Prolonged Cycles as a Common Reproductive Pattern in ... - BioOne

Journal of Herpetology, Vol. 38, No. 1, pp. 73–79, 2004 Copyright 2004 Society for the Study of Amphibians and Reptiles

Prolonged Cycles as a Common Reproductive Pattern in Viviparous Lizards from Patagonia, Argentina: Reproductive Cycle of Phymaturus patagonicus NORA R. IBARGUËNGOYTIÁ Departmento de Zoologıá, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue. Unidad Postal Universidad del Comahue, Bariloche, 8400, Rıó Negro, Argentina. Consejo Nacional de Investigaciones Cientı´ficas y Tećnicas (CONICET); E-mail: [email protected] ABSTRACT.—Previous studies have shown both prolonged and plastic cycles in viviparous females of the genus Liolaemus (Iguania: Liolaemidae) from the cold temperate climate of Patagonia. Males have shown interspecific variation in the duration of the breeding season, ranging from continuous to annual. Both cycles are far different from the reproductive cycles previously described for lizards from temperate climates. I examined maximum juvenile size, growth, sexual dimorphism, male and female reproductive cycles, and litter size of viviparous Phymaturus patagonica (Iguania: Liolaemidae), a species restricted to rock promontories in the Patagonian steppe. The reproductive cycle in males is annual with spermatogenesis beginning in December and peaking in early spring of the next year. Spermatozoa are stored in the epididymides for at least two months until mid-January. In contrast, females have a biennial cycle. Thus, prolonged female cycles and large interspecific differences in male cycles characterize viviparous lizards from Patagonia.

Reptiles inhabiting cold climates often show distinctive life-history traits, such as retention of eggs in the oviducts during most of embryogenesis, evolutionary transitions from oviparity to viviparity, adaptive synchronization of parturition with benign environmental conditions (Olsson and Shine, 1999), plasticity in the relative timing of reproductive events, and prolonged reproductive cycles (Ibarguëngoytıá and Cussac, 1996, 1998). In viviparous lizards living in cold temperate zones, female reproductive cycles are usually annual and characterized by low rates of vitellogenesis and embryonic development as a consequence of low temperatures (Pearson, 1954; van Wyk, 1991, 1994; Meńdez de la Cruz et al., 1998). The timing of reproduction in viviparous lizards is physiologically constrained because vitellogenesis and pregnancy in squamates are mutually exclusive phenomena (Callard et al., 1992). Therefore, one would expect that viviparous lizards inhabiting cold climates would tend toward multiannual reproductive cycles with extensive vitellogenesis (van Wyk, 1991; Cree et al., 1992; Cree and Guillette, 1995), prolonged pregnancy (Vial and Stewart, 1985; Cree and Guillette, 1995) and allocation of vitellogenesis and pregnancy in separate breeding seasons (Ibarguëngoytıá and Cussac, 1996, 1998). However, female lizards with extended cycles have been reported in only a few cases, and most examples are from the southern hemisphere: Cordylidae (van Wyk, 1991), Scincidae (Olsson and Shine, 1999), Gekkonidae (Cree and Guillette, 1995), and Liolaemidae (sensu Frost et al.,

2001; Habit and Ortiz, 1996; Ibarguëngoytıá and Cussac, 1996, 1998). Previous studies on reproduction and thermal physiology of the Patagonian lizards Liolaemus elongatus and Liolaemus pictus (Liolaemidae) have shown low frequencies of female reproduction with biennial to triennial (L. pictus) and annual to biennial (L. elongatus) female reproductive cycles (Ibarguëngoytıá and Cussac, 1996, 1998) and have shown interspecific differences in male cycles. Male L. pictus begin to reproduce synchronously, and show a continuous reproductive pattern during the activity season. In contrast, male L. elongatus reproduce during a relatively brief period and a small proportion of males delay spermatogenesis for one year (Ibarguëngoytıá and Cussac, 1999). These studies have shown how severe thermal conditions can constrain the timing and duration of vitellogenesis, pregnancy, and female availability, thereby affecting the male reproductive cycle and the evolution of dimorphic traits (Ibarguëngoytıá and Cussac, 1999, 2002). The genus Phymaturus (Liolaemidae), entirely viviparous and herbivorous, is distributed in the highlands of the Andes, in the volcanic plateaus of Patagonia, from Catamarca to the southern border of Chubut, and on the Chilean side of Andes. Phymaturus patagonicus is restricted to Patagonian steppe and inhabits a very harsh environment with cold and snowy winters where lizards are active from spring to autumn (Cei, 1986). Little is known about the ecology or reproductive biology of Phymaturus (Daciuk 1978; Blackburn, 1982; Shine, 1985; Cei 1986,

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¨ ENGOYTIÁ NORA R. IBARGU

1993; Habit and Ortiz, 1996). The first aim of this study is to provide basic data relevant to the reproductive biology of P. patagonicus, specifically minimum adult size, growth, male and female reproductive cycles as determined by histology and morphology, litter size, and sexual dimorphism. The second aim is to discuss the results in the context of the reproductive traits of viviparous lizards living in cold climates. Such information may contribute to conservation plans for this genus, especially with regard to populations inhabiting the steppe of Patagonia. MATERIALS AND METHODS Fieldwork was conducted in January and February (1987, 1989, and 1991), and from November, to February (2000–2001) in rock promontories in Rıó Negro and Neuqueń provinces, Argentina (40.5–41.58S and 70.5–71.48W). Study animals (N 5 26) were caught by noose and transported to the lab on the day of capture. Four pregnant females were kept in a laboratory terrarium (40 3 20 3 21 cm) until they gave birth (N 5 8 neonates). Voucher specimens were deposited in Centro Regional Universitario Bariloche of the Universidad Nacional del Comahue. The remainder of the sample corresponds to two collections: (1) N 5 19, collected from January to February (1999–2000), in Rıó Negro and Chubut; situated between 41.5–448S and 68.5–708W deposited in the Centro Regional de Investigacioń La Rioja; and (2) N 5 5, collected from January to March (1983), in Chubut, situated at 448S and 698W deposited in the Museo Argentino de Ciencias Naturales Bernardino Rivadavia. Lizards were killed by intraperitoneal administration of sodium thiopental, fixed in Bouin’s solution for 24 h, and preserved in 70% ethanol. Male gonads were removed and dehydrated in an ethanol series and embedded in paraffin. Sections (4–7 lm) were stained with Masson trichromic (Martoja and Martoja Pierson, 1970). Small lizards with umbilical scars (snout–vent length 44–56 mm), were not dissected and their sex was not determined. Follicular size, estimated as the diameter of the largest follicle, and testicular size, estimated as the antero-posterior diameter of left and right testes, were measured with a vernier caliper on camera lucida schemes. Litter size was estimated by counting the number of embryos in the uterus and the number of the neonates born in lab. Seasonal references (spring, summer, autumn and winter) refer to seasons of the Southern Hemisphere. The following data were recorded for each lizard: sex, snout–vent length (SVL), head length, head width and width at vent (tail base). Specific growth rate was calculated as the slope of the regression line between date and SVL using the entire dataset.

A subset of males (N 5 12; 71–98 mm SVL) was studied histologically. The most advanced cell type present at the luminal margin of the seminiferous tubule, following Mayhew and Wright (1970), was used to determine stages of spermatogenesis. The stages correspond to (0) only spermatogonia, (1) spermatocytes, (2) spermatids, (3) spermatogonia and many spermatozoa in the tubule and in the epididymis, and (4) cellular debris characteristic of testicular regression. Presence or absence of spermatozoa in seminiferous tubules or epididymis was also considered. Development of interstitial tissue lying between seminiferous tubules was qualitatively classified as scarce, medium or highly developed. Cell type recognition was based on Pudney (1995). Because examination by light microscopy of left and right testes of two individuals did not show differences in spermatogenesis stages, gonads were considered as equal in subsequent analysis. Seminiferous tubule diameter and germinal epithelium height were measured from different sections of testes (N 5 40 for each individual) using an eyepiece micrometer in a Olympus System Microscope Model BX40. Mean values for each individual were used in statistical analysis. Data were analyzed using regression and correlation analysis, t-tests and analysis of variance (ANOVA), and of covariance (ANCOVA), using SVL as the covariate. Normality and variance homogeneity assumptions were tested with a Kolmogorov-Smirnov test and with Levene’s test, respectively (Sokal and Rohlf, 1969). RESULTS Sexual maturity was determined as the minimum adult size showing reproductive activity. These values were 85 mm in a pregnant female and 87 mm in the smallest spermatogenic male. The frequency distribution of SVL of juveniles was bimodal, with a group of juveniles with umbilical scars from 44–56 mm SVL captured either in the field or born in lab during February and March, and a second group from 70–84 mm SVL captured from December to March (Fig. 1A). SVL did not differ between adult males and females (ANOVA, F1,33 5 1.79, P . 0.10), nor did width at vent (ANCOVA, F1,31 5 0.11, P . 0.7, with SVL as the covariate). Nevertheless, males showed a significant greater head width and head length than females (ANCOVA; head width: F1,31 5 12.93; head length: F1,32 5 9.5, P , 0.005, with SVL as the covariate). The ratio males: females captured was 19:26, but when considering only adults, the ratio males:females was 12:23. Male Reproductive Cycle.—Right and left mean testicular size did not differ in either juvenile or adult males (Paired t-test, t 5 1.57, df 5 28,

PHYMATURUS PATAGONICA REPRODUCTIVE CYCLE

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FIG. 2. Testicular size versus date in the lizard Phymaturus patagonicus. Numbers indicate the spermatogenesis stages.

FIG. 1. (A) Snout–vent length of juvenile Phymaturus patagonicus versus date of capture or birth in lab; (B) regression between SVL and date of adults and juveniles considering the growth in two-year span.

P . 0.13). Consequently, the larger testis was used for the following analysis. The logarithms of testicular size and SVL of adults were positively correlated (Regression, F1,10 5 6.8, P , 0.03) and showed an isometric relationship (the 95% confidence interval for slope, b 5 4.74, lower bound 5 0.63, upper bound 5 8.85). mean testicular size, tubular diameter and epithelium height for each individual were all positively correlated with one another (all r 0.93, P , 0.01, N 5 10). Histological analysis revealed that juvenile males with spermatogenic stage 0 were present from November to February. Spermatogenesis stages 1–2 were present from December to February, showing an increment in testicular size with a peak in February. Testes in spermatogenesis stage 3, with spermatozoa in seminiferous tubules, were present in November and December. The individuals found with testic-

ular regression, cellular debris and degenerating spermatozoa in the seminiferous tubules were present only in December. Individuals with spermatozoa in the epididymis were found in spermatogenesis stage 2 in mid-January; in spermatogenesis stage 3 in November and December and in the individuals with spermatogenesis stage 4 in December (Fig. 2). The amount of interstitial tissue lying between seminiferous tubules was intermediate in juveniles and consisted mostly of fibroblasts whereas the interstitial tissue of adults was composed of Leydig cells. Scarce interstitial space was found from December to February in the spermatogenesis stage 1, spermatogenesis stage 2 and spermatogenesis stage 4. In November and December, a high recruitment of Leydig cells was found corresponding to spermatogenesis stage 3. Female Reproductive Cycle.—Follicular size of vitellogenic females increased significantly with Julian date (Regression, F1,16 5 36.7, P , 0.0001). Adult females showed vitellogenesis from November to the end of February. The largest ovaries were found in the middle of November and the next vitellogenic female showing incipient vitellogenesis was an individual found in November. This indicates that the vitellogenic cycle starts in November and continues throughout summer, winter, and into the following spring until November of next year when ovulation takes place. The time span from the onset of vitellogenesis to the peak in vitellogenic activity in preovulatory females was approximately one year (Fig. 3).

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FIG. 3. Date versus follicular size of adult females in the lizard Phymaturus patagonicus. Frequency distribution of pregnant females (wide bars) and juveniles with umbilical scar (thin bars) are also indicated.

Gravid females (N 5 7) were present from November to the end of February. Females differed in the developmental stage of the embryos (sensu Lemus, 1967; Leyton et al., 1980). Embryos in gravid females captured in November (N 5 2) showed stage 20 of development, characterized by embryos with a curvate trunk, outlines of eyes and years, 1–2 branchial arches and 12 pairs of somites. A female captured at the end of January showed advanced pregnancy characterized by fetuses with skin completely pigmented, with scales. Pregnant females captured at the end of December and in January (N 5 4) gave birth at the end of February and in March. Gravid females showed a fixed brood size of two. DISCUSSION Phymaturus patagonicus gave birth in the second half of February and the beginning of March. The bimodal body size distribution of juveniles suggests that juveniles take two years to reach sexual maturity with a growth rate of 0.06 mm day 1 (Fig. 1B). This is in agreement with observations for L. elongatus and L. pictus that achieve sexual maturity in the second year of life (Ibarguëngoytıá and Cussac, 1996, 1998) with growth rates of 0.05 mm day 1 and 0.04 mm day 1, respectively (unpubl. data). Alternatively, the absence of juveniles between 50 and 70 mm SVL in our samples could be explained if there are differences in the behavior of the individuals in this size range reducing catchability. The only sexual dimorphic trait in P. patagonicus previously documented is the absence of vent pores in females (Cei, 1986). My results reveal

that P. patagonicus is not dimorphic either in snout–vent length or in the width at vent, but like L. pictus and L. elongatus (Ibarguëngoytıá and Cussac, 1996, 1998), P. patagonicus males have larger heads than females. These results suggest an effect of sexual selection on sexual size dimorphism (Mouton and van Wyk, 1993; Censky, 1995). The female-biased sex ratio of captured individuals (0.73) could be a capture bias or the result of differential survivorship. Excluding juveniles, the sex ratio (0.52) was much closer to 1:1. However, because only about one-half of the females were reproductive during the activity season, the operational sex ratio was male-biased and estimated in the range 1.0–1.5. In general, a male-biased operational sex ratio results in intrasexual competition among males, which in turn increases the risk of predation on males (Sugg et al., 1995). Male Reproductive Cycle.—Testicular size and SVL of adult P. patagonicus showed an isometric relationship. In addition, testicular size, tubular diameter, and epithelium height were positively correlated. Nevertheless, testicular size alone may be a weak indicator of spermatogenesis stage and sexual maturity since the size of the testes is also a consequence of changes in the size of the interstitial space that changes composition in relation to reproductive activity. Adults and juveniles may show similar interstitial space volumes, but primarily Leydig cells occupy space in adults, whereas this interstitium in juveniles consists mostly of connective tissue. Male P. patagonicus show an annual reproductive cycle. Spermatogenesis begins in December and continues until February. Individuals with spermatozoa in seminiferous tubules and epididymis were found during late spring. In addition, these individuals were the only ones that showed a high development of Leydig cells, probably associated with a peak of serum testosterone concentration characteristic of spermiogenesis and the mating season (Cree et al., 1992). Nevertheless, spermatozoa also were found in the epididymis in January in individuals with testicular regression and at the beginning of spermatogenesis. Continuous breeding is a common reproductive strategy in tropical lizards, whereas seasonal reproduction is common in temperate lizards (Flemming, 1994). Previous studies on male reproductive cycles in reptiles from Temperate Zone have revealed two major patterns. In the first pattern, termed prenuptial, spermiogenesis occurs just before or during mating in spring or autumn (Pudney, 1995). In the second pattern, postnuptial, spermiogenesis occurs in autumn, spermatozoa are stored in the epididymis or vas deferens over winter, and mating occurs in spring (Cree et al., 1992; Pudney, 1995).

PHYMATURUS PATAGONICA REPRODUCTIVE CYCLE The male reproductive cycle of Phymaturus flagellifer begins with spermatogenesis in November, characterized by the presence of early spermatocytes, and continues until February when spermatozoa are present in tubules and in the epididymis, coincident with the time when copulation occurs (Habit and Ortiz, 1996). In contrast, male P. patagonicus reproduce in synchrony with ovulation in females in spring, and spermatozoa still exist in the epididymis for two months. The timing of the reproductive cycle of P. patagonicus is similar to the male cycle of L. elongatus, but there is no delay in reproduction of small males. Instead P. patagonicus begins to reproduce as soon as sexual maturity is achieved, just as L. pictus does. Female Reproductive Cycle.—The brood size of P. patagonicus is fixed at two offspring, a condition similar to that of other Phymaturus species such as Phymaturus antofagastensis (two offspring; Cei, 1993), the Chilean P. flagellifer (one to two offspring; Habit and Ortiz, 1996) but fewer than P. flagellifer from Argentina (three to five offspring), and Phymaturus somuncurensis and Phymaturus zapallensis (three offspring; Cei, 1986). The two females of P. patagonicus found in November with embryos in development stage 20 suggest ovulation takes place in this month. In addition, pregnant females captured in December and January that gave birth at the end of February and beginning of March indicate a gestation span of approximately four months from middle spring to the end of summer. The fact that recently born juveniles are found in the middle and at the end of summer reinforces these conclusions. Pregnant females collected on the same date show the same developmental state of embryos, suggesting a high synchrony in gestation among females. I observed no evidence that females start vitellogenesis immediately after parturition; instead, they appear to become reproductively quiescent for approximately eight months from autumn until the next activity season. The simultaneous presence of vitellogenic females and pregnant females during spring and summer indicate a biennial reproductive cycle for P. patagonicus females. Two main reproductive patterns have been described in the female reproductive cycles of squamates. One pattern features pregnancy over winter with birth in the spring in species as Sceloporus mucronatus and Sceloporus torquatus (Meńdez de la Cruz et al., 1998) and Liolaemus (Pearson, 1954; Leyton et al., 1982; Ramı´rez-Pinilla, 1991). The second pattern consists of pregnancy occurring during spring and summer with birth in autumn as observed for example in Liolaemus (Leyton and Valencia, 1992) and in the family Cordylidae (van Wyk, 1989; Flemming, 1993, 1994).

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Phymaturus patagonicus, as in L. pictus and L. elongatus, shows a common third pattern, with pregnancy during spring and summer and parturition in autumn with a long vitellogenic period of one year. The prolonged span of vitellogenesis in these species results in prolonged cycles: biennial in P. patagonicus, annual to biennial in L. elongatus and biennial to triennial in L. pictus. The female reproductive cycle of P. patagonicus shows distinct differences from P. flagellifer from Chile (Habit and Ortiz, 1996). Phymaturus flagellifer has a more northern distribution (32–378S) than P. patagonicus, but experiences harsh weather conditions and spends several months inactive each year (Habit and Ortiz, 1996). Females of P. flagellifer exhibit vitellogenesis during either five or 10 months, depending on whether females start vitellogenesis before or after inactivity months, and are pregnant through winter, as in the viviparous females of S. mucronatus and S. torquatus of the Northern Hemisphere (Habit and Ortiz, 1996; Meńdez de la Cruz et al., 1998). Phymaturus patagonicus, like L. elongatus and L. pictus, exhibits vitellogenesis for a period lasting one year, including several moths of inactivity and is pregnant only in the active months throughout spring and summer. The factors acting upon the timing of reproductive events in species may be diverse. Most of the hypotheses put forth to explain the seasonal timing of reproduction in reptiles identify the potential sources of embryonic mortality (James and Shine, 1985), body temperatures during gestation acting upon the fitness of offspring (Beuchat, 1986; Charland, 1995), predation pressure on gravid females and offspring, food availability, factors affecting competition among juveniles (James and Shine, 1985) and thermal environments (Ibarguëngoytıá and Cussac, 2002), among others. Acknowledgments.—I wish to express my gratitude to F. Cruz, V. Cussac, and J. Krenz for the critical review of the manuscript. I thank C. Cańdido and L. Valeo for their kind assistance in fieldwork, and two anonymous reviewers. This work was partially supported by Universidad Nacional del Comahue, Concejo Nacional de Investigaciones Cientı´ficas y Tećnicas, Agencia Nacional de Promocioń Cientı´fica y Tecnolo´gica (PICT 98:04867). LITERATURE CITED BEUCHAT, C. A. 1986. Reproductive influences on the thermoregulatory behavior of a live-bearing lizard. Copeia 1986:971–979. BLACKBURN, D. G. 1982. Evolutionary origins of viviparity in the Reptilia. I. Sauria. AmphibiaReptilia 3:185–205.

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CALLARD, I. P., L. FILETI, L. PE´REZ, L. SORBERA, G. GIANNOUKUS, L. KLOSTERMAN, P. TSANG, AND J. MCCRACKEN. 1992. Role of the corpus luteum and progesterone in the evolution of vertebrate viviparity. American Zoologist 32:264–275. CEI, J. M. 1986. Reptiles del centro, centro-oeste y sur ´ ridas de la Argentina. Herpetofauna de las Zonas A y semia´ridas. Museo Regionale di Scienze Naturali, monografia IV. Torino, Italy. ———. 1993. Reptiles del noroeste, nordeste y este de la Argentina. Herpetofauna de las selvas subtropicales, Puna y Pampas. Museo Regionale di Scienze Naturali, monografie XIV. Torino, Italy. CENSKY, E. J. 1995. Mating strategy and reproductive success in the teiid lizard, Ameiva platei. Behaviour 132:529–557. CHARLAND, M. B. 1995. Thermal consequences of reptilian viviparity: thermoregulation in gravid and nongravid garter snakes (Thamnophis). Journal of Herpetology 29:383–390. CREE, A., AND L. GUILLETTE. 1995. Biennial reproduction with a fourteen-month pregnancy in the Gecko Hoplodactylus maculatus from southern New Zealand. Journal of Herpetology 29:163–173. CREE, A., J. COCKREM, AND L. GUILLETTE. 1992. Reproductive cycles of male and female tuatara (Sphenodon punctatus) on Stephens Island, New Zealand. Journal of Zoology (London) 226: 199–217. DACIUK, J. 1978. Datos bio-ecolo´gicos obtenidos en cautividad del lagarto Phymaturus palluma palluma (Molina, 1872). Anales de Parques Nacionales 14:80–86. FLEMMING, A. F. 1993. Male reproductive cycle of the lizard Pseudocordylus m. melanotus (Sauria: Cordylidae). Journal of Herpetology 27:473–478. ———. 1994. Male and female reproductive cycles of the viviparous lizard, Mabuya capensis (Sauria: Scinidae) from South Africa. Journal of Herpetology 28:334–341. FROST, D. R., R. ETHERIDGE, D. JANIES, AND T. TITUS. 2001. Total evidence, sequence alignment, evolution of Polychrotid lizards, and a reclassification of the Iguania (Squamata: Iguania). American Museum Novitates 3343:1–38. HABIT, E. M., AND J. ORTIZ. 1996. Ciclo reproductivo de Phymaturus flagellifer (Reptilia, Tropiduridae). Boletin de la Sociedad de Biologıá de Concepcioń, Chile 67:7–14. IBARGUËNGOYTIÁ, N. R., AND V. CUSSAC. 1996. Reproductive biology of Liolaemus pictus (Tropiduridae): a biennial viviparous lizard? Herpetological Journal 6:137–143. ———. 1998. Reproduction of the viviparous lizard Liolaemus elongatus in the highlands of Patagonia: plastic cycles in Liolaemus as a response to climate? Herpetological Journal 8:99–105. ———. 1999. Male response to low frequency of female reproduction in viviparous Liolaemus (Tropiduridae). Herpetological Journal 9:111–117. ———. 2002. Body temperatures of two viviparous Liolaemus lizard species, in Patagonian rain forest and steppe. Herpetological Journal 12:131–134. JAMES, C., AND R. SHINE. 1985. The seasonal timing of reproduction: a tropical-temperate comparison in Australian lizards. Oecologia 67:464–474.

LEMUS, D. 1967. Contribucioń al estudio de la embriologıá de reptiles chilenos II. Tabla de desarrollo de la lagartija vivı´para Liolaemus gravenhorsti. Biolo´gica 40:39–61. LEYTON, V. C., AND J. VALENCIA. 1992. Follicular population dynamics, its relation to the clutch and litter size in Chilean Liolaemus lizards. In W. Hamlett (ed.), Reproductive Biology of South American Vertebrates, pp. 177–199. Springer-Verlag. New York. LEYTON, V. C., E. MIRANDA, AND E. BUSTOS-OBREGOŃ. 1980. Gestational chronology in the viviparous lizard Liolaemus gravenhorsti (Gray) with remarks on ovarian and reproductive activity. Archives de Biologie 91:347–361. LEYTON, V. C., A. VELOSO, AND E. BUSTOS OBREGOŃ. 1982. Modalidad reproductiva y actividad cıćlica gonadal en lagartos iguańidos de distintos pisos altitudinales del interior de Arica (Lat. 18–108S). In A. Veloso and E. Bustos-Obregoń (eds.), El hombre y los ecosistemas de montanã 1. La vegetacioń y los vertebrados ectote´rmicos del transecto Arica-Lago Chungara´, pp. 293–301. Proyecto MAB-6 UNEP/ UNESCO 110577-01, Montevideo, Uruguay. MARTOJA, R., AND M. MARTOJA PIERSON. 1970. Tećnicas de histologıá animal. Toray-Masson, Barcelona, Spain. MAYHEW, W. W., AND S. WRIGHT. 1970. Seasonal changes in testicular histology of three species of the lizard genus Uma. Journal of Morphology 130:163–186. MEŃDEZ-DE LA CRUZ, F. R., M. VILLAGRAŃ-SANTA CRUZ, AND R. ANDREWS. 1998. Evolution of viviparity in the lizards genus Sceloporus. Herpetologica 54:521– 532. MOUTON, P. LE F. N., AND J. VAN WYK. 1993. Sexual dimorphism in cordylid lizards: a case study of the Drakensberg crag lizard, Pseudocordylus melanotus. Can. J. Zool. 71:1715–1723. OLSSON, M., AND R. SHINE. 1999. Plasticity in frequency of reproduction in an Alpine lizard, Niveoscincus microlepidotus. Copeia 1999:794–796. PEARSON, O. P. 1954. Habits of the lizard Liolaemus multiformis multiformis at high altitudes in southern Peru´. Copeia 1954:111–116. PUDNEY, J. 1995. Spermatogenesis in nonmammalian vertebrates. Microscopy Research and Technique 32:459–497. RAMI´REZ PINILLA, M. P. 1991. Estudio histolo´gico de los tractos reproductivos y actividad cıćlica anual reproductiva de machos y hembras de dos especies del geńero Liolaemus (Reptilia: Sauria: Iguanidae). Unpubl. Ph.D. diss., Universidad Nacional de Tucumań, Facultad de Ciencias Naturales e Instituto Miguel Lillo, Tucumań, Argentina. SHINE, R. 1985. The evolution of viviparity in reptiles: an ecological analysis. In C. Gans and F. Billet (eds.), Biology of Reptilia. Vol. 15, pp. 605–695. John Wiley and Sons, New York. SOKAL, R. R., AND F. ROHLF. 1969. Biometry. The principles and practice of statistics in biological research. Freeman and Company, New York. SUGG, D. W., L. FITZGERALD, AND H. SNELL. 1995. Growth rate, timing of reproduction, and size dimorphism in the southwestern earless lizard (Cophosaurus texanus scitulus). Southwestern Naturalist 40: 193–202.

PHYMATURUS PATAGONICA REPRODUCTIVE CYCLE vAN WYK, J. H. 1989. The female cycle of the lizard, Cordylus polyzonus poyzonus (Sauria: Cordylidae) in the Orange Free State. South African Journal of Zoology 24:263–269. ———. 1991. Biennial reproduction in the female viviparous lizard Cordylus giganteus. AmphibiaReptilia 12:329–342. ———. 1994. Physiological changes during the female reproductive cycle of the viviparous lizard Cordylus

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giganteus (Sauria: Cordylidae). Herpetologica 50:480–493. VIAL, J. L., AND J. STEWART. 1985. The reproductive cycle of Barisia monticola: a unique variation among viviparous lizards. Herpetologica 41:51–57. Accepted: 14 November 2003.

Journal of Herpetology, Vol. 38, No. 1, pp. 79–87, 2004 Copyright 2004 Society for the Study of Amphibians and Reptiles

A New Character within the Taxonomically Difficult Sphenomorphus Group of Lygosomine Skinks, with a Description of a New Species from New Guinea ALLEN E. GREER1,2

AND

GLENN SHEA3

1

The Australian Museum, 6 College Street, Sydney, New South Wales 2010, Australia; E-mail: [email protected] 3 Faculty of Veterinary Science, University of Sydney, New South Wales 2006, Australia; E-mail: [email protected] ABSTRACT.—The postsupraocular, a small oblique scale just posterior to the supraoculars and medial to the pretemporal scales, is a derived character within the taxonomically difficult Sphenomorphus group of lygosomine skinks. This character occurs in 22 of the approximately 125 described species of Sphenomorphus currently recognized. The species with this distinctive character occur in the southern Philippine Islands, New Guinea, and the Solomon Islands and are called, informally, the Sphenomorphus maindroni group. A new species in the group is described from New Guinea, where most of the species occur. A key to the species with the distinctive character is provided.

The Sphenomorphus group is one of three lineages of lygosomine skinks (Greer, 1979). It includes approximately 478 described species and ranges from southern India and eastern Asia east through the Indonesian Archipelago as far as the Solomon Islands and Australia; it also occurs disjunctly in North and Central America. The recent taxonomic history of the group has seen the description of numerous species and the hiving off of distinct genera from a central core ‘‘genus,’’ originally called Lygosoma but now known as Sphenomorphus. Current research in the group involves the continued teasing apart of other lineages within ‘‘Sphenomorphus’’ leaving an ever-smaller paraphyletic residue. An integral part of this research is the identification of new derived characters that may be, at best, useful in diagnosing natural groups and, at worst, useful in discriminating among species. The purpose of this paper is to describe one such character and to 2

Corresponding Author.

describe a new species in the group of species with the character. MATERIALS AND METHODS Sample sizes are reported either as specimens (for midline strutures or only one side of bilateral structures) or as cases (both sides of bilateral structures). Snout–vent length was measured to the nearest 0.5 mm by applying the ventral surface of the specimen to a steel rule. The presuboculars are those scales between the lower preocular and the supralabial directly below the eye. The postsuboculars are those scales along the anterodorsal edge of the penultimate supralabial. Other head scale characters are labeled in Figure 1. The paravertebrals are counted in one row beginning with the first scale fully posterior to the posterior edge of the hind legs forward to and including the nuchals. The subdigital lamellae of the fourth digit of the pes are counted as all scales

80

A. E. GREER AND G. SHEA

FIG. 1. Sphenomorphus fuscolineatus new species (AM R 127701: holotype). Scale abbreviations are as follows: F 5 frontal; FN 5 frontonasal; FP 5 frontoparietal; IL 5 infralabial; IP 5 interparietal; L 5 loreal; N 5 nasal; NU 5 nuchal; P 5 parietal; PO 5 preocular; POSO 5 postsubocular; PSL 5 postsupralabial; PSO 5 postsupraocular; R 5 rostral; SC 5 supraciliary (only anterior and posterior scales in supraciliary row are labeled); SL 5 supralabial; 18 5 primary temporal; 28 5 secondary temporal, and 38 5 tertiary temporal.

wider than the plantar scales distal to the level of the cleft between the third and fourth digits. The number of species of skinks examined for the new character has not been totalled but would include, on a conservative estimate, probably 95% of all currently recognised species in the family. RESULTS New Character within the Sphenomorphus Group The new character is subtle but consistent within species. It is the presence of a small scale just posterior to the supraoculars scales and just medial to the two pretemporal scales and which from its position can be called the postsupraoc-

ular scale (Fig. 1). Twenty-two described species of Sphenomorphus have this scale: Sphenomorphus anotus Greer, 1973; Sphenomorphus brunneus Greer and Parker, 1974; Sphenomorphus cinereus Greer and Parker, 1974; Sphenomorphus cranei Schmidt, 1932; Sphenomorphus darlingtoni (Loveridge, 1933); Sphenomorphus fasciatus (Gray, 1845); Sphenomorphus forbesi (Boulenger, 1888); Sphenomorphus fragilis (Macleay, 1877); Sphenomorphus fuscolineatus new species; Sphenomorphus leptofasciatus Greer and Parker, 1974; Sphenomorphus longicaudatus (de Rooy, 1915); Sphenomorphus loriae (Boulenger, 1897); Sphenomorphus maindroni (Sauvage, 1878); Sphenomorphus microtympanum Greer, 1973; Sphenomorphus nigriventris (de Rooy, 1915); Sphenomorphus nigrolineatus (Boulenger, 1897); Sphenomorphus oligolepis (Boulenger, 1914); Sphenomorphus papuae (Kinghorn, 1928); Sphenomorphus schultzei (Vogt, 1911); Sphenomorphus scutatus (Peters, 1867); Sphenomorphus solomonis (Boulenger, 1887), and Sphenomorphus undulatus (Peters and Doria, 1878). For the purposes of discussion, we propose to call this group the S. maindroni group after one of the better known and more widely distributed New Guinea species. There is as yet no other derived character concordant with the postsupraocular scale, and it remains to be determined whether the group is monophyletic. Parenthetically we note that the name ‘‘postsupraocular scale’’ was used for the first time in some species descriptions of the genus Tropidophorus (Hikida et al., 2002). This scale was described relative to other scales but not illustrated with a labeled figure. However, it is undoubtedly the scale that has been previously designated as the upper or anterior pretemporal of two pretemporals. Because the concept of pretemporals has been used consistently in skink systematics for nearly 20 years (e.g., Greer, 1983), we have no hesitation in using the new name ‘‘postsupraocular’’ for what is undoubtedly a new scale in skink systematics. The S. maindroni group is distributed within a smaller but contiguous part of the overall range of the Sphenomorphus group. The S. maindroni group occurs in the southern part of the Philippines, the Palaus, New Guinea and the Bismarck Archipelago, and the Solomon Islands (Fig. 2). The center of abundance for the genus is New Guinea where 19 of the 22 described (including S. fuscolineatus n. sp.) species occur. The genus does not occur in Australia. The species in the S. maindroni group are cryptozoic inhabitants of the litter and upper soil layers, usually in moist forest. Their activity in the open, to the extent that it occurs at all, is crepuscular and nocturnal (Greer and Parker, 1974, 1979).

NEW SKINK CHARACTER AND SPECIES

81

FIG. 2. Distribution of the Sphenomorphus maindroni group. Small islands on the edge of the range are labeled.

The mode of reproduction is known for 18 of the 22 species (including the new species) of the S. maindroni group (Table 1). The majority of these species are oviparous, but four, S. cinereus, S. leptofasciatus, S. longicaudatus, and S. nigriventris, are ovoviviparous and one, S. fragilis, is ‘‘intermediate’’ in its reproductive mode in that it lays thinly shelled eggs which hatch almost immediately, that is, development occurs inside the female but the young are born in a ‘‘shell’’ (Greer and Parker, 1979; Guillette, 1992). Brood size is variable in 13 species and possibly a constant two in S. darlingtoni, S. oligolepis, S. scutatus, S. undulates, and the new species and a constant one in S. schultzei (Table 1; Greer 1977). Five of the six species with a variable brood size and for which there is an adequate sample size (N 5 10) show a significant positive intraspecific correlation between female size and brood size (Table 1), but S. nigrolineatus does not (but it is the only one with a sample size as small as 10). There is also a significant positive interspecific correlation between mean female

size and mean brood size (r 5 0.78, P , 0.0003, N 5 17). DESCRIPTION OF A NEW SPECIES OF Sphenomorphus Sphenomorphus fuscolineatus New Species Figures 1, 3, 4 Holotype.—Australian Museum (AM) R127701: Tifalmin, West Sepik Province, Papua New Guinea, 58079S, 1418249E, H. G. Cogger, 9 April 1987. Paratypes.—Australian Museum (AM) R 118819–20: Namasado (750–1000 m), Southern Highland Province, Papua New Guinea, 68159S, 1428479E; R127697–700, 127702–03: same locality data as holotype; R 145922: Tifalmin (1300 m), West Sepik Province, Papua New Guinea, 58079S, 1418249E, H.G. Cogger, 11 April 1986. Bernice P. Bishop Museum (BPBM): 2500, 2507, 3194, 3201, 3219, 3230, 3234: Sibil Valley (1200 m), Star Mountains, Hollandia District (?), West Irian, L. and S. Quate, 15 October to 10 November, 1961; 2511 and 3199: Sibil Valley

82


TABLE 1. Mode of reproduction (o 5 oviparous; ov 5 ovoviviparous), gravid female size and brood size in the species of the Sphenomorphus maindroni group, and the correlation coefficient (r) between female size and clutch within species. Note that Sphenomorphus fragilis lays thinly shelled eggs which hatch in a few hours. Snout–vent length (mm) of females

Brood size

Species

Mode

Range

Mean

SD

Range

Mean

SD

brunneus cinereus cranei darlingtoni fasciatus forbesi fragilis fuscolineatus leptofasciatus longicaudatus maindroni nigriventris nigrolineatus oligolepis papuae schultzei scutatus solomonis undulatus

O OV O O O O OV O OV OV O OV O O O O ? O O

66–87 84–105 57–79 52–64 67–77 34–39 41–51 44–49 67–86 74–88 60–63 55–81 60–70 53 70–80 36–40 40 47–79 54–59

77.7 92.0 64.2 56.0 71.7 37.0 46.0 46.2 72.4 79.6 61.0 71.9 64.6 53.0 73.6 38.0 40.0 61.2 57.0

4.41 8.77 9.09 5.42 4.99 2.65 2.95 1.61 5.22 5.50 2.62 8.18 3.24 — 3.37 — — 6.81 2.65

2–8 3–5 2–5 2 3–5 1–2 2–6 2 1–5 2–4 1–3 2–6 3–5 2 2–5 1 2 1–6 2

5.1 4.0 2.8 2.0 3.7 1.7 2.7 2.0 3.1 2.6 2.0 3.7 3.8 2.0 3.6 1.0 2.0 2.9 2.0

1.19 1.00 1.03 — 0.96 0.58 0.90 — 0.97 0.89 0.53 1.04 0.63 — 1.13 — — 1.07 —

(1250 m), Star Mountains, Djajawidjaja Division, Irian Jaya, Indonesia, 15 October 1961. Museum of Comparative Zoology (MCZ): 152316: Karimui (1150 6 20 m), Chimbu Province, Papua New Guinea; 152403–04: Tifalmin (1300 m), West Sepik Province, Papua New Guinea. Benoit Mys specimen 9298 (see Mys, 1988:143, as Ictiscincus fuscolineatus): Miringi (400–480 m), East Sepik Province, Papua New Guinea. This specimen is deposited in the Institut Royal des Sciences Naturelles de Belgique, Brussels. The name as used by Mys is a nomen nudum. Naturalis-Nationaal Natuurhistorisch Museum (formerly: Rijksmuseum van Natuurlijke Historie (RMNH) 21840–61, 21863– 21874, 21886–21904: Sibil, Ouest-Irian; 21875– 21885: Nimdol (1220 m), Ouest-Irian. University of Papua New Guinea (UPNG) 1033: Efogi, Central Province, Papua New Guinea. Additional Specimen (Not a Paratype).—Papua New Guinea National Museum (PNGNM): field tag number TR 3?. This specimen was collected by an expedition to Crater Mountain Wildlife Management area, Eastern Highlands Province, Papua New Guinea in 1999 (Anonymous, undated). The specimen is now in the PNGNM and bears an only partly legible field tag. The specimen is probably either TR 37 or TR 38 in Anonymous (undated: table on pp. 15–18) but the second digit on the field tag is illegible. The measurements provided for these two specimens conflict with the coloration descriptions and tentative identifications in the table, and there may have been some error in data recording (fide G. Shea, identifier of the

r

0.41* 0.59ns 0.97** — — — 0.66*** — 0.31* 0.04ns 0.71* 0.46*** 0.34ns — 0.19ns — — 0.61*** —

N

36 5 5 4 4 3 28 10 42 5 8 49 10 1 7 3 1 74 3

expedition’s collection). The coordinates for the general Crater Mountain Wildlife Management area are: 68439S, 1458059E. Diagnosis.—This species of Sphenomorphus may be distinguished from all other species in the S. maindroni group (Table 2) in the following combination of characters: longitudinal scale rows at midbody 28–35; only anteriormost pair of chin scales in medial contact; presuboculars modally three; supralabials seven, fifth below center of eye; paravertebrals 59–74; size small to medium (SVL 5 59 mm), and dorsal coloration brown with a dark brown dorsolateral stripe extending from snout to the posterior trunk. Description.—Size small, snout–vent length 24– 59 mm; as proportion of snout–vent length, length of tail 107–158%, length of front limb 20– 24% and length of rear limb 27–35%; tail varies from nearly oval to square in cross-section; limbs pentadactyl, clawed. Snout round in dorsal and lateral profile; rostral with three lobes, dorsal lobe rounded and in broad contact with frontonasal and each lateral lobe vertically truncated and ending directly below center of nostril; supranasals absent; frontonasal wider than long; prefrontals large, usually in contact (81.8%, N 5 44) but occasionally separated (13.6%) or rarely separated by an azygous scale (2.3%) or fused to each other (2.3%); frontal longer than wide; supraoculars four, first two contact frontal; postsupraocular present; frontoparietals distinct; interparietal distinct with small clear parietal

NEW SKINK CHARACTER AND SPECIES

83

FIG. 3. Sphenomorphus fuscolineatus new species, in life, from Namasado, Southern Highlands Province, Papua New Guinea. Photo: S. Donnellan.

eye spot posterior of center; parietals in contact behind interparietal; transversely enlarged nuchals, 0–5 per side, 0–8 (mean 5 4.4, N 5 73) in total; anteriormost nuchal and upper secondary temporal usually separated along edge of parietal by one scale (95.5% of 22 cases) or rarely in contact (4.5%). Nasal entire, shaped like an anteriorly tilted bishop’s miter in outline; nostril located slightly anteroventrally in nasal; loreals two, equal in depth; lower eyelid scaly, lower palpebral scales small; preoculars two, ventral larger than dorsal; supraciliaries 7–9 (mode 5 8, mean 5 8.3), first three and last large, first in contact with frontal and first three in contact with first supraocular and last projecting dorsomedially; presuboculars two to four, mostly three (95.5% of 45 specimens); supraciliaries and upper palpebrals in contact; postsuboculars none to three, usually three (57.1% of 42 cases) or two (40.7%); pretemporals two; supralabials seven, fifth below center of eye and contacting eyelid scales, seventh (last) horizontally divided; postsupralabials two; external ear opening circular to broadly vertically oval and lacking anterior projections; tympanum moderately recessed and pale. Temporal region, although somewhat fragmented, shows a basic pattern of primary temporals two; secondary temporals two, upper

largest and overlapped by lower; tertiary temporals bordering lower secondary temporal two. Mental wider than long; postmental single, in contact with two anteriormost infralabials on each side; three pairs of enlarged chin scales, members of first pair in contact, members of second pair separated by one small scale and members of third pair separated by three small scales; large chin scales abut infralabials, that is, genials do not encroach between enlarged chin scales and infralabials; infralabials 6–7. Scales of body cycloid, smooth, in 28–35 longitudinal rows at midbody; paravertebrals only slightly wider than adjacent scales, 59–74 in a single row; subdigital lamellae of fourth toe of rear foot, 13–20, basal lamellae obliquely lobed, due in part to a postaxial groove; scales on dorsal surface of fourth toe in multiple rows basally declining to two single scales distally; inner preanals overlap outer. Inguinal fat bodies absent. Color in Preservative.—Ground color of dorsum and sides mottled pale and medium brown; venter pale brown; throat often brown spotted; a dark-brown dorsolateral stripe extends from the snout to the base of the tail and is bordered above by a pale stripe, generally sharp-edged

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FIG. 4. Sphenomorphus fuscolineatus new species (RMNH 21897: paratype) from Sibil, West Irian.

and continuous anteriorly but often diffuse or even broken posteriorly; the dark-brown dorsolateral stripe usually edged above with a thin, diffuse pale stripe, especially anteriorly. Tongue color pale over basal one-third, dark grey distally (RMNH 21870, 21845). Parietal peritoneum unpigmented.

The single specimen from Efogi, Central Province, PNG lacks the dark dorsolateral stripe and has the pale and dark markings of the dorsum orientated linearly over the anterior part of the body. This locality is at the extreme eastern end of the known distribution, raising the possibility that the color pattern is subject to geographic variation. Color in Life.—Venter of body and limbs cream (MCZ 152316) to bright yellow (MCZ 152403– 04), of tail pale pink (MCZ 152316) to bright pink (MCZ 152403-04; F. Parker, unpubl.). Osteology.—Premaxillary teeth 9; palatal ramus of pterygoid enters infraorbital vacuity, that is, no ectopterygoid process; postorbital absent; presacral vertebrae 26; sternal/mesosternal ribs 3/2; phalangeal formula of manus and pes, respectively, 2.3.4.5.3/2.3.4.5.4. Sexual Dimorphism.—There was no significant differences between the sexes in the number of supraciliary scales, nuchals (total), paravertebrals or subdigital lamellae (Mann-Whitney test). Details of Holotype.—In those characters which vary, the holotype (AM R127701) has the following variants: prefrontals in contact; transversely enlarged nuchals 1/1; presuboculars 3/3; supraciliaries 8/8; postsuboculars 3/3; primary temporals 2/1; infralabials 6/6; longitudinal scale rows at midbody 30; paravertebrals 66; subdigital lamellae 17/17; sex female.

TABLE 2. Morphometric characters for the species of the Sphenomorphus maindroni group. Superscript ‘‘c’’ indicates cases instead of individuals (see Materials and Methods). Abbreviations: MBSR 5 midbody scale rows; PARAS 5 paravertebrals; SBDL 5 subdigital lamellae, and SVL 5 snout–vent length. SVL

MBSR

PARAS

SBDL

Nuchals (total)

Species

Range

N

Range

Mean

N

Range

Mean

N

Range

Mean

N

Range

Mean

N

anotus brunneus cinereus cranei darlingtoni fasciatus forbesi fragilis fuscolineatus leptofasciatus longicaudatus loriae maindroni microtympanus nigriventris nigrolineatus oligolepis papuae schultzei scutatus solomonis undulatus

25–33 25–87 40–105 36–79 39–64 29–77 34–39 17–54 24–59 63–86 66–94 53–80 33–67 45 31–89 26–75 51–55 40–80 28–47 31–41 22–79 35–66

3 64 16 23 20 57 11 139 60 14 15 5 27 1 86 62 5 40 21 11 191 43

24–26 25–30 37–42 28–43 33–36 30–32 24 22–26 28–35 32–37 26–28 32–34 30–35 26 28–39 26–30 24–28 33–39 20–28 24–26 24–32 24–34

24.7 26.7 38.7 34.9 35.0 30.5 24.0 24.1 29.4 34.6 27.1 33.0 32.8 26.0 30.2 27.7 26.6 35.6 23.9 25.0 27.1 27.0

3 57 13 111 14 12 11 33 83 12 8 5 24 1 50 50 5 29 24 11 157 47

— 60–70 99–118 69–94 71–82 76–88 57–63 63–75 59–74 87–102 64–70 90–98 77–101 72 75–92 61–71 — 84–112 53–58 54–63 60–71 64–93

— 63.9 108.8 79.5 76.9 82.3 59.3 68.4 65.4 94.3 66.7 95.2 88.7 72.0 81.0 65.7 — 95.5 55.5 57.9 65.2 71.8

— 23 11 23 14 14 11 8 81 23 4 5 25 1 40 16 — 32 4 7 22 43

9–10 14–20 19–25 22–31 11–18 21–24 10–13 15–19 13–20 19–23 16–21 14–17 21–28 8–10 14–19 16–21 9–12 20–27 9–15 14–17 12–18 17–23

9.0 17.0 21.5 24.6 15.0 22.5 11.5 16.2 15.5 20.8 17.8 14.7 24.2 9.0 16.2 18.3 20.1 22.8 11.8 15.7 15.4 19.9

6c 58 15 55 17 10 10 26 81 11 13c 8c 11 2c 34 49 9c 29 24 11 156 36

6–8 3–10 0–4 0–16 0–6 6–14 5–8 5–10 0–8 4–12 1–8 0–7 0–10 8 1–5 6–12 5–13 0–13 0–5 4–9 0–11 4–9

7.3 7.1 1.9 5.5 1.2 10.1 6.5 8.1 4.4 6.3 5.9 2.5 5.2 8.0 1.7 8.3 8.2 5.8 1.3 7.5 6.8 6.7

3 42 9 118 14 13 11 20 73 11 8 10 25 1 35 53 5 36 16 8 58 21

NEW SKINK CHARACTER AND SPECIES Etymology.—The species name derives from the Latin for dark (fuscus) and line (linea) and draws attention to the thin dark dorsolateral line on the neck and body, which is unusual in the S. maindroni group. Distribution.—The species is known only from the highlands of central New Guinea between 400–1200 m and from one location on the north coast (Fig. 5). Considering the species’ large overall range, it is odd that it is not known from more localities. Geographic Variation.—The only known specimen from the north side of the ranges (Miringi; northernmost locality on Fig. 5) differs from all other specimens in having more midbody scale rows (35 vs. 28–32) and more subdigital lamellae (20 vs. 13–18). Habits and Habitat.—The three MCZ specimens have associated field notes: MCZ 152316 was ‘‘found in leaf litter in primary forest’’ and MCZ 152403-04 were ‘‘found in leaf litter in forest’’ (F. Parker, unpubl.). Reproduction.—Ten of the available specimens carry yolking follicles or oviducal eggs. These females measure 44–49 mm SVL and carry two eggs each (Table 1). Dates of collection for these females were 9–10 April (N 5 2) and 1 June to 1 August (N 5 8); in both periods some females carry yolking eggs and others shelled oviducal eggs. These data indicate that the species is oviparous and reproductively active at least over the latter part of the rainy season and the first half of the dry season. Comparison with Similar Species.—The dark dorsolateral stripe is a distinctive color feature of S. fuscolineatus and, hence, is a convenient character to quickly eliminate all but a few species in the S. maindroni group from further consideration when trying to identify the new species. Sphenomorphus fuscolineatus shares its dark dorsolateral stripe with Sphenomorphus fragilis and Sphenomorphus nigrolineatus. It differs from these two species in having six infralabials on each side instead of five (and, hence, two infralabials contacting the postmental on each side instead of one); the prefrontals usually in contact instead of separated; presuboculars 3–4 instead of two, and in lacking auricular lobules instead of having low, rounded lobules along the anterior edge of the ear opening. Clarifications and Corrections.—The S. maindroni group as identified here includes part of the S. solomonis group both as it was originally identified (Greer, 1967) and subsequently expanded (Greer and Parker, 1967, 1974; where the name S. fasciatus group was confusingly substituted for the original name S. solomonis group). The S. solomonis group included several species of what are here called the S. maindroni group along with other New Guinea as well as

85

FIG. 5. Map of New Guinea showing distribution of Sphenomorphus fuscolineatus. Dots indicate type specimens, circle indicates additional specimen from the Crater Mountain Wildlife Management area.

Australian taxa (below). However, it now seems likely that the S. solomonis group, which was never diagnosed in terms of an exclusive derived character, is not a monophyletic group and hence has little residual value as a taxonomic concept. Indeed, many of the species originally included in the group have now been transferred to other genera, that is, Eugongylus (Greer and Shea, 2000), Eulamprus (Greer, 1989), Glaphyromorphus (Greer, 1990) and Lipinia (Shea and Greer, 2002). However, most of the S. solomonis group’s New Guinea species are included in what is here called the S. maindroni group. Because this latter group seems more likely to be a monophyletic group than the S. solomonis group, because it can be diagnosed on the basis of at least one unique derived character and it has geographic continuity, we encourage its use instead of the S. solomonis group for purposes of future research. Examination of the relevant types and additional specimens suggests that the species called S. derooyae in the only recent general review of the New Guinea species in this group (Greer and Parker, 1974) is probably Sphenomorphus papuae. Sphenomorphus fragilis has been reported incorrectly as having two infralabials contacting the postmental on each side (Greer and Parker, 1979); in fact, it has only one. KEY TO THE SPECIES OF Sphenomorphus WITH THE POSTSUPRAOCULAR SCALE (Sphenomorphus maindroni GROUP) 1. Prefrontals meet medially . . . . . . . . . . . . . . . . . 2 Prefrontals separated . . . . . . . . . . . . . . . . . . . 16

86


2. Supralabials modally seven or eight, fifth or sixth correspondingly subocular . . . . . . . . . . . . 3 Supralabials modally six, fourth subocular . . . 15 3. Supraciliaries contacting first supraocular, usually three . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 Supraciliaries contacting first supraocular, usually four . . . . . . . . . . . . . . . . . . . . . . . . . . 10 4. Presuboculars three or more . . . . . . . . . . . . . . . 5 Presuboculars two . . . . . . . . . . . . . . . . brunneus 5. Paravertebrals 59–92 . . . . . . . . . . . . . . . . . . . . . 6 Paravertebrals 87–118 . . . . . . . . . . . . . . . . . . . . 9 6. Supralabials seven, fifth subocular . . . . . . . . . . 7 Supralabials eight, sixth subocular . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . longicaudatus 7. Infralabials contacted by postmental, two; oviparous . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 Infralabials contacted by postmental, one; ovoviviparous . . . . . . . . . . . . . . . . . . . nigriventris 8. Enlarged chin scale pairs in contact 1.5–2; dark dorsolateral ‘‘stripe,’’ at most, diffuse and ill-defined; size larger (maximum SVL 5 66 mm) . . . . . . . . . . . . . . . . undulatus Enlarged chin scale pairs in contact, 1; dark dorsolateral stripe thin but distinct; size smaller (maximum SVL 5 48 mm) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . fuscolineatus 9. Dorsally light crossbands only slightly narrower than darker interspaces; ventrally with discrete dark marks . . . . . . . . . . . . cinereus Dorsally light crossbands very thin and much narrower than darker interspaces; ventrally uniformly greyish brown . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . leptofasciatus 10. Upper secondary temporal overlaps lower secondary temporal . . . . . . . . . . . . . . . . . . . . 11 Upper secondary temporal overlapped by lower secondary temporal . . . . . . . . . . . . . . . . 13 11. Midbody scale rows 33–42; paravertebral scales 84–118; New Guinea . . . . . . . . . . . . . . . 12 Midbody scale rows 30–32; paravertebral scales 76–88; Philippine Islands . . . . . . . . fasciatus 12. Ground color generally brownish; pale cross bands generally one scale wide; paravertebral scales noticely wider than more lateral scales; single scale rows on dorsal surface of fourth toe 5 5; maximum snout–vent length 80 mm; oviparous . . . . . . . . . . . . . . . . . . . papuae Ground color generally greyish; pale cross bands generally two scales wide; Paravertebral scales about as wide as more lateral scales; single scale rows on dorsal surface of fourth toe 5 3; maximum snout–vent length 105 mm; ovoviviparous . . . . . . . . . . . . . . cinereus 13. Postorbital bone present; New Guinea . . . . . . 14 Postorbital bone absent; Solomon Islands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . cranei 14. Throat dark mottled, belly clear; usually a dark dorsolateral stripe; single scale rows on dorsal surface of fourth toe 5 3; north

15.

16. 17.

18.

19.

20. 21.

22.

23.

24.

coast of New Guinea, Bismarck Archipelago and Admiralty Islands . . . . . . . . . . . . . maindroni Throat and belly with longitudinal dark streaks; no dark dorsolateral stripe; single scale rows on dorsal surface of fourth toe 5 4; central mountains and north coast (one locality) of New Guinea . . . . . . . . . fuscolineatus Nasal and first supralabial distinct; midbody scale rows 33–36 . . . . . . . . . . . . darlingtoni Nasal and first supralabial fused; midbody scale rows 20–28 . . . . . . . . . . . . . . . . . . . schultzei Supralabials seven, fifth subocular . . . . . . . . . 17 Supralabials six, fourth subocular . . . . . . . . . . 22 A distinct dark upper lateral stripe from head to tail . . . . . . . . . . . . . . . . . . . . . . . . . . . 18 At most a dark aggregation of pigment in upper lateral area of shoulder . . . . . . . . . . . . . 19 Size larger (maximum SVL 75 mm); ectopterygoid process absent (Greer and Parker, 1974:plate 1); oviparous; midbody scales rows 26–30 (mode 28) . . . . . . . . . . . . nigrolineatus Size smaller (maximum SVL 54 mm); ectopterygoid process present Greer and Parker, 1974: plate 1); ovoviviparous; midbody scales rows 22–26 (mode 24) . . . . . . . . . . . fragilis Subdigital lamellae 12–20; size larger (maximum SVL of smallest species 5 79 mm) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20 Subdigital lamellae 9–12; size small (maximum SVL 5 55 mm) . . . . . . . . . . . . . . . oligolepis Ectopterygoid process present . . . . . . . . . . . . . 21 Ectopterygoid process absent . . . . . . . . brunneus Infralabials contacted by postmental on each side usually one; midbody scale rows 24–30 (usually 26–28); paravertebral scale rows 60–71 . . . . . . . . . . . . . . . . . . . . . . solomonis Infralabials contacted by postmental on each side usually two; midbody scale rows 32–34; paravertebral scale rows 90–98 . . . . . loriae External ear opening and tympanum well developed . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23 External ear opening a conical depression; tympanum heavily encroached upon or entirely covered by scales . . . . . . . . . . . . . . . . 24 Infralabials four; subdigital lamellae 14–17; Palau Is . . . . . . . . . . . . . . . . . . . . . . . . . scutatus Infralabials five; subdigital lamellae 10–13; New Guinea . . . . . . . . . . . . . . . . . . . . . . . . forbesi Tympanum small but distinct . . . . microtympanus Tympanum covered by scales . . . . . . . . . . anotus

Acknowledgments.—We thank P. Koshland for the line drawing in Figure 1 and H. Finlay for labeling this figure. LITERATURE CITED ANONYMOUS. Undated. Crater Mountain 1999. Biological Research and Conservation Study in the Crater Mountain Wildlife Management Area, Eastern

NEW SKINK CHARACTER AND SPECIES Highlands Province, Papua New Guinea. A privately produced report. GREER, A. E. 1967. A new generic arrangement for some Australian scincid lizards. Breviora 267:1–19. ———. 1977. On the adaptive significance of the loss of an oviduct in reptiles. Proceedings of the Linnean Society of New South Wales 101:242–249. ———. 1979. A phylogenetic subdivision of Australian skinks. Records of the Australian Museum 32:339– 371. ———. 1983. A new species of Lerista from Groote Eylandt and the Sir Edward Pellew Group in northern Australia. Journal of Herpetology 17:48–53. ———. 1989. The Biology and Evolution of Australian Lizards. Surrey Beatty and Sons, Chipping Norton, New South Wales, Australia. ———. 1990. The Glaphyromorphus isolepis species group (Lacertilia: Scincidae): diagnosis of the taxon and description of a new species from Timor. Journal of Herpetology 24:372–377. GREER, A. E., AND F. PARKER. 1967. A new scincid lizard from the northern Solomon Islands. Breviora 275: 1–20. ———. 1974. The fasciatus species group of Sphenomorphus (Lacertilia: Scincidae): notes on eight previously described species and descriptions of three new species. Papua New Guinea Scientific Society Proceedings 25:31–61. ———. 1979. On the identity of the New Guinea scincid lizard Lygosoma fragile Macleay 1877, with

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notes on its natural history. Journal of Herpetology 13:221–225. GREER, A. E., AND G. SHEA. 2000. A phylogenetically important lygosomine skink resurrected from taxonomic obscurity: Lygosoma unilineatum de Rooij, 1915. Journal of Herpetology 34:85–91. GUILLETTE, L. J. 1992. Morphology of the reproductive tract in a lizard exhibiting incipient viviparity (Sphenomoprhus fragilis) and its implications for the evolution of the reptilian placenta. Journal of Morphology 212:163–173. HIKIDA, T., N. L. ORLOV, J. NABHITABHATA, AND H. OTA. 2002. Three new depressed-bodied water skinks of the genus Tropidophorus (Lacertilia:Scincidae) from Thailand and Vietnam. Current Herpetology 21: 9–23. MYS, B. 1988. The zoogeography of the scincid lizards from North Papua New Guinea (Reptilia: Scincidae). I. The distribution of the species. Bulletin de L’Institut Royal des Sciences Naturelles de Belgique 58:127–183. SHEA, G. M., AND A. E. GREER. 2002. From Sphenomorphus to Lipinia: generic reassignment of two poorlyknown New Guinea skinks. Journal of Herpetology 36:148–156. Accepted: 14 November 2003.