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Home , Eastern newt, Newt, Notophthalmus, Striped newt, Taricha

Bull. Chicago Herp. Soc. 41(8):149-153, 2006

The “False Breeding Season” of the Eastern , viridescens David M. Sever Department of Biological Sciences Southeastern Louisiana University Hammond, LA 70402

Abstract The terrestrial red eft stage is so different from the body form of the aquatic adult of the that the two were considered separate species for nearly 60 years. Some populations lack the eft stage whereas in other populations the adults are aquatic only during the breeding season. In populations in which the adults are permanently aquatic or migrate to breeding ponds in fall, an autumnal mating season may occur, which has been termed the “false breeding season” because oviposition does not occur until the spring mating season. However, this period is not “false” but rather the early portion of an extended mating season made possible by female sperm storage.

The eastern newt, Notophthalmus viridescens, is one of the I became interested in variation in the life history of most widely distributed in North America, and can Notophthalmus viridescens when studying female sperm storage be found from eastern Texas northward to Canada and then in a population of red-spotted on the Department of eastward to the Atlantic coast (Petranka, 1998). Four subspe- Energy’s Savannah River site, near Aiken, South Carolina cies are recognized. A great deal of literature exists on the life (Sever et al., 1996). In the pond inhabited by the newts we history of the eastern newt, but most of it concerns the north- studied, mating took place from December into April, and eastern form, the red-spotted newt, N. v. viridescens. Much of females, which do indeed store sperm in cloacal spermathecae, this interest was sparked by the discovery that many popula- kept laying through May. Then something remarkable tions have pond-dwelling, aquatic adults and larvae, but the happened: all of the newts vanished from the pond, not to be larvae metamorphose into an immature “red eft” stage that seen in the water again until the following October. Thus, the leaves the water and assumes a terrestrial existence for any- adult “aquatic” stage was not a permanent condition; even the where from one (Gibbons and Semlitsch, 1991) to seven adults in this population had a terrestrial phase. (Healy, 1974) years. Red efts, especially younger ones, can be I wanted to see how widespread this condition was in the bright vermilion and have granular skin, but as efts reach literature, but the more I delved into past studies, the more I maturity, the morphology changes once again as the was impressed with just how much variability exists. The migrate back to aquatic, generally lentic (Petranka, literature is quite extensive, but serious gaps exist in our 1998). The adult animals are a shade of green dorsally, and knowledge of life histories of eastern newts, especially western have compressed tails. In N. v. viridescens, both the eft and and southern populations. Studies on the northern red-spotted the adult have a lateral row of red spots bordered by black, newt, however, date back into the nineteenth century. One resulting in the traditional common name. In the other sub- aspect of the life history of the red-spotted newt that has come species, the red spots are either absent (central newt, N. v. under much scrutiny is the timing of the breeding season, louisianensis and the Florida peninsula newt, N. v. piaropicola) especially if an autumnal “false breeding season” exists. In or form a series of broken lines (broken-, N. v. this paper, I review some of the relevant literature dealing with dorsalis). Aquatic adult males develop especially prominent the timing of the breeding season in Notophthalmus viridescens. tail fins during the breeding season. The aquatic adult and the I emphasize the older literature, which is not easily accessible. terrestrial eft are so different that the original descriptions by First, however, I shall review the nomenclatural history of the Rafinesque (1820) placed them in different subgenera, and the species, and the relationship of the to discoveries controversy over whether they represented different species or about the life history of the red-spotted newt. not was not definitely settled until Cope (1889). The existence of a terrestrial stage and an aquatic stage is Taxonomic History not just limited to Notophthalmus viridescens, but is generally The eastern newt was first described by the great American characteristic of all salamanders within the naturalist Constantine Samuel Rafinesque (Rafinesque, 1820). referred to as “newts” (including other species in the genus As mentioned previously, he placed the adult form and the red Notophthalmus and those in the genera Cynops, , Tri- eft in different subgenera; the genus he choose for both was turus plus some more obscure taxa), and is the reason for , a genus Rafinesque described in 1815 that contains separating out these species by this common designation from the European newts. The adult form, with a type locality of other salamanders. Within Notophthalmus viridescens, how- “Lake George, Lake Champlain” in New York, was designated ever, some populations contain paedomorphic individuals, Triturus (Diemictylus) viridescens (vulgar name, “Green which do not fully metamorphose (i.e., larval are retained) Ebbet”), and the eft, with no type locality except in the broad- and which may spend their entire life in a permanent pond est terms (“states of New York, New Jersey, Connecticut, (Noble, 1926, 1929; Brandon and Beemer, 1966; Healy, 1974; Vermont, etc.”), was named Triturus (Notophthalmus) miniatus Reilly, 1986, 1987).

149 (“Red Ebbet”). 1962 that because Baird (1850) first referred viridescens to Notophthalmus rather than Diemictylus, that Notophthalmus Spencer Fullerton Baird, founder of the herpetological had preference under the rule of first revisor (ICZN, 1962). collections at the Smithsonian Institution, removed the two forms from Triturus, although he kept them as different spe- Variation in Life History cies. Baird (1850) noted, however, “Thus, of the highly natu- ral genus Notophthalmus (Diemyctylus) one species (Diemycty- The first review of the life-history of the red-spotted newt lus viridescens) is the most aquatic of all American forms, the was by Gage (1891). He opened his paper by stating: “The other (D. miniatus) the most terrestrial; yet the two are so working out of the complete life-history of this newt has extend- much alike in shape as to render it a matter of some difficulty ed from 1819SQ 1820, when Say and Rafinesque first considered to distinguish them.” Note that Baird seemingly considered the it, until the present year. . . . During this period of seventy- genera Notophthalmus and Diemictylus interchangeable, but he two years it has been the subject of numerous investigations; mentioned Notophthalmus first, which gave that name priority. but from the striking changes in coloration, habit, and structure Also, Baird (1850) misspelled Diemictylus, and this mistake passed through in its various stages of development it has was perpetuated for the rest of the nineteenth century. proved unusually puzzling to the naturalist and physiologist.” Edward Hallowell, a Philadelphia physician best known for Gage (1891) established that fertilization in Notophthalmus his work on reptiles, expressed even stronger doubts about viridescens was internal, by isolating four females from New separation of the forms into different species. He stated York from any males. All laid fertile eggs. Gage believed that (Hallowell, 1856), “Diemyctylus viridescens and D. miniatus only 6SQ 7 eggs can be laid before a female requires an additional are probably the same, the orange color and roughness being mating. In New York, the mating/oviposition period was appearances which, the female more especially, presents after a AprilSQ June. Gage, however, noted that specimens from au- long sojourn on land. At least this may be inferred from the tumn appeared to be in breeding condition, and if “the two known habits of European Tritons.” sexes are placed together a typical mating will occur, and the emission of spermatophores will occur exactly as described for The noted American herpetologist and paleontologist Ed- the spring, or proper breeding season. . . . It is not easy to ward Drinker Cope commented on the eastern newt in 1859 in understand the purpose of this autumnal mating, as no eggs his first publication, written at the age of 18. Cope (1859) were ever found in the oviducts in autumn, and it is not known wrote, “We include in the above synonyms (of Diemyctylus whether ovulution [sic] takes place at other times than in the viridescens) those of the nominal species D. miniatus, which spring. . . .” we think with Dr. Hallowell (’56) is a state of D. virides- cens. . . . The color or character of the skin seems to be de- Jordan (1893), studying a population in Massachusetts, noted pendent upon the amount of moisture in the situations in which that that observations of fall mating by Gage were based upon they are found. Those from high and dry spots are redder and captive specimens, where their sexual activity may be due merely rougher than those from marshy situations.” to the “forced association of the two sexes . . . at a somewhat higher temperature than . . . their natural . . . .” How- Definitive evidence that the forms were the same species did ever, Jordan also observed “on several occasions in the autumn not come for nearly 20 more years when Kelly (1878) reported months . . . pairs in the ponds engaged in the preliminary that he “. . . brought home a number of Diemyctylus miniatus ‘Liebesspeil,’ but have at no time observed any approach to Raf., or little red or red eft, and after keeping them in a such an outbreak of sexual susceptibility as occurs in early dark box filled with saturated moss, they changed their color spring. . . . [I] think that production of spermatophores may from a bright vermilion to the olive state characteristic of the take place sporadically in the autumn under natural conditions.” D. viridescens. . . . The conclusion, then, is that instead of two well-marked species or a species and a variety, we have but a Jordan (1893) further reported, “The seminal receptacles of single species, Diemyctylus miniatus.” Subsequently, Monks females captured in the autumn usually contain spermatozoa, (1880), Pike (1886), and Gage and Norris (1890) all reported although not in the same abundance as in spring. One may transformations of captive red efts into the adult form. account for the presence of the spermatozoa by supposing either that they are the acquisition of a recent mating, or that Cope (1889) in his magnificent tome The Batrachia of North they have been kept over from the preceding spring. It is America summarized the available literature and concluded, possible that both explanations are valid in individual cases. . . . “There are two forms of this subspecies, which have received Females that have been kept in confinement all winter are not the names of viridescens and miniatus. . . . These have been apt to lay eggs in the spring as are individuals freshly captured.” shown to be stages of one and the same ; they are not Jordan noted that in the spring, the ovipository season extended distinguished otherwise than as seasonal forms, which may be from April until the end of June, but that a given female proba- by reason of the environment rendered permanent for a longer bly lays eggs for no more than eight weeks. One female laid or shorter time.” Cope settled on viridescens as the specific 96 eggs between April 24 and May 13, after being isolated name because it was mentioned first in the publication from males (also reported in Jordan, 1891). Jordan thus rea- (Rafinesque, 1820) that described both viridescens and minia- soned that Gage was in error when he stated only 6SQ 7 eggs tus. But in another twist, Rafinesque also used the generic could be fertilized by one mating: “ It does not seem to me name Diemictylus prior to using Notophthalmus. However, the necessary that more than one mating should occur in a single International Commission on Zoological Nomenclature ruled in season, but I agree with Gage that in a state of nature several

150 matings of the same female may and frequently do take place.” Mount (1975) in Alabama, and Trauth et al. (2004) in Arkan- Jordan also was the first author to propose that fertilization sas; January to May by Minton (2001) in Indiana; and February occurs not in the oviducts, but as the eggs pass through the to May by Gibbons and Semlitsch (1991) on the Savannah cloaca. River Site in South Carolina. None of these authors mentioned aquatic adults leaving ponds for terrestrial habitats. Pope (1924) based his observations on populations he stud- ied in Illinois (which would be N. v. louisianensis) and six Healy (1974, 1975) studied a population in coastal Massa- northeastern states (Maine, Massachusetts, New Hampshire, chusetts, and definitely stated that adults do not leave the pond. New York, New Jersey, Pennsylvania). “The curious phenom- The terrestrial eft stage was 3SQ 7 years. Some newts were enon of mating and depositing spermatophores in the fall has paedomorphic, however, and therefore omitted the eft stage. been recorded by both Gage and Jordan, but neither is able to The paedomorphs were able to reproduce for the first time at account for it. I have observed it both in the field and the age two, which gave them a significant reproductive advantage laboratory, but can see no real explanation. The fact that no over individuals with an eft stage. Whether mating occurred in eggs are laid in the fall seems to make it quite superfluous. I fall was not mentioned, but if mating was limited to spring, believe, however, that it is merely a preliminary to the spring that would be quite different than the reports of Jordan (1893) mating season. . . . [M]ating begins in fall, being interrupted and Adams (1940) on red-spotted newts in Massachusetts. only by the period of inactivity due to cold weather, and begin- A few studies on populations in the North report that some ning again in the spring, as soon as the temperature of the or all of the adult newts leave the ponds in the summer (some- water begins to rise. Newts left in the laboratory will continue times because the ponds have dried up) and spend the fall and/ mating all winter to some extent, though not as actively as or winter on land. Hurlbert (1969) in New York found both a when first captured. I have also seen mating in the middle of fall and a spring migration to the breeding sites. The fall mi- July after the usual mating season was over.” grations almost exclusively involved efts, maturing individuals Adams (1940), like Jordan, studied newts in Massachusetts. returning to the water for the first time. Whether or not mat- Male newts contained abundant sperm in their vasa deferentia ing among these maturing individuals occurred in fall was not from September through May, and some specimens even re- mentioned by Hurlbert (1969). The spring migration included tained a few sperm during the midsummer months. Sperm adults that apparently had hibernated on land. were found in the spermathecae of females “. . . examined in (1978) and Massey (1990) in the mountains of Virginia, every month of the year but they are especially abundant in the reported a breeding migration in March and April to the ponds, fall and spring.” Oviposition, however, was strictly limited to and an August to September emigration to terrestrial hibernacu- the spring. Out of hundreds dissected, only one female collect- la. Breeding occurred from mid-March to late June (Massey, ed during the fall and winter had an oviducal , whereas in 1988), and no fall breeding season existed (Massey, 1990). AprilSQ June, eggs were found in the oviducts of some newts High mortality was found among adults; Gill (1978) found the from every collection. In both males and females, “The go- average female was expected to breed 1.3 times, and Massey nads are in a preparatory growth state during the summer and (1990) found that 75% of the females that bred one year did not by October have attained the mature condition which results in appear in the subsequent year. However, a year after breeding, a false breeding season. . . . The true breeding season of the eight females were recaptured, apparently in April, in pit traps spring and the false one of the autumn were both observed as around a partially fenced pond (Massey, 1990). Seven of the Gage (1891), Jordan (1893) and Pope (’24) have described females had sperm in their spermathecae, although it was not them.” abundant, indicating no recent insemination. Massey (1990) Neither Gage (1891), Jordan (1893), Pope (1924) nor concluded that the sperm were retained from a previous breed- Adams (1940) mentioned whether the adults in the newt popu- ing season, and therefore, these females were inseminated in lations they studied remained aquatic all year, but clearly, the June of the previous year at latest. Thus, these females had matings that were observed in fall and spring were based upon stored sperm for at least 10 months. The viability of the sperm specimens observed in or collected from ponds. and whether they were in sufficient quantity to fertilize eggs was unknown, but Massey suggested the possibility of between Bishop (1941), in his monograph on the salamanders of breeding season sperm competition. New York, reported once again a false breeding season in the fall in which courtship occurs and spermatophores may be However, the pond used in the study by Massey was only deposited although no eggs are laid. Bishop always referred to partially fenced, and, as noted by Hurlbert (1969), newts the adults as “aquatic,” implying that once they mature and following their arrival at a pond wander back and forth be- enter ponds, they stay there permanently. Bishop mentioned tween water and land, a phenomenon also recorded in other fall and spring migrations from terrestrial habitats to ponds, but species, and termed “wandering behavior” (Pimentel, 1960; these migrations apparently consisted of maturing efts. Hasumi and Iwasawa, 1992). Thus, the female newts could have mated in the current season in this or another pond. Also, Only a few other state or regional field guides or handbooks if the males in this population are typical of others reported seem to report original data on this wide-ranging species, and from northern states during the fall and winter (Adams, 1940), even these accounts are mostly anecdotal and lack substantive the males do possess sperm in their vasa deferentia from Sep- data. For example, the breeding seasons were simply charac- tember onward, and one cannot definitely rule out a fall mat- terized as: winter and early spring by Smith (1961) in Illinois, ing.

151 Finally, a study on a related species, Taricha granulosa, is in the spermathecae if females, indicating mating activity, until noteworthy. Specker and Moore (1980) reported, “Male newts December. exhibit reproductive behaviors during the fall when androgen The fact that early authors wondered why mating occurred levels are high. In fact, male courtship behaviors of amplectic in the fall when no egg-laying was happening indicates that clasping are observed in the ponds during all but the summer they underestimated the significance of female sperm storage. months, when androgen levels are lowest. We suspect that the Sperm storage allows the decoupling of mating activity form sexual behaviors which occur during the fall are false-breeding oogenesis, ovulation, fertilization and/or oviposition. The activities and no spermatophores are deposited.” decoupling of these activities furthermore allows extension of the mating season and facilitates multiple matings, which are Conclusions known to occur in Notophthalmus viridescens (Gabor et al., As a working hypothesis, a “false breeding season” in the 2000). Thus the “false breeding season” is not really “false”, fall occurs in populations in the northern states in which the it is simply the early portion of an extended mating season. No adults do not leave the pond in summer or fall for winter hiber- one knows how long a female eastern newt can effectively store nation on land, either because they are permanently aquatic or sperm, but a period of six months is certainly known in other because they migrate to breeding ponds in fall and overwinter salamanders (Sever et al., 1996), and the 10 months suggested in them (Gage, 1891; Jordan, 1891, 1893; Pope, 1924; Adams, by Massey (1990) is not beyond reason. 1940). Northern populations of eastern newts that do not The geographic variation in breeding cycles of this wide- engage in pre-hibernation mating are those that hibernate on spread species certainly deserves more study. The basic ques- land and do not migrate to ponds until spring (Hurlbert, 1969; tion remains: why do some populations hibernate on land Gill, 1978; Massey, 1990). In the population we studied in whereas others migrate to ponds (or never leave them) and South Carolina, hibernation does not occur so mating is not commence mating in fall? This review on the breeding cycle of interupted, and indeed midwinter is the height of the breeding the eastern newt illustrates that we still lack basic knowledge season (Sever et al., 1996). Note also that we first found about the life histories of even our most common . adults back in the pond in October, but we did not find sperm

Literature Cited Adams, D. E. 1940. Sexual conditions in Triturus viridescens III. The reproductive cycle of the adult aquatic form of both sexes. American Journal of Anatomy 66:235-275. Baird, S. F. 1850. Revision of the North American tailed-Batrachia, with descriptions of new genera and species. Journal of the Academy of Natural Sciences Philadelphia, 2nd series, 1:281-294. Bishop, S. C. 1941. The salamanders of New York. New York State Museum Bulletin 324:1-365. Brandon, R. A., and D. J. Beemer. 1966. Neotenic newts, Notophthalmus viridescens louisianensis, in southern Illinois. Herpetologica 22:213-217. Cope, E. D. 1859. On the primary divisions of the Salamandridae, with descriptions of two new species. Proceedings of the Academy of Natural Sciences Philadelphia 11:122-128. ))))))). 1889. The Batrachia of North America. U.S. National Museum Bulletin 34:1-525. Gabor, C. R., J. D. Krenz and R. G. Jaeger. 2000. Female choice, male interference, and sperm precedence in the red-spotted newt. Behavioral Ecology 11:115-124. Gage, S. H. 1891. Life-history of the vermilion-spotted newt (Diemyctylus viridescens Raf.). American Naturalist 25:1084-1110. Gage, S. H., and H. W. Norris. 1890. Notes on the Amphibia of Ithaca. Proceedings of the American Association for the Advancement of Science 39:338-339. Gibbons, J. W., and R. D. Semlitsch. 1991. Guide to the reptiles and amphibians of the Savannah River Site. Athens: University of Georgia Press. Gill, D. E. 1978. The metapopulation ecology of the red-spotted newt, Notophthalmus viridescens (Rafinesque). Ecological Monographs 48:145-166.

Hallowell, E. 1856. Description of several species of Urodela, with remarks on the geographic distribution of the caducibranchiate division of these animals and their classification. Proceedings of the Academy of Natural Sciences Philadelphia 8:6-11. Hasumi, M., and H. Iwasawa. 1992. Wandering behavior and cutaneous changes in winter-dormant male salamanders (Hynobius nigrescens). Herpetologica 48:279-287. Healy, W. R. 1974. Population consequences of alternative life histories in Notophthalmus v. viridescens. Copeia 1974:221-229.

152 ))))))). 1975. Breeding and postlarval migrations of the red-spotted newt, Notophthalmus viridescens, in Massachusetts. Ecology 56: 673-680. Hurlbert, S. H. 1969. The breeding migrations and interhabitat wandering of the vermilion-spotted newt Notophthalmus viridescens (Rafinesque). Ecological Monographs 39:465-488. ICZN (International Commission on Zoological Nomenclature). 1962. Opinion 635. Bulletin of Zoological Nomenclature 19:152-154. Jordan, E. O. 1891. The spermatophores of Diemyctylus. J. Morphology 5:263-270. ))))))). 1893. The habits and development of the newt (Diemyctylus viridescens). J. Morphology 8:269-366. Kelly, H. A. 1878. Identity of Diemyctylus miniatus with D. viridescens. American Naturalist 12:399. Massey, A. 1988. Sexual interactions in red-spotted newt populations. Animal Behaviour 36:205-210. ))))))). 1990. Notes on the reproductive ecology of red-spotted newts (Notophthalmus viridescens). J. 24:106-107. Minton, S. A., Jr. 2001. Amphibians and reptiles of Indiana, 2nd ed. Indianapolis: Indiana Academy of Science. Monks, S. P. 1880. The spotted . American Naturalist 14:371-374. Mount, R. H. 1975. The reptiles and amphibians of Alabama. Auburn, Alabama: Auburn University Agricultural Experimental Station. Noble, G. K. 1926. The Long Island newt: A contribution to the life history of Triturus viridescens. American Museum Novitates 228:1-11. ))))))). 1929. Further observations on the life-history of the newt, Triturus viridescens. American Museum Novitates 348:1-22. Petranka, J. W. 1998. Salamanders of the United States and Canada. Washington, D.C.: Smithsonian Institution Press. Pike, N. 1886. Some notes on the life-history of the common newt (Diemyctylus miniatus viridescens). American Naturalist 20:17-25. Pimentel, R. A. 1960. Inter- and intrahabitat movements of the rough-skinned newt, Taricha torosa granulosa (Skilton). American Midland Naturalist 63:470-496. Pope, P. H. 1924. The life-history of the common water-newt (Notophthalmus viridescens), together with observations on the sense of smell. Annals Carnegie Museum 15:305-362. Rafinesque, C. S. 1820. Annals of nature or annual synopsis of new genera and species of animals, plants, etc. discovered in North America. Lexington, Kentucky: Thomas Smith . Reilly, S. M. 1986. Ontogeny of cranial ossification in the eastern newt, Notophthalmus viridescens (: Salamandridae), and its relationship to and neoteny. J. Morphology 188:315-326. ))))))). 1987. Ontogeny of the hyobranchial apparatus in the salamanders Ambystoma talpoideum (Ambystomatidae) and Notophthalmus viridescens (Salamandridae): The ecological morphology of two neotenic strategies. J. Morphology 191:205-214. Sever, D. M., L. C. Rania and J. D. Krenz. 1996. The annual cycle of sperm storage in spermathecae of the red-spotted newt, Notophthalmus viridescens (Amphibia: Salamandridae). J. Morphology 227:155-170. Smith, P. W. 1961. The amphibians and reptiles of Illinois. Illinois Natural History Survey Bulletin 28:1-298. Specker, J. L., and F. L. Moore. 1980. Annual cycle of plasma androgens and testicular composition in the rough-skinned newt, Taricha granulosa. General and Comparative Endocrinology 42:297-303. Trauth, S. E., H. W. Robison and M. V. Plummer. 2004. The amphibians and reptiles of Arkansas. Fayetteville: The University of Arkansas Press.

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