvarius, Bufo cognatus, Bufo woodhousii) in Central Arizona