Short Communications

SALAMANDRA 44 1 54-58 Rheinbach, 20 February 2008 ISSN 0036-3375

Notes on reproduction in fi ve species of Emoia (Squamata: Scincidae) from Papua New Guinea

Stephen R. Goldberg & Fred Kraus

Abstract. Males of Emoia caeruleocauda, E. jakati, E. longicauda, E. obscura and E. pallidiceps from Pa- pua New Guinea exhibit extended periods of sperm formation. Emoia caeruleocauda, E. longicauda, E. obscura produced clutches of 2 eggs; E. jakati and E. pallidiceps produced clutches of -2 eggs. One E. ob- scura female contained corpora lutea from a previous clutch and concomitant yolk deposition, and two contained oviductal eggs and concomitant yolk deposition for subsequent clutches, indicating the pro- duction of multiple clutches under natural conditions. Estimates of minimum sizes for sexual maturity are given for each Emoia species. Key words. Scincidae, Emoia caeruleocauda, Emoia jakati, Emoia longicauda, Emoia obscura, Emoia pal- lidiceps, reproduction, Papua New Guinea.

Th e skink genus Emoia consists of 72 spe- these species except for E. longicauda, which cies ranging from southeastern Asia to the has not been studied, produce clutches of two islands in the Central Pacifi c (Brown 99). eggs (Brown 99, McCoy 2006). Th e pur- Th e greatest diversity ofEmoia species occurs pose of this report is to present the fi rst his- on New Guinea and adjacent islands (Brown tological information on reproductive cycles 99). Ecological data are available for rela- for each of these species based on an exami- tively few of these species, probably refl ecting nation of gonadal material of specimens from the remoteness of most species from centers Papua New Guinea. Estimates of minimum of herpetological research activity. Nonethe- sizes at maturity are given for each species. less, most species investigated to date lay two Th e fi rst information on the reproductive bi- eggs and hatchling sizes have been reported ology of E. longicauda is presented. for several species (Greer 968, Brown 99, Emoia skinks from Milne Bay Province, Morrison 2003). Papua New Guinea were examined from Emoia caeruleocauda is known from Bor- the herpetology collection of the Bernice P. neo, Palau, Mariana Islands, Caroline Islands, Bishop Museum (BPBM), Honolulu, Hawaii. Marshall Islands, southern Philippines, Su- Skinks were collected from 2002 to 2004 as lawesi, Moluccas, New Guinea and associ- part of biodiversity surveys and were stud- ated island archipelagos, Solomon Islands, ied from a geographically constrained region Vanuatu and Fiji; Emoia jakati is known (Milne Bay Province) so as to minimize the from Palau, Caroline Islands, Marshall Is- potential for confounding geographic varia- lands, New Guinea and adjacent island archi- tion in the reproductive cycles (Appendix). pelagos, and Solomon Islands (Brown 99, Survey schedules disallowed comprehensive McCoy 2006). Emoia longicauda is known sampling throughout the year but were suf- from New Guinea, Cape York Peninsula in fi ciently spaced in time to allow some infer- Queensland, Australia, Admirality Islands ence of yearly reproductive patterns. Th e left and Mussau Island, north of New Ireland; testis and ovary were removed, processed by Emoia obscura and Emoia pallidiceps are re- standard histological techniques and stained stricted to New Guinea (Brown 99). All with Harris’ hematoxylin followed by eosin

© 2008 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT) http://www.salamandra-journal.com Short Communications counterstain (Presnell & Schreibman 2. SD, 0.56 SE, range = 4-48 mm; 25 males 997). Histology slides were deposited at with mean SVL = 4.6 mm ± 3.5 SD, 0.70 SE, BPBM. Maturity of males was recognized by range = 33-47 mm; 4 neonates with mean SVL their having spermiogenesis in progress, of = 26.0 mm ± 2.6 SD, .3 SE, range = 23-29 mm. females by their undergoing yolk deposition. All males were undergoing spermiogenesis: Clutch size of females was determined from January (5 males), August (4), September enlarging follicles or oviductal eggs. Lizard (6). Th e smallest reproductively active male snout-vent length (SVL) was measured using measured 33 mm SVL (BPBM 5934) and was a plastic millimeter rule to the nearest mil- taken September 2002. Reproductively ac- limeter. tive females were present in the three months Two stages were observed in the testicu- sampled (January, August and September) lar cycle: () recrudescence, in which there (Table ). Mean clutch size for 2 females was is a proliferation of cells in the germinal epi- .8 ± 0.39 SD, 0. SE, range: -2. Th e smallest thelium for the next period of spermiogen- reproductively active females with oviductal esis (sperm formation). Primary and second- eggs (BPBM 5935) and enlarged ovarian fol- ary spermatocytes are the predominant cells; licles (> 6 mm) (BPBM 5955) both measured some spermatids but no spermatozoa may be 4 mm SVL and were from September 2002. present; (2) spermiogenesis, in which sem- One neonate was from April (BPBM 9988), iniferous tubules are lined by spermatozoa one from August (BPBM 5922), two from and clusters of metamorphosing spermatids September (BPBM 5937, 5950). are present. Emoia longicauda: Th e sample (n = 24) Emoia caeruleocauda: Th e sample (n = 24) consisted of 4 females with mean SVL = 8. consisted of 4 females with mean SVL = 46.3 mm ± 5. SD, .3 SE, range = 69-87 mm; 9 mm ± 2. SD, 0.57 SE, range = 43-49 mm; 7 males with mean SVL = 86.4 mm ± 8.8 SD, 2.9 males with mean SVL = 49.0 mm ± 3.5 SD, .3 SE, range = 68-00 mm;  neonate with SVL = SE, range = 44-54 mm; 3 neonates with mean 38 mm. All males were undergoing spermio- SVL = 24.0 mm ± 2.7 SD, .5 SE, range = 22- genesis: January (6 males), April () and May 27 mm. All males were undergoing spermio- (2). Th e smallest reproductively active male genesis except for one male obtained in Janu- measured 68 mm SVL (BPBM 680) and ary that was in late recrudescence. It meas- was taken January 2003. Reproductively ac- ured 44 mm SVL (BPBM 6730) and con- tive females were present in three of the four tained metamorphosing spermatids but no months sampled: January, February, and May sperm. Males undergoing spermiogenesis (Table ). Th e one April female was reproduc- were from: January (3 males); April (); Sep- tively inactive. Mean clutch size for 6 females tember (2). Th e smallest reproductively ac- was 2.0, 0.0 SD, 0.0. SE. Th e smallest repro- tive male (spermiogenesis in progress) meas- ductively active female measured 77 mm SVL ured 45 mm SVL (BPBM 9985) and was tak- (BPBM 6792) and was from January 2003. en April 2004. Reproductively active females Two females, 69 mm SVL (BPBM 6797) and were present in the three months sampled 72 mm SVL (BPBM 6804) were not repro- (January, April and September) (Table ). ductively active. One neonate (BPBM 20742) Mean clutch size for  females was 2.0, 0.0 was from April. SD, 0.0. SE. Th e smallest reproductively ac- Emoia obscura: Th e sample (n = 57) con- tive females measured 43 mm SVL (BPBM sisted of 24 females with mean SVL = 5.6 998) from April 2004 and (BPBM 6722) mm ± 5.0 SD, .0 SE, range = 39-60 mm; 29 from January 2003. One neonate (BPBM males with mean SVL = 49.7 mm ± 6.6 SD, .2 6728) was from January, two (BPBM 9982, SE, range = 34-60 mm; 4 neonates with mean 9983) were from April. SVL = 27 mm ± .8 SD, 0.9 SE, range = 25-29 Emoia jakati: Th e sample (n = 43) consist- mm. All males were undergoing spermiogen- ed of 4 females with mean SVL = 44.3 mm ± esis: April (8 males), May (8) and September

55 Short Communications

Tab. 1. Stages in ovarian cycle of fi ve species of Emoia skinks from Papua New Guinea. *Two E. obscura females with oviductal eggs also contained follicles undergoing yolk deposition. **Represents one E. obscura from September (not in the table) with corpora lutea from a previous clutch and yolk deposi- tion for a subsequent clutch.

Number of speci- Quiescent Early yolk depo- Enlarged follicles Oviductal eggs mens sition > 3 mm Emoia caeruleocauda 4 January 9  0 7  April 3 0 2  0 September 2  0 0  Emoia jakati 4 January 4 0   2 August  0 0  0 September 9   4 3 Emoia longicauda 4 January 5 2 0  2 February  0 0  0 April   0 0 0 May 7 2 3 2 0 Emoia obscura 24 February  0 0  0 April 0 0  5 4* May 7 2 2 2  September** 5 0 0 2 2 October  0 0 0  Emoia pallidiceps 22 January 6 0 2 3  February 9 0  5 3 April  0 0  0 August  0 0  0 September 2 0 0   October 3 0  2 0

(3). Th e smallest reproductively active male Mean clutch size for 8 females was 2.0, 0.0. measured 34 mm SVL (BPBM 555) and was SD, 0.0 SE. Th e smallest reproductively ac- taken 22 April 2002. Reproductively active tive female measured 39 mm (BPBM 5974) females were present in the fi ve months sam- and was from September 2002. One neonate pled: February, April, May, September, and (BPBM 5526) was from April, one from May October (Table ). One female from Septem- (556), one from August (BPBM 5562) and ber (BPBM 5974) contained corpora lutea one from September (BPBM 5976). from a previous clutch and yolk deposition Emoia pallidiceps: Th e sample (n = 35) for a subsequent clutch, and two females consisted of 22 females with mean SVL = 5.3 from April (BPBM 5524, 5529) with oviduc- mm ± 5.0 SD, . SE, range = 43-60 mm; 2 tal eggs were also undergoing yolk deposition males with mean SVL = 49.0 mm ± 4.4 SD, for a subsequent clutch, indicating E. obscura .3 SE, range = 4-55 mm;  neonate with SVL may produce multiple clutches the same year. = 25 mm. All males were undergoing sper-

56 Short Communications miogenesis: January (0 males); February () clutch also occurs (Zug 99). and August (). Th e smallest reproductively Th e number of clutches produced byEmoia active male measured 4 mm SVL (BPBM in a year is not known. However, the tropical 78) and was from January 2003. Repro- climate that they inhabit permits year-round ductively active females were present in the activity, which will enhance the possibility six months sampled: January (6), February of multiple clutch production. In captivity, (0), April (), August (), September (2), and E. caeruleocauda females produced clutches October (3) (Table ). Mean clutch size for 7 approximately every thirty days (McCoid et females was .9 ± 0.24 SD, 0.06 SE, range = al. 997). Our fi nding of both corpora lutea -2. Th e smallest reproductively active female and early yolk deposition in one female, as measured 43 mm SVL (BPBM 5983) and was well as two females with oviductal eggs and from September 2002. One neonate (BPBM yolk deposition for subsequent clutches in 793) was from January. wild E. obscura, indicate production of mul- Previous studies on reproduction in Emoia tiple clutches in wild populations during the have indicated long periods of reproductive same year. activity with reproduction possible through- We do not know of prior histological stud- out the year (Baker 947, Alcala & Brown ies of the testicular cycles of Emoia lizards, 967, Schwaner 980). Baker (947) report- however, Zug et al. (982) reported year- ed that in Vanuatu, where Emoia cyanura round spermatogenesis in the skink Carlia exhibited year-round reproductive activity, bicarinata at Port Moresby, Papua New Guin- there was a peak in November and Decem- ea with peaks during March to April and Au- ber. Our samples confi rm extended repro- gust to October. Wilhoft (963) reported duction for both males and females but were Carlia (as Leiolopisma) rhomboidalis under- too small to identify a peak period of activity, went spermiogenesis throughout the year in if one exists for these species. Neonates for tropical Australia. Our histological results several species (E. caeruleocauda, E. jakati, for Emoia in Milne Bay Province, Papua New E. obscura) were found throughout a span of Guinea confi rm extended periods of sper- 4-6 months too, consistent with extended re- miogenesis for E. caeruleocauda, E. jakati, E. production. longicauda E. obscura and E. pallidiceps. Th e relationship between lizard size and Subsequent investigations on diff erent clutch size is not clear. Schwaner (980), who species of Emoia will be needed to ascertain a studied Emoia with larger body sizes from more complete picture of variability in the re- American Samoa reported E. nigra females productive cycles (clutch sizes and duration to reach maturity at 86 mm SVL and produce of spermiogenesis) exhibited by members clutches of 2-4 eggs and E. samoense to reach of this genus; however, this study goes some maturity at 84 mm and produce clutches of way toward indicating protracted breeding of 4-7 eggs. In contrast, E. lawesii matured at 78 these lizards in New Guinea. mm SVL and had a mean clutch size of only .8, and E. adspersa matured at 64 mm SVL and had a mean clutch size of only .9. Acknowledgements Data presented herein indicate clutches of two eggs are uniformly produced by E. caer- We thank P. Banige, I. Bigilale, F. Francisco, uleocauda, E. longicauda, and E. obscura, P. Lagalaga, F. Malesa, D. Salepuna, M. Sam- son, J. Tekwae, B. Uruwa, J. Volo, Allen, Dage, whereas E. jakati and E. pallidiceps produced Don, Genta Sr., Genta Jr., Gule, James, Lawa- either  or 2 eggs. Clutches of two eggs ap- si, Munda, Pipi, Suki, and Tannu for field as- pear to be the case for most species of Emoia sistance; and S. Andrew, Aussiya, H. Korage, (Greer 968, Brown 99, McCoy 2006) al- D. Libai, B. Libasi, D. Mitchell, P. Robert, B. though occasional production of one egg per Salepina, B. Yawai, and Conservation Interna-

57 Short Communications tional for logistical fi eld assistance. We thank the Wilhoft,ilhoft, D.C.D.C. (963):(963): Gonadal histology and many landowners who kindly granted us permis- seasonal changes in the tropical Australian li- sion to survey on their lands; the PNG National zard, Leiolopisma rhomboidalis. – J. Morphol., Museum and Art Gallery for providing in-coun- 3: 85-204. try collaborative assistance; and the Department Zug, G.R. (99): Th e lizards of Fiji: natural histo- of Environment and Conservation, National Re- ry and systematics. – Bishop Mus. Bull. Zool., search Institute, and Milne Bay Provincial Gov- 2: -36. ernment for permission to conduct this research. Th is research was supported by NSF grant DEB- Zug, G.R., M.M. Barber & J.C. Dudley (982): 003794. Th is is contribution 07-8 from the Pa- Gonadal histology and reproduction in Carlia cifi c Biological Survey at the Bishop Museum. bicarinata (Scincidae, Sauria, Reptilia) of the Port Moresby Area, Papua New Guinea. – Her- petologica, 38: 48-425. References

Alcala, A.C. & W.C. Brown (967): Population Appendix ecology of the tropical scincoid lizard, Emoia atrocostata, in the Philippines. – Copeia, 967: Emoia caeruleocauda (n = 24) – Papua New Guin- 596-604. ea: Milne Bay Province; Fergusson Island (BPBMBPBM Baker, J.R. (947): Th e seasons in a tropical rain- 595-598), Misima Island (BPBM 678-28, forest. Part 6. Lizards (Emoia). – J. Linn. Soc., 6730-3, 6733), Sudest Island (BPBM 998-83, 6: 243-247. 9985-87). Emoia jakati (n = 43) – Papua New Guinea: Brown, W.C. (99): Lizards of the genus Emoia Milne Bay Province; Fergusson Island (BPBM (Scincidae) with observations on their evoluti- 592-30, 5932, 5934-4, 5944, 5946, 5948, on and biogeography. – Mem. Cal. Acad. Sci., 5950-5952, 5954-55), Normanby Island (BPBM 5: -94. 5959, 596-62, 6868-73, 6875-77), Misima Is- Greer, A.E. (968): Clutch size in the scincid ge- land (BPBM 6868-73, 9988). nus Emoia. – Copeia, 968: 47-48. Emoia longicauda (n = 24) – Papua New Guin- McCoid, M.J., S.E., Henke, R.A., Hensley & C. ea, Milne Bay Province; Misima Island (BPBM Clark (997): Natural history notes: Emoia ca- 6789, 679-93, 6795-97, 6799-02, 6805, 7392, eruleocauda (Pacifi c Blue-tailed Skink): captive 20742, 20744-20745), Halowia (BPBM 6804), Du- reproduction. – Herpetol. Rev., 28: 202. abo (BPBM 7392), Rossel Island (BPBM 20746-5, 20753-54). McCoy, M. (2006): Reptiles of the Solomon Is- Emoia obscura (n = 57) – Papua New Guinea: lands. – Sofi a, Bulgaria, (Pensoft Publishers), Milne Bay Province: Cloudy Mts. (BPBM 552-26, 47 pp. 5528-34, 5537-52), Mt. Pekopekowana (BPBM) Morrison, C. (2003): A Field Guide to the Her- 5553-54, 556-62, 5564-65, 5569, 557-77, Fer- petofauna of Fiji. – (Oceania Printers), Suva, gusson Island (BPBM 5963-68, 5970-7), Da- Fiji, 2 pp. due (BPBM 5972-74), Normanby Island (BPBM Presnell, J.K., & M.P. Schreibman (997): 5976), Duabo (BPBM 5979), Halowia (BPBM Humason’s Animal Tissue Techniques, 5th Ed. – 778). (Th e Johns Hopkins Press), Baltimore, 572 pp. Emoia pallidiceps (n = 35) – Papua New Guinea: Schwaner, T.D. (980): Reproductive biology of Milne Bay Province: Cloudy Mts. (BPBM 5580), lizards on the American Samoan islands. – Oc- Fergusson Island (BPBM 598), Normanby Island cas. Pap. Mus. Nat. Hist., Univ. Kansas, 86: - (BPBM 5982-84, 5987, 779-8, 783-89, 79- 53. 96, 798-200), Mt. Simpson (BPBM 720-07, 7209-0, 725).

Manuscript received: 21 March 2007 Authors’ addresses: Stephen R. Goldberg, Whittier College, Department of Biology, Whittier, Califor- nia 90608, USA, E-Mail: [email protected]; Fred Kraus, Bishop Museum, Department of Natural Science, 1525 Bernice Street, Honolulu HI 96817, USA, E-Mail: fk [email protected].

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