Ecology and Reproductive Cycles of the Introduced Gecko, Hemidactylus Turcicus, in the Southern United States

Ecology and Reproductive Cycles of the Introduced Gecko, Hemidactylus turcicus, in the Southern United States

FRANCIS L. ROSE and CLYDE D. BARBOUR

Reprinted from THE AMERICAN MIDLAND NATURALIST Vol. 79, No. 1, pp. 159-168, January, 1968 , University of Notre Dame Press Notre Dame, Indiana i Ecology and Reproductive Cycles of the Introduced Gecko, Hemidactylus turcicus, in the Southern United States

FRANCIS L. ROSE

and

CLYDE D. BARBOUR

Reprinted from THE AMERICAN MIDLAND NATURALIST Vol. 79, No. 1, pp. 159-168, January, 1968 University of Notre Dame Press Notre Dame, Indiana Ecology and Reproductive Cycles of the Introduced Gecko, Hemidactylus turcicus, in the Southern United States

FRANCIS L. ROSE and CLYDE D. BARBOUR Department of Biology, Texas Technological College, Lubbock 79409, and Department of Zoology and Entomology, University of Utah, Salt Lake City 84112

ABSTRACT: The Mediterranean gecko, Hemidactylus turcicus, is firmly established in the southern United States. Animals were active immediately after nightfall and there was a decrease in numbers of active individuals after midnight. Eighty-two percent of the geckos recaptured one time were within 6 m of the initial capture site. There was no correlation between distance moved by a gecko and time of recapture after marking. Juveniles regenerated their tails faster than males and males faster than females. The relative tail length (tail length/snout-vent length) increased ontogenetically. The sex ratio of adults was almost exactly 1:1. The reproductive season extended from April to August and females matured in the winter or spring of their second year. About two months were required to produce one clutch of two eggs; each female produced from two to three clutches per season. Eggs were laid in a cleared space and covered with debris. The average incubation period was 40 (37-45) days. Hatchlings had an average snout-vent length of 25.9 (25.0-27.7) mm and resisted starvation and dehydration for 30 to 33 days. In August, the testes were regressed but in December numerous primary spermatocytes were present and spermiogenesis was in progress. In January, one specimen contained a few sperm in the epididymides and the lumina within the testes were well developed. In July, spermatogenic activity was reduced but sperm remained packed in the epididymides. Light period may be the predominant environmental factor controlling reproduction in Hemidactylus turcicus in southern Louisiana. INTRODUCTION The family Gekkonidae is distributed throughout the tropics and in some warm temperate regions. It is predominantly an Old World family with numerous species in Africa and Asia but is well repre- sented on most continents. Individuals are usually nocturnal or crepuscular, have vertical pupils, large eyes, expanded digital tips, and lack movable eyelids. Many of the species are vocal, some freely but others only under stress. Two genera and two species are native to the United States: Phyllodactylus tuberculosus in extreme south central California, Cole- onyx variegatus brevis in southwestern New Mexico and southwestern Texas, and C. v. variegatus in southwestern Utah, extreme southern Nevada, southern and western Arizona, and southern California. Three genera and four species have been introduced into the United States: Sphaerodactylus cinereus, S. not atus, Gonatodes fuscus, and Hemidactylus turcicus. The last named species was reported from Key West (Stejneger, 1922), Miami (Barbour, 1936), and Gainesville, Florida (King, 1958) ; New Orleans, Louisiana (Ether- idge, 1952), and Brownsville, Texas (Conant, 1958) . 159 160 THE AMERICAN MIDLAND NATURALIST 79(1)

In New Orleans Hemidactylus turcicus is found commonly on old buildings, rock walls, and burial vaults. It apparently reaches its greatest densities in the above-ground cemeteries found throughout the city. Several individuals were collected from buildings on the Tulane University campus, but the gecko was thought to have a low density there. On 30 September 1964, seven geckos were observed scurrying around storm drains on two large granite buildings and several others were seen moving about on window ledges and screens. Our initial interest in these lizards was to determine their general area of movements and until we began marking them we did not realize how large the population was. An effort was made to learn as much about this introduced gecko as time allowed. The following report is based on a study which extended from October, 1964 to June, 1966. HABITAT AND ACTIVITY This study was conducted on two large five-story granite block buildings on the Tulane University campus. At night the geckos were concentrated primarily behind vertical storm drains and around windows. The drains extended from the ground to the roof and were used as cover for vertical movements. During the day the lizards retreated into small crevices and cracks between granite blocks and in rotten and cracked wooden window frames. King (1958) reported an activity peak for Hemidactylus in Gaines- ville, Florida at 8 to 9 PM with a gradual decline to 6 AM. Our data showed a less distinct peak but this may have been due to the small sample sizes. For example, at 9 PM King counted 59 animals but the greatest number we saw per hour was 21. In general, the geckos began moving about immediately after complete darkness, and after midnight there was a gradual decline in the number observed. Geckos were seen every month and one animal was seen moving about on a building when the air temperature was 42 F.

RECAPTURE AND MOVEMENTS Of the 265 animals marked, 106 (40%) were recaptured one time (Table 1). The greatest number of recaptures for a single animal was six.

TABLE 1.—Summary of capture and movement data for Hemidactylus turcicus IN,4?.an distance between Times Number of Percent captures captured individuals recaptured (meters) 1 106 40.0 5.4 2 49 18.5 3.8 3 21 10.5 5.4 4 12 4.5 5.6 5 5 1.8 2.1 6 2 0.7 0.3 1968 ROSE ET AL.: ECOLOGY OF HEMIDACTYLUS 161

After recapture the shortest distance between the place of capture and the preceding capture site was noted. Admittedly, this gave no estimate of the home range size since we were unable to consider vertical movements greater than 2.5 m; however, the data indicated that the animals remained in a rather limited horizontal area. The mean distance between the initial capture site and the point of the first recapture was 5.4 ± 9.7 (0 - 69.8) m. Of the animals recaptured one time, 82% were recaptured within 6 m of the initial capture site. There was no correlation between distance moved and time elapsed since marking (Table 1). Only once was an animal seen on the ground but two mature males changed buildings during the study. To accomplish this they had to traverse an open space of about 9.7 m. Such radical movements are to be expected if a species is to invade new areas.

FOOD AND FEEDING HABITS Vision plays a predominant role during feeding by H. turcicus. Moving meal worms were readily eaten in the laboratory and dead ones were rejected. In May (Table 2) the most prevalent food item was the tent caterpillar, which literally covered the ground and buildings during that time. By July most of the caterpillars were gone and the most common insects seen were ants and small beetles. Several geckos were captured while feeding on earwigs, mosquitoes, and homopterans.

TAIL REGENERATION While the geckos were being marked, the tails of several were broken. When recaptured, these animals were in various stages of tail regeneration. To determine more accurately the regenerative rate we broke the tails of numerous animals, juveniles and adults. Care was taken to break the tail near its base and when a natural

TABLE 2.—Stomach contents of Hemidactylus turcicus in May (N = 21 ) and July (N = 40), 1965 May July No. stomachs Percent No. stomachs Percent with items occurren-e with items occurrence I N SECTA 21 100.0 38 95.0 Lepidoptera 12 56.7 2 5.0 (caterpillars) Hymenoptera 5 23.8 10 25.0 Coleoptera 1 4.8 9 22.5 Hemiptera 1 4.8 7 17.5 Orthoptera 1 4.8 5 12.5 Diptera 1 4.8 3 7.5 Homoptera 0 0.0 6 15.0 Dermoptera 0 0.0 2 5.0 ARAC H NOIDEA 0 0.0 2 5.0 162 THE AMERICAN MIDLAND NATURALIST 79(1) break occurred on a distal portion, the tail was rebroken. After recapture the regenerated portion was measured. When a tail was broken there was little or no bleeding because of constriction of the blood vessels and an overall muscular contrac- tion such that the broken edges of the skin were drawn inward. Thus, a cap was formed over the exposed musculature. To determine a common base line to compare regenerative rate in different size groups we plotted the snout-vent length (abcissa) against the tail length of 15 juveniles, 10 males, and 10 females. A line was calculated using the method of least squares and this line was considered the median normal tail length at a particular snout- vent length. The regenerated portions were then expressed as a percent of the median normal length. This value was plotted against the number of days (abcissa) since the tail was broken (Fig. 1). During the course of this portion of the study (60 days) none of the geckos completely regenerated its tail. The most complete regeneration was by a juvenile — 84% in 35 days. In general the regenerative rate for juveniles was higher than that of males, and males higher than females; however, the differences were not sig- nificant at the 95% confidence interval (juveniles and females: t = 1.14, 22 df). Cagle (1946) reported that 11 Hemidactylus garnoti:z on the island of Tinian (Marianna Group) regenerated the tail completely in 20 to 65 days. Relative tail length (tail length/S-V length) increased ontogenetically. Two embryos had an average relative tail length of .73; eight juveniles between 25 and 34 mm S-V length, .94 (.87-1.05) ; eight animals between 35 and 44 mm, .96 (.92-1.02) ; and 15 adults above 45 mm, 1.07 (1.01-1.21).

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TIME (DAYS) Fig. 1.—Percent tail regeneration in male (m), female (f), and juvenile (j) Hemidactylus. The value plotted is the percent regeneration of the median normal tail length at a particular snout-vent length. 1968 ROSE ET AL.: ECOLOGY OF HEMIDACTYLUS 163

REPRODUCTION Sex was not determined in juvenile geckos. Of 130 adults sexed 49% were males. Several monthly samples deviated from the 1:1 ratio (Fig. 2) but the sample sizes were insufficient for reliable comparisons. FEMALES The reproductive season apparently extended from April to early August. The first female seen with large eggs (ovarian) was on 18 May, and the last female with oviducal eggs on 8 August. Eggs from the latter animal hatched on 22 September. Females mature the winter or spring of their second year. Two animals, 33 and 34 mm S-V, collected on 28 October 1964 (obviously summer hatchlings) were recaptured four and five times from early June to 12 and 28 August 1965. Both were females and both attained a S-V length of 54 mm. Even though both attained the S-V length required for follicle development, neither had enlarged eggs. A pair of geckos was observed copulating on 1 June 1965; no others were noted. The female was 49 mm S-V length and contained only small ovarian eggs (largest about 2.0 mm in diameter). Ap- parently sperm are stored since the eggs are fertilized in the oviduct. Whether multiple copulations are necessary for a female to lay twice

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MAY JUNE JULY Fig. 2.--Percent male (M), female (F), and juvenile (J) geckos collected in May (20), June (15). and July (30), 1965. 164 THE AMERICAN MIDLAND NATURALIST 79(1) in a season is not known. King (1958) observed copulating H. turcicus on 12 July in Gainesville, Florida. Members of the Gekkonidae characteristically have two eggs per clutch. Ovarian dissection of two females in May and one in June revealed that individual follicles between respective ovaries were at the same stage of development (Table 3). Apparently the follicles enlarge gradually to about 2.5 mm in diameter then undergo rapid vitellogenesis. Ovulation occurs when the follicles reach 8-8.5 mm in diameter. Yolking of the subsequent pair of follicles is delayed until after ovulation; however, some yolking may occur prior to laying. A female collected on 24 May contained two shelled eggs in the oviducts (shelled eggs are distinguishable from unshelled ones through the body wall by their white appearance). Fourteen days later she had only small yellow ovarian follicles, but on 25 July, she again contained two shelled oviducal eggs. Thus, about two months were required by this female to produce one clutch of two eggs. Quite possibly most females produce only two clutches per season but some may produce three. In three cases where we were able to follow the female from fall of 1964 through August, 1965, each animal produced two clutches. However, it is conceivable that if a female produces an early spring clutch she will have ample time to produce two more. Church (1962) noted that some female geckos contained two eggs in a single ovary large enough to be ovulated, ". . . but no case of a pair or more of eggs in the same oviduct was recorded." No H. turcicus contained two enlarged ova in a single ovary; however, one female contained two eggs in a single oviduct during this study. Egg laying and incubation period.-Despite intensive searching only one natural clutch was found. On 9 June, two eggs were found on the floor of a small unused closet which was littered with debris. The eggs were in the center of a cleared space about 25 mm in diameter and a gecko was close by. Twelve hours later the eggs were covered by small pieces of debris that formed a mound about 20 mm high. To determine if other females made such a nest, we constructed

TABLE 3.-Ova diameter in three Hernidactylus turcicus. The ova are arranged in order of decreasing diameter. Animal No. 1 also contained two unshelled oviducal eggs, 8.4 and 8.6 mm No.! No. 2 No. 3

1.8 2.0 2.5 2.5 1.8 2.0 1.5 1.6 1.4 1.4 1.5 1.5 1.3 1.4 1.2 1.3 1.0 1.0 1.0 1.0 1.0 1.0 0.6 0.6 0.8 0.8 0.6 0.6 0.3 0.3 0.8 0.8 0.5 0.5 0.2 0.2 0.7 0.7 0.5 0.5 0.2 0.2 1968 ROSE ET AL.: ECOLOGY OF HEMIDACTYLUS 165 a box 3' x 1' x 6" and filled it to a depth of inch with debris from the closet. Females with shelled oviducal eggs were placed in the box. All 12 females laid within one week and all constructed nests. If the eggs were subsequently exposed they were not re-covered. To our knowledge this was the first observation of nest building in the Gekkonidae. The eggs were ovoid, hard-shelled, and appeared large in com- parison to the female producing them. Their average length was 10.9 (10.4-11.7) mm and their average width, 8.9 (8.5-9.9) mm. Church (1962) noted that female H. frenatus ate the eggs, both naturally and under laboratory conditions. Oophagy by H. turcicus was not observed. The females were released and the "brooding box" remained in the closet at a temperature of about 31 C. The average incubation period was 40 (37-45) days for 11 eggs allowed to hatch. Church (1962) reported that the eggs of H. frenatus in the laboratory normally hatched in about three months, about 100% longer than the maximum for H. turcicus. Just prior to hatching the eggs appeared discolored. Apparently as hatching neared the internal egg membranes were broken down. This allowed the shell to become moistened and when the main body of the embryo rested against the internal surface, the shell be- came partially transparent. Hatching was not observed. Hatchlings.—The average snout-vent length of the 11 hatchlings was 25.9 (25.0-27.7) mm. Etheridge (1952) reported Hemidactylus from New Orleans with a snout-vent length of 22.3 mm, 10.8% smaller than our minimum. However, his animals were preserved prior to measuring (pers. comm.). King (1958) reported a minimum snout-vent length of 25 mm for H. turcicus from Gainesville, Florida. The young exhibited remarkable facility in resisting the dry en- vironment where the eggs were laid; neither water nor food was necessary for about a month. Three hatchlings in a clear plastic container were misplaced and not found for 26 days. At this time all three hatchlings were alive and we decided to continue starvation. Two died after 30 days and one after 33 days. Whether death was due to starvation or dehydration was not determined.

MALES The smallest male sexed was 42.5 mm S-V length. The size at sexual maturity was not determined. Although two or more males were found often behind the same drain, relatively little combat was observed. Two large males were found fighting in June, 1965. Either one or both emitted squeaking noises and their jaws were locked in combat. When disturbed they fell to the ground but neither released its grip until collected. Several males were collected with freshly amputated toes and tails and we attributed this to combat. Testicular cycle.—Testicular sections were prepared from geckos 166 THE AMERICAN MIDLAND NATURALIST 79(1) collected in January (4), April (2), May (4), July (3), August (2) and December (2). The tissue was fixed in Bouin's solution and the paraffin sections were stained with iron hematoxylin. The testicular cycle was similar to that reported for Uta stansburiana (Hahn, 1964) and essentially all temperate zone lizards. Spermatogenic activity began in late fall or early winter, the time of minimum testicular size. By December numerous primary spermatocytes were present, spermiogenesis was in progress, and maturing sperm were seen in clusters. The thin-walled epididymides contained no sperm. In January spermiogenesis continued but the lumina remained poorly developed. One out of four specimens contained a few sperm in the thin-walled epididymides. In April (Fig. 3, B and D) sperm were packed in the epididymides and the epididymal epithelium reached its maximum height. Spermiogenesis was active and the lumina were well developed and bordered by numerous maturing sperm. Thus, by April a male gecko was capable of inseminating a female. There was little change in the May testes. In July spermatogenic activity was reduced as was spermiogenesis but sperm remained packed in the epididymides. In August (Fig. 3, A and C) there was rapid regression of the testes. The lumina were

Fig. 3.--Section of the testis and epididymis of Hemidactylus. The Au;ust testis (A) is regressed, the epididymal ducts contain degeneratin -: germinal products (C), and the epididymal epithelium is thin. Maturin; sperm line the lumina in the April testis (B) and the epididymal epi:laelium is thick (D). 1968 ROSE ET AL.: ECOLOGY OF HEMIDACTYLUS 167

occluded with degenerating germinal elements and the epididymal walls were reduced in thickness.

DISCUSSION The Mediterranean gecko is firmly established in the southern United States. Since the animal is nocturnal, there is little or no overt competition with other lizards. Within the study area only two other lizards occur: Anolis carolinensis and Lygosoma laterale. Both these species are diurnal. In addition, Lygosoma is restricted to the ground and rarely ventures onto the buildings. Thus, in habitat choice and activity period Hemidactylus rarely comes into contact with other lizards. Probably H. turcicus has been introduced into New Orleans several times. When discovered the animal had already spread throughout much of the city. Whether it was introduced directly from the Old World, from populations already established on the eastern seaboard, from the West Indies, or from all these sources is unknown. Hemidactylus is capable of sustaining itself through the most severe winters in New Orleans (Etheridge, 1952) . The most de- vastating environmental phenomenon operative on the population while under our observation was the hurricane which struck New Orleans in September, 1965. The high winds ripped off shingles from the roof, and damaged drains. The driving rains filled cracks in the buildings with water. The population on the buildings was reduced severely in number after the disaster to the extent that a maximum of only five geckos was seen per night. Quite possibly the effect was not in killing the animals but in forcing them to disperse. The environmental factors regulating the reproductive cycle of Hemidactylus in New Orleans must be similar to those affecting the parent population, or the animal exhibits remarkable plasticity in adaptation. Although both temperature and day length probably affect the reproductive cycles of Hemidactylus, day length may be the controlling factor in New Orleans. For example, spermatogenic activity was reduced in July and testicular regression was completed in August. However, the mean monthly temperature does not start to fall until August. Day length, however, began to shorten in June. Unfortunately, no experimental evidence as to the effect of light and temperature on the reproductive cycle of Hemidactylus is available. The reduced rate of tail regeneration by females during the study may be associated with the reduction in energy available during the period of rapid vitellogenesis. Males would have more energy available since they would not have to yolk eggs. Apparently the geckos spend a great deal of time on the higher surfaces of the buildings. For example, some geckos were not seen for over a year between recaptures but when recaptured they were within 75 cm of the initial capture site. Since they were not observed on the lower surfaces in the intervening period, we assumed they 168 THE AMERICAN MIDLAND NATURALIST 79(1) were higher up on the buildings. Several unmarked animals were seen on the third-floor level and on the roof of one building. The building of a nest and covering the eggs with debris was unexpected. This explains why the eggs were not found previously in New Orleans and why we were unable to find more eggs. Apparently when no debris is available the geckos will lay on a clear surface, since eggs have been found in a filing cabinet in Gainesville, Florida ( Wayne King, pers. comm.). The ability of hatchlings to withstand starvation and dehydration for over 30 days is interesting. Although no accurate notes were kept on adults, they seemed to emaciate quickly in the absence of food. Young hatching in late September from eggs laid in August would not have to feed until October. In more temperate areas with the lower winter temperatures, young hatching late in the year might possibly be able to overwinter without feeding at all.

Acknowledgments.—We are grateful to Dr. Gerald Gunning for advice and especially to Dr. Clyde Jones for his numerous contributions during the course of this study. Dr. James Reed and Mr. Glen Clernmer aided us during various aspects of the project. REFERENCES BARBOUR, T. 1936. Two introduced lizards in Miami, Florida. Copeia, 1936: 113. CAGLE, F. R. 1946. Tail loss and regeneration in a Pacific island gecko. Ibid., 1946:16. CHURCH, G. 1962. The reproductive cycles of the Javanese house geckos, Cosymbotus platyuruc, Hemidactylus frenatus, and Pero pus mutilatus. Ibid., 1962:262-269. CONANT, R. 1958. A field guide to reptiles and amphibians. Houghton Mifflin Co., Boston. 366 p. ETHERIDGE, R. E. 1952. The warty gecko, Hemidactylus turcicus turcicus (Lin- naeus), in New Orleans, Louisiana. Copeia, 1952:47-48. HAHN, W. E. 1964. Seasonal changes in testicular and epididymal histology and spermatogenic rate in the lizard Uta stansburiana stejnegeri. J. Morphol., 115:447-460. KING, W. 1958. Observations on the ecology of a new population of the Medi- terranean gecko, Hemidactylus turcicus, in Florida. Quart. J. Florida Acad. Sci., 24:317-318. STE J NEGER, L. 1922. Two geckos new to the fauna of the United States. Copeia, 1922:56.

SUBMITTED 5 JANUARY 1967 ACCEPTED 10 APRIL 1967 \