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Reproduction in seven species of Microlophus (Squamata: tropiduridae) from South America.

Abstract.-Information on the reproductive cycles of seven species of Microlophus (M. koepckeorum, M. occipitalis, M. peruvianus, M. stolzmanni, M. theresiae, M. thoracicus and M. tigris) from coastal northern South America gathered from a histological examination of gonadal material is presented. All species exhibited extended reproductive activity present in both austral spring-summer and autumn. Histological evidence is presented that M. peruvianus may produce multiple clutches in the same year. Comparisons are made with the reproductive cycles of other species of Microlophus.

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The genus Microlophus consists of some 20 species and is restricted in distribution to South America and the Galapagos Islands (Peters & Donoso-Barros 1986). Microlophus koepckeorum, M. peruvianus, M. theresiae, M. thoracicus, M. tigris are endemic to Peru (Lehr 2002). Microlophus occipitalis is known from southwestern Ecuador and northern and central Peru, and M. stolzmanni is known from northwestern Peru and possibly southwestern Ecuador (Peters & Donoso Barros 1986). Information on reproduction of M. peruvianus, M. theresiae, M. thoracicus and M. tigris (all as Tropidurus) are in Dixon & Wright (1975) and M. (as Tropidurus) occipitalis is in Watkins (1996). The purpose of this paper is to add information on the reproductive cycles of seven species of Microlophus lizards from coastal northern South America.

MATERIALS AND METHODS

Histological examinations were performed on 313 museum specimens of seven species of Microlophus on deposit with the Natural History Museum of Los Angeles County (LACM), Los Angeles, California (Table 1). Counts were made of oviductal eggs or enlarged follicles (> 4 mm length). The left testis and epididymis were removed from males; the left ovary was removed from females for histological examination. Tissues were embedded in paraffin and cut into sections at 5[micro]m. Slides were stained with Harris' hematoxylin followed by eosin counterstain (Presnell & Schreibman 1997). Testis slides were examined to determine the stage of the male cycle; ovary slides were examined for the presence of yolk deposition. Histological slides of most gonads from 45 juveniles: M. koepckeorum (n = 4), M. occipitalis (n = 6), M. peruvianus (n = 3), M. stolzmanni (n = 13), M. theresiae (n = 6), M. thoracicus (n = 8), M. tigris n = 5) were made to determine the minimum size at which maturity was reached. In cases where the gonads were extremely small, immaturity was assumed and no histology was performed. The relationship between female SVL and clutch size was examined by linear regression analysis and an unpaired t test was used to compare male and female mean body sizes (SVL) (Instat vers. 3.0b, Graphpad Software, San Diego, CA).
Table 1. Sample sizes (n), mean sizes (snout-vent length, mm)
[+ or -] SD and range for males of seven species of Microlophus
from South America. *Indicates mean snout-vent length of males was
significantly larger than that of females (unpaired t-test).

 DF t P n X [+ or -] SD (Range)

M. koepckeorum * 40 6.9 <0.001 21 67.6 [+ or -] 6.8 (52-78)
M. occipitalis * 59 4.9 <0.001 28 62.8 [+ or -] 11.9 (35-79)
M. peruvianus * 40 2.9 <0.001 17 86.8 [+ or -] 18.8 (50-109)
M. stolzmanni * 35 6.1 <0.001 19 88.2 [+ or -] 17.4 (65-120)
M. theresiae * 21 4.7 0.0001 6 68.0 [+ or -] 3.9 (62-72)
M. thoracicus * 40 4.7 <.0001 23 63.2 [+ or -] 7.8 (43-77)
M. tigris - - - 16 61.9 [+ or -] 13.8 (40-80)

 Female

 n X [+ or -] SD (Range)

M. koepckeorum * 21 55.7 [+ or -] 4.1 (50-67)
M. occipitalis * 33 51.5 [+ or -] 5.1 (44-65)
M. peruvianus * 25 73.0 [+ or -] 12.6 (55-93)
M. stolzmanni * 18 62.1 [+ or -] 5.3 (53-73)
M. theresiae * 17 59.8 [+ or -] 3.6 (53-67)
M. thoracicus * 19 53.9 [+ or -] 4.3 (47-64)
M. tigris 5 55.0 [+ or -] 8.5 (45-67)


Specimens examined.--The following specimens of Microlophus were examined from the herpetology collection of the Natural History Museum of Los Angeles County (LACM).

Microlophus koepckeorum (n = 46) PERU: Lambayeque Department (49083, 49084, 49086, 49087, 49089-49098, 49100, 49104, 109569, 122583-122585, 122587-122592, 122594-122606, 122608-122613, 122615); collected 1968, 1970, 1976.

Microlophus occipitalis (n = 67) PERU: La Libertad Department (48853-48861, 48866-48869, 48902-48904, 48906-48908, 122639, 125348, 136012); Lambayeque Department (48870, 48872, 48873, 48897-48901, 122617-122622, 122627-122630, 122632, 122633, 122635-122638); La Libertad Department (136013); Piura Department (48876, 48877, 48891-48895): Tumbes Department (48878-48890); collected 1968, 1976.

Microlophus peruvianus (n = 45) CHILE: Antofagasta Province (122000); ECUADOR: Esmeraldas Province (154385-154387, 154389-154394); PERU: Ancash Department (49021, 49037) Ica Department (49018, 49019, 49040, 49042, 49044-49046); La Libertad Department (136004-136011); Lima Department (9342-9345, 9347, 49023, 49024, 49026, 49028-49030, 49032, 49034, 49036, 49050, 49055-49057); collected 1965, 1966, 1968, 1984.

Microlophus stolzmanni (n= 50) PERU: Cajamarca Department (49107, 49108, 49110-49116, 49119-49123, 49126-49129, 49131, 49132, 122641, 122646, 122649-122651, 122653-122657, 122659, 122660, 122662-122667, 122669, 122670, 122672-122676, 122678-122682); collected 1968, 1976.

Microlophus theresiae (n = 29) PERU: Ica Department (49060-49063, 49075-49077); Lima Department (LACM 49064, 49068-49072, 49074, 49079, 122692-122698, 122700-122706); collected 1968, 1976.

Microlophus thoracicus (n = 50) PERU: Ancash Department (48911, 48914-48918, 48953, 48954, 48956-48963, 48965-48967, 48969-48974, 48976-48979, 122737, 122738, 122742, 122746, 122747); Ica Department (122726-122731, 122733-122736); La Libertad Department (48951); Lambayeque Department (48922, 48924); Lima Department (48980, 48983, 48984); collected 1968, 1976.

Microlophus tigris (n = 26) PERU: Lima Department (48830-48838, 48841,-48847, 48849, 122712-122714, 122716, 122718-122722); collected 1968, 1976.

RESULTS AND DISCUSSION

Microlophus koepckeorum.-The mean SVL of males was significantly larger than that of females (Table 1). All 21 males examined (May = 10, June = 2, August = 1, November = 8) were undergoing spermiogenesis (= sperm formation). In this stage, the seminiferous tubules were lined by spermatozoa or groups of metamorphosing spermatids and the epididymides contained sperm. The smallest reproductively active male (122592) was undergoing spermiogenesis, measured 52 mm SVL and was from May. Monthly stages in the ovarian cycle are in Table 2. Reproductively active females were found in May-June and November. Mean clutch size (n = 13) was 3.2 [+ or -] 0.69 SD, range = 2-5. Linear regression analysis revealed a significant positive correlation between female body size (SVL) in mm and clutch size for 13 M. koepckeorum females (r = 0.82, P = 0.0007). The smallest reproductively active females (both from May) each measured 50 mm SVL (122595, early yolk deposition and 122601, three follicles >4 mm). Dixon & Wright (1975) reported M. koepckeorum mature at 50 mm SVL, and reproductively active females were found in August, November and December with 2-4 yolked ovarian follicles or oviductal eggs.
Table 2. Monthly stages in ovarian cycles of seven species of
Microlophus from Peru.

 Month n No yolk Early yolk Follicles Oviducal
 deposition deposition >4 mm eggs

M. koepckeorum May 12 2 1 5 4
 Jun 5 0 2 1 2
 Nov 4 0 2 1 1

M. occipitalis Jun 9 2 2 4 1
 Aug 1 0 1 0 0
 Nov 7 3 0 3 1
 Dec 16 15 0 1 0

M. peruvianus May 4 1 1 * 0 2
 Jun 2 0 0 2 0
 Aug 1 0 0 1 0
 Oct 1 1 0 0 0
 Nov 10 4 ** 1 0 5
 Dec 7 2 ** 2 2 1

M. stolzmanni Jun 13 0 1 10 2
 Nov 5 0 0 3 2

M. theresiae Jun 11 0 2 9 0
 Dec 6 5 0 0 1

M. thoracicus May 5 1 1 2 1
 Dec 14 2 0 4 8

M. tigris May 1 1 0 0 0
 Dec 4 2 0 1 1

*= one M. peruvianus female from May contained corpora lutea from a
previous clutch and concomitant yolk deposition for a subsequent
clutch; ** = one M. peruvianus female from November and another from
December each contained corpora lutea but were not undergoing yolk
deposition.


Microlophus occipitalis.--The mean SVL of males was significantly larger than that of females (Table 1). All 28 males examined (May = 6, June = 2, November = 7, December = 13) were undergoing spermiogenesis. The smallest reproductively active male (spermiogenesis) measured 35 mm SVL (48853) and was from November. Reproductively active females were found June, August, November and December (Table 2). The smallest reproductively active female (48906, two follicles > 4 mm, measured 44 mm SVL and was from December). Mean value for nine clutches was 4.5 [+ or -] 1.8 SD, range = 2-8. Linear regression analysis revealed a significant positive correlation between female body size (SVL) in mm and clutch size for 9 M. occipitalis females (r = 0.75, P = 0.021). Dixon & Wright (1975) reported oviductal eggs in females from July, August and November, clutches of 2-4 eggs were produced. Males mature between 50-55 mm SVL and females between 45-47 mm SVL (Dixon & Wright 1975). Watkins (1996) studied a population of M. occipitalis at Guayas Province, Ecuador. He reported males (mean SVL = 63.0 [+ or -] 15.7 mm) were larger than females (mean SVL = 55.1 [+ or -] 7.5 mm) and the smallest female with oviductal eggs or enlarged follicles measured 48 mm SVL. Burt (1935) reported that a series of 15 M. occipitalis from Ecuador collected in January exhibited gradation in size from juveniles to adults suggesting an extended breeding season.

Microlophus peruvianus-The mean SVL of males was significantly larger than that of females (Table 1). Sixteen of 17 males examined were undergoing spermiogenesis (May = 5, June = 6, November = 4, December = 1). One November male (SVL = 66 mm) appeared to have completed spermiogenesis. The germinal epithelium was reduced to a few layers in thickness, occasional metamorphosing spermatids but no spermatozoa were present. The smallest reproductively active male (spermiogenesis) measured 63 mm SVL (49021) and was from November. Reproductively active females were present May, June, August and November (Table 2). The smallest reproductively active M. peruvianus female contained two oviductal eggs (49028) measured 56 mm SVL and was from November. Mean clutch size for 13 gravid females was 3.5 [+ or -] 1.3 SD, range = 2-6). Linear regression analysis revealed a significant positive correlation between female body size (SVL) in mm and clutch size for 13 M. peruvianus females (r = 0.60, P = 0.032). Dixon & Wright (1975) reported M. peruvianus females were reproductively active during July-September and November and December. One M. peruvianus female from May (154389) contained corpora lutea from a previous clutch and concomitant vitellogenic follicles for a subsequent clutch indicating M. peruvianus can produce multiple clutches in the same year. One female each from November (49032) and December (49055) contained corpora lutea indicating eggs had recently been deposited. There was no concomitant yolk deposition for a subsequent clutch. Leyton et al. (1981) reported males and females of M. (as Tropidurus) peruvianus were reproductively active throughout the year in northern Chile.

Microlophus stolzmanni.-The mean SVL of males was significantly larger than that of females (Table 1). All 19 males examined were undergoing spermiogenesis (May = 1, June = 8, November = 10). The smallest reproductively active male (spermiogenesis) measured 65 mm SVL (122672) and was from June. Reproductively active females were found in June and November (Table 2). The smallest reproductively active female (49128, measured 53 mm SVL) and was from November. Mean clutch size for 17 females was 2.6 [+ or -] 0.86, range = 1-4. Linear regression analysis revealed a significant positive correlation between female body size (SVL) in mm and clutch size for 13 M. stolzmanni females (r = 0.53, P = 0.029). Dixon & Wright (1975) reported M. stolzmanni females were reproductively active in November, matured between 65-76 mm SVL and produced 3-4 oviductal eggs.

Microlophus theresiae.--The mean SVL of males was significantly larger than that of females (Table 1). All 6 males examined were undergoing spermiogenesis (June = 3, November = 1, December = 2). The smallest reproductively active male (spermiogenesis) measured 62 mm SVL (49072) and was from December. Reproductively active females were found in June and December (Table 2). Mean clutch size for 10 females was 3.4 [+ or -] 0.84, range = 2-5. Linear regression analysis revealed no significant positive correlation between female body size (SVL) in mm and clutch size for 10 M. theresiae females. The smallest reproductively active female (122696, 3 follicles > 4 mm), measured 58 mm SVL and was from June. Dixon & Wright (1975) reported M. theresiae females contained oviductal eggs or enlarged follicles in December.

Microlophus thoracicus.--The mean SVL of males was significantly larger than that of females (Table 1). Seventeen of nineteen males were undergoing spermiogenesis: (May = 3, November = 6, December = 8). One male from May was undergoing late recrudescence (renewal of germinal epithelium for the next period of spermiogenesis). A few metamorphosing spermatids were noted. Another May male was in late spermiogenesis, clusters of metamorphosing spermatids and spermatozoa were present. The germinal epithelium was reduced in cellularity. The smallest reproductively active male (spermiogenesis) measured 43 mm SVL (48983) and was from December. Reproductively active females were found in May and December (Table 2). The smallest reproductively active female (48966, 2 oviductal eggs) measured 46 mm SVL and was from December. Mean clutch size for 15 females was 2.5 [+ or -] 0.83, range = 1-4. Linear regression analysis revealed a significant positive correlation between female body size (SVL) in mm and clutch size for 15 M thoracicus females (r = 0.60, P = 0.018). Dixon & Wright (1975) reported M. thoracicus females were reproductively active in November and December, mature at 45-50 mm SVL and produce 1-5 eggs per clutch with a mean of 3.1 eggs for 40 females.

Microlophus tigris--There was no significant difference between mean males and females in SVL (Table 1). Fourteen of 16 males examined were undergoing spermiogenesis: (May = 8, December = 6). Two males from December were in recrudescence prior to the next period of sperm formation. Germinal epithelium contained sufficient numbers of cells to support spermiogenesis, A few metamorphosing spermatids but, as yet, no spermatozoa were present. The smallest reproductively active male (spermiogenesis) measured 40 mm SVL (122713) and was from May. Reproductively active females were found in December (Table 2). The smallest reproductively active female (48834, 2 follicles > 4 mm) measured 56 mm SVL and was from December. Mean clutch value for two females was 3.0 [+or -]1.4 SD, range = 2-4. There was insufficient data to perform regression analysis to examine the relation between body size and clutchsize. Dixon & Wright (1975) reported M. tigris females were reproductively active in September, November and December and produced clutches of 2-5 eggs.

It appears that other species of Microlophus from Peru and elsewhere have extended reproductive cycles. Goldberg & Rodriguez (1986) reported on reproduction in M. quadrivittatus and M. theresioides (both as Tropidurus) from northern Chile. In both species maximum numbers of males were undergoing spermiogenesis in spring although varying numbers of spermiogenic males were found in most months indicating an extended reproductive cycle. Some males with regressed testes were found in summer; female reproductive activity (enlarged follicles or oviductal eggs) was limited to spring (Goldberg & Rodriguez 1986). This contrasts with six of the seven species of Microlophus presented herein which were reproductively active in both austral winter and spring (spring female data was limited to only one specimen of M. tigris). Furthermore, Vitt & Goldberg (1983) similarly reported some males of Microlophus (as Tropidurus) torquatus from northeastern Brazil were undergoing spermiogenesis and females were reproductively active in all months. Subsequent examination of the reproductive biology of other Microlophus species are needed before the diversity of reproduction exhibited by these lizards can be ascertained.

ACKNOWLEDGMENTS

I thank Christine Thacker for permission to examine Microlophus sp.

LITERATURE CITED

Burt, C. E. 1935. Notes on a collection of lizards from western Mexico and tropical America. Trans. Amer. Micros. Soc., 54:167-178.

Dixon, J. R. & J. W. Wright. 1975. A review of the lizards of the iguanid genus Tropidurus in Peru. Nat. Hist. Mus. Los Angeles Co, Contrib. Sci., 271:1-39 pp.

Goldberg, S. R. & E. Rodriguez. 1986. Reproductive cycles of two iguanid lizards from northern Chile, Tropidurus quadrivittatus and Tropidurus theresioides. J. Arid Environ., 10:147-151.

Lehr, E. 2002. Amphibian und Reptilien in Peru. Natur und Tier, Munster. 206 pp.

Leyton, V., A. Veloso & E. Bustos. 1981. Modalidad reproductiva y actividad ciclica gonadal en lagartos iguanidos de distinctos pisos altitudinales del interior de Arica (Lat. 18[degrees]10'S). Pp. 293-316 in Vol. I La vegetacion y los vertebrados inferiores de los pisos altitudinales entre Arica y el Lago Chungara (A. Veloso & E. Bustos, eds.). Proyecto MAB-6, UNEP-UNESCO-1105-77-01.

Peters, J. A. & R. Donoso-Barros. 1986. Catalogue of the Neotropical Squamata:Part II Lizards and Amphisbaenians. Smithsonian Institution Press, Washington, D.C. 293 pp.

Presnell, J. K. & M. P. Schreibman. 1997. Humason's Animal Tisssue Techniques, 5th Ed. The Johns Hopkins University Press, Baltimore, 572 pp.

Vitt, L. J. & S.R. Goldberg. 1983. Reproductive ecology of two tropical iquanid lizards: Tropidurus torquatus and Platynotus semitaeniatus. Copeia, 1983:131-141.

Watkins, G. G. 1996. Proximate causes of sexual size dimorphism in the iguanian lizard Microlophus occipitalis. Ecology, 77:1473-1482.

SRG at; sgoldberg@whittier.edu

Stephen R. Goldberg

Department of Biology, Whittier College

Whittier, California 90608
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Date:Nov 1, 2008
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