2006 SOUTHEASTERN NATURALIST 5(2):227–234 Characteristics of the Foreclaw Display Behaviors of Female Trachemys scripta (Slider Turtles) R. Brent Thomas1,* and Ronald Altig2 Abstract - A common assumption is that titillation by adult female Trachemys scripta (Slider Turtles) always represents female participation in courtship, but there is only limited empirical support for this assertion and some data may contradict this supposition. Behavioral interactions were staged among wild-caught T. scripta throughout the local season of activity for this species (April–October). Each of 47 trials involved 6 turtles (total = 282 turtles: 94 melanistic males, 94 nonmelanistic males, 94 females) videotaped for 3 h (total = 141 h). During our study, titillation behaviors initiated by females were largely intrasexual, exhibited no peak during the local mating period, and did not stimulate males to attempt copulation. We concluded that such characteristics were inconsistent with the traditional assumption of a courtship function and were more consistent with the characteristics of agonistic signals, signals that communicate sender identity, or compound signals with multiple communicative functions that may change ontogenetically or in different social contexts. Because the communicative value(s) of these displays is not yet fully understood, we argue that the traditional term “titillation” that has been used to refer to these displays is inappropriate and should be replaced with “foreclaw display” which is neutral with respect to the potential communicative function(s). Introduction Bradbury and Vehrencamp (1998) define communication as an exchange of a signal between a sender and a receiver to the benefit of both parties and divide the types of information communicated into categories based on the type of information being exchanged: (1) sender identity, (2) sender location, and (3) specific contexts. Sender identity refers to signals that provide information regarding individual, species, sex, or social group recognition. Sender location signals relay information about the distance, altitude, or compass angle of the receiver relative to the sender. Signals in the contexts category involve such information as conflict resolution, territory defense, sexual interactions, parent-offspring interactions, social integration, environmental contexts, and autocommunication. However, a given signal may provide information dealing with information in all three categories simultaneously. Many turtles of both sexes in the family Emydidae perform elaborate display behaviors often referred to as “titillation” (Ernst et al. 1994). Jackson and Davis (1972a) described titillation as a complex, stereotyped series of movements in which the adducted forelimbs of the male are brought parallel to the head of the female, and the claws of the forelimbs are drummed and 1Division of Natural Sciences and Engineering, University of South Carolina Upstate, 800 University Way, Spartanburg, SC 29303. 2Department of Biological Sciences, PO Drawer GY, Mississippi State University, Mississippi State, MS 38762. *Corresponding author - rthomas@uscupstate.edu. 228 Southeastern Naturalist Vol. 5, No. 2 vibrated against the eyes and interocular region of the female. In this context, titillation is commonly assumed to be a courtship signal (Carpenter and Ferguson 1977, Ernst et al. 1994, Fritz 1991, Kramer and Burghardt 1998, Lovich et al. 1990a, Seidel and Fritz 1997). Adult males (Cagle 1950, Jackson and Davis 1972a, Taylor 1933, Zappalorti 1976), adult females (Jackson and Davis 1972b, Jackson 1977, Lovich et al. 1990a, Zappalorti 1976), and juveniles of both sexes (Cagle 1955, Kramer and Burghardt 1998, Morris 1976, Rives 1978) initiate and receive titillation behaviors. The receiver sometimes reciprocates the behavior toward the initiator (Ernst 1971, Rives 1978, Wahlquist 1970, Zappalorti 1976). Titillation behaviors performed by adults of either sex are thought to represent courtship displays, and juvenile titillation is thought to represent some form of precocial courtship (Kramer and Burghardt 1998). Suggestions that titillation may serve other functions (Cagle 1955, Rives 1978) have not been explored, and studies designed to specifically examine other possible communicative functions of female titillation behaviors have not been performed. The functions of any form of communication must be understood before conducting studies of sexual selection (e.g., mate-choice studies). Previous researchers of sexual selection in turtles assumed that titillation displays by either sex always represented at least a part of courtship regardless of context and that female choice is an important selective force within all species that perform such displays (see Berry and Shine 1980). It is important to examine the specific evidence that forms the basis for the conclusion that the titillation behavior by female emydids constitutes initiation of or participation in courtship. Ernst (1971) observed female Chrysemys picta (Schneider) initiating titillation on “several occasions” (number not specified), and males attempted to copulate subsequent to female titillation on three occasions. Lovich et al. (1990a) reported that female Trachemys scripta Schoepff sensu Seidel directed 5 titillations toward males during 47 trials, and in all cases males remained passive. Wahlquist (1970) reported a single observation of a captive, immature female Graptemys flavimaculata (Cagle) reciprocating the titillations of an adult male conspecific. Jackson and Davis (1972b) videotaped 1 male and 1 female Pseudemys concinna (Le Conte) in captivity for 8 h/day over a 10-day period in April and reported that the female “occasionally” (number not specified) performed titillation behaviors. Jackson (1977) reported female initiation of titillation between a single pair of adult Pseudemys nelsoni (Carr) in a tank that also contained several other species. Zappalorti (1976) stated that female C. picta stroke the forefeet of the male with their foreclaws to signal receptivity, but provided no data or citations to support this conclusion. Three attempted copulations preceded by titillation initiated by a female (Ernst 1971) provide the only support for the idea that titillation by females represents some part of courtship. All others mentioned above simply report that females performed titillation. Additionally, all such reports have been rather cursory during only a small fraction of the activity season, did not consider the possibility of intraspecific (or intrasexual) variation, and did not quantitatively examine the social contexts of the displays in order to question the potential communicative function(s). We 2006 R.B. Thomas and R. Altig 229 suggest that the assumption that titillation by females represents their participation in courtship is at best premature and that the literature provides very little supportive evidence. Some evidence seems to conflict with the assumption of a courtship function. For example, observations of immature individuals performing titillation, interspecific titillation, and the titillation of foreign objects such as food, pencils, and fingers (Rives 1978) suggests that titillation may communicate other types of information. The general rationale seems to be that if an emydid turtle of any sex titillates, then all members of that population and all members of all populations titillate under the same presumed behavioral scenario. Likewise, it has been commonly assumed that the communicative function of titillation behavior remains the same in every population, environment, social context, and season. Intraspecific and intrasexual variations in behavior are now considered normal, and typological attitudes regarding courtship behaviors are in conflict with current views (Foster and Endler 1998, Gross 1996). The purpose of our study was to quantitatively examine the characteristics of the titillation displays of female T. scripta in a controlled laboratory setting. If the longstanding assumption that female titillation constitutes female participation in courtship is correct, then the occurrences of these behaviors should have at least some of the following characteristics: (1) females should direct titillation toward adult males more often than toward females, (2) females should reciprocate the titillations of adult males more frequently than those initiated by other females, (3) the peak frequency of female titillations should occur more often during the local mating season (Sept. through Oct.; Thomas 2002, Thomas et al. 1999), and (4) female titillations should stimulate copulation attempts from males at some reasonable but unknown rate. We quantified the frequency and direction of female titillations, the frequency and direction of reciprocal titillations, and the number of times that copulation was attempted by a male after being titillated by a female, and examined seasonal variation in the frequency of these behaviors. Methods Hoop traps and basking traps were used to collect Trachemys scripta in several adjacent sewage lagoons near the campus of Mississippi State University, Oktibbeha County, MS (33°27'N, 88°47'W). Traps were usually checked every day from April through October 1997, and all individuals with elongated foreclaws, a cloaca positioned posterior to the carapace margin, and a plastron length greater than 110 mm were considered adult males. Individuals with a plastron length greater than 160 mm and lacking these secondary sex characteristics were considered adult females (Gibbons and Greene 1990). Turtles were haphazardly assigned to individual tanks (60 x 90 x 35 cm) for 24–48 h to allow them to adjust to laboratory conditions. Turtles were marked (Cagle 1939) and released at their point of capture after the completion of a trial. Individuals were not used more than once for any purpose in any of the trials, and individuals removed from the same trap at the same time were not used in the same trial. 230 Southeastern Naturalist Vol. 5, No. 2 The plastic experimental tanks were 70 x 145 x 40 cm. The tanks were drained, cleaned (first with soap, then with alcohol), rinsed, filled with fresh water to a depth of 30 cm, and allowed to age for at least 24 h after each trial. Wide-spectrum lighting provided a 12D:12L photoperiod, and the water temperature was maintained between 22 and 25 °C. All trials lasted 3 h and were conducted between 1030 and 1330 CST. Observational trials were recorded with an 8-mm video camera situated above the tank. Researchers were not in the laboratory at any time during a trial. The morphology and behavior of melanistic male T. scripta differs from that of nonmelanistic males and females, e.g., titillation behaviors of nonmelanistic males apparently serve a courtship function while the titillations performed by melanistic males are probably not associated with courtship (Thomas 2002). Because of these differences, we used the stages described by Tucker et al. (1995) to quantify stage of melanism (0 = nonmelanistic; 1 = limited melanic expression; 2 = fully melanistic) and, a trial consisted of placing two adult individuals of each of the following categories in the tank: (1) melanistic males (stage 2), (2) nonmelanistic males (stage 0 or 1), and (3) females. An identification number assigned to each turtle was written on the carapace with a grease pencil. The occurrence of titillation, reciprocal titillation, copulation attempts, and the identity of both the initiator and recipient were recorded from the tapes. A copulation attempt was defined as an individual attempting to mount by shifting into a position to copulate with another individual (see Davis and Jackson 1970), but the inability to actually see intromission required all of these to be conservatively considered as attempts. We noted whether or not a female initiated titillation prior to a copulation attempt by a male. Forty-seven trials (3 h/trial, total = 141 h) involving 6 turtles per trial (total = 282 turtles: 94 melanistic males, 94 nonmelanistic males, 94 females) were conducted as follows: April (N = 5), May (N = 7), June (N = 11), July (N = 9), August (N = 6), September (N = 6), and October (N = 3). The use of chi-squared statistic would be innappropriate given that observations within a trial were probably not independent. However, the results of each trial were independent of each other. Therefore, we followed the advice of Kramer and Schmidhammer (1992) and used ANOVA to compare both the mean number of titillations initiated by females across categories and mean rate of female reciprocations across categories (i.e., melanistic males, nonmelanistic males, and females). Separation of means was accomplished using Fisher’s LSD (Sokal and Rohlf 1994). A Kruskal-Wallis test compared the median monthly trial totals of female initiation of titillation (Conover 1971), i.e., the median of the total number of times that females initiatiated titillation in each of the individual trials conducted during a specific month. The Bonferroni procedure was used to adjust the type-I error rate for the three tests (i.e., 0.05/3 = 0.017; Sokal and Rohlf 1994). 2006 R.B. Thomas and R. Altig 231 Results Female Trachemys scripta initiated titillation during 33 (70.2%) of the 47 trials. Female initiated titillation occurred 198 times and 113 of these displays were directed toward females, 39 toward melanistic males, and 46 toward nonmelanistic males. On average, female T. scripta directed titillations toward the other female 3.5 times/trial, toward melanistic males 1.2 times/trial, and nonmelanistic males 1.4 times/trial. Females directed their titillation behaviors toward the other female significantly more often than toward melanistic or nonmelanistic males (F = 4.923; d.f. = 2, 93; P = 0.009). Mean separation procedures indicated no significant difference between the number of female titillations directed toward melanistic and nonmelanistic males (P = 0.789). Females received a total of 597 titillations: 188, 296, and 113 from melanistic males, nonmelanistic males, and females, respectively. Reciprocal titillation by female T. scripta was observed during 18 (38.3%) of the 47 trials (Table 1). In response to receiving titillation, females reciprocated titillation 39 times (melanistic males = 16, nonmelanistic males = 3, females = 20). The overall reciprocation rate for all trials (percent of time that females responded by reciprocating the titillation bout initiated by another individual of a specific category) was 17.4, 8.6, and 1.0% for females, melanistic males, and nonmelanistic males respectively. Females reciprocated the titillations of other females significantly more frequently than those of melanistic and nonmelanistic males (F = 4.749; d.f. = 2, 83; P = 0.011). However, the results of mean separation procedures indicated no significant difference between female reciprocation rate for titillations received from melanistic and nonmelanistic males (P = 0.937). Males attempted copulation 233 times during the trials, but none of these attempts occurred subsequent to female initiated titillation toward a male. The median monthly trial totals for female titillations were not significantly different (H = 9.312; d.f. = 6; P = 0.157; Table 1); thus, no peak in the median monthly trial frequency of female titillations was observed. Discussion If the sole purpose of titillation by female T. scripta is participation in or elicitation of courtship, then at least an indication of the predictions stated in Table 1. Number of trials during each month, mean (± SE), median, and range of monthly trial totals for female initiation of titillation followed by the percent of trials in which females initiated or reciprocated titillation. % trials % trials with female with female Month # trials Mean (± SE) Median Range initiation reciprocation April 5 6.2 (4.8) 3.0 0–25 60.0 20.0 May 7 1.7 (1.4) 0.0 0–10 42.9 14.3 June 11 5.1 (1.6) 3.0 0–18 90.9 45.5 July 9 6.9 (2.4) 3.0 0–21 88.9 55.6 August 6 2.7 (2.5) 0.0 0–15 33.3 16.7 September 6 2.3 (0.9) 2.0 0–5 66.7 50.0 October 3 2.3 (0.9) 2.0 1–4 100.0 66.7 Overall 47 4.2 (0.9) 2.0 0–25 70.2 38.3 232 Southeastern Naturalist Vol. 5, No. 2 the introduction should have been observed. We observed the converse of each of these predictions and found no evidence to support the idea that female titillation is any sort of courtship signal. Specifically, female titillation behaviors were directed toward females more frequently than toward other males, exhibited no obvious peak during the local mating period, and did not stimulate males to attempt copulation. We suggest that signals with such characteristics are more likely to communicate something about the identity of the sender or information relevant to some yet unknown aspect(s) of conflict resolution (see Rives 1978 for similar arguments). Similarly, titillations by melanistic male T. scripta may not serve a courtship function, but titillation may function as a courtship signal for nonmelanistic males (see Thomas 2002). Melanistic males and females are on average larger, older, and probably more experienced than nonmelanistic males (Lovich et al. 1990b). It is possible that these larger individuals use titillation to communicate different types of information than the smaller nonmelanistic males, and thus the communicative functions of these behaviors likely change ontogenetically. Further research should address the influence of the relative size of individuals, density of individuals, sex ratio, age, experience, or other demographic factors on the display behaviors of T. scripta. For example, the current study is not sufficient to determine to what extent (if at all) female T. scripta alter their display behaviors in the presence of different numbers of conspecifics. Likewise, the possibility of geographic variation cannot be dismissed. The possibility that our results were solely an artifact of an unnatural lab situation, while possible, seems unlikely. The initiation of social behaviors occurred within a few minutes of the beginning of a trial, and turtles did not spend a great deal of time swimming around the perimeter of the tank in an attempt to escape. Trial animals were not long-term captives (i.e., only held 48 h or less prior to a trial), and corticosterone levels (an indicator of stress) of (non-trial) T. scripta housed under trial conditions were comparable to those of wild T. scripta (W.B. Cash, Maryville College, Maryville, TN, unpubl. data). The photoperiod was held constant during all trials rather than changing photoperiod seasonally to reflect natural patterns of day length, and it is possible that the lack of seasonal differences in female initiation of titillation could have been the result of an “unchanging” photoperiod. While possible, it may be premature to make such an inference given the paucity of studies that specifically examine the impact(s) of photoperiod on turtle behavior (see Burger 1937, Cash 2000). Additionally, non-melanistic male T. scripta were tested under exactly the same set of “unchanging” conditions and exhibited significant seasonal differences in regards to initiation of titillation behaviors in spite of the constant photoperiod (Thomas 2002). Therefore, if constant laboratory photoperiod influenced the behavior of test animals, then it must have differentially influenced female and nonmelanistic male T. scripta. Further research on the specific impact(s) of photoperiod on turtle behavior/physiology is needed before such issues can be addressed knowledgeably. In summary, we found no evidence to support the assumption that titillation by female T. scripta serves a courtship function and the evidence in the literature is not sufficient to support this widely accepted assertion; in some 2006 R.B. Thomas and R. Altig 233 cases, the data seem contradictory to a courtship explanation (e.g., Rives 1978). We conclude that courtship may not be the purpose (or at least not the sole purpose) for female titillations and that such displays may communicate other types of information. To avoid similar logical errors as discussed above, we note that it is premature to dismiss the possibility that female titillation may serve a courtship function in other situations or social contexts (e.g., different density, species composition, size/age composition, or sex ratio). We further argue that the term “titillation” explicitly provides the connotation that these displays are exclusively involved in courtship. Given that the available evidence is insufficient to support such connotations, we suggest that the term should be replaced with “foreclaw display,” a neutral term with respect to the potential communicative function(s) of such behaviors. Acknowledgments All animals were collected under MSU-IACUC protocol approval number 96- 010. We wish to acknowledge the support of Mississippi State University Department of Biological Sciences and the University of South Carolina Upstate Division of Natural Sciences and Engineering. We also thank C.M. Taylor, W.J. Diehl, P. Gerard, and W.S. Parker, and two anonymous reviewers for their helpful comments on previous versions of this manuscript. Literature Cited Berry, J.F., and R. Shine. 1980. Sexual size dimorphism and sexual selection in turtles (order Testudines). Oecologia 44:185–191. Bradbury, J.W., and S.L. Vehrencamp. 1998. Principles of Animal Communication. Sinauer Associates, Inc., Sunderland, MA. 882 pp. Burger, J.W. 1937. Experimental sexual photoperiodicity in the male turtle, Pseudemys elegans (Wied). American Naturalist 71:481–487. Cagle, F.R. 1939. A system for marking turtles for future identification. Copeia 1939:170–173. Cagle, F.R. 1950. The life history of the Slider Turtle, Pseudemys scripta troostii (Holbrook). Ecological Monographs 20:32–54. Cagle, F.R. 1955. Courtship behavior in juvenile turtles. Copeia 1955:307. Carpenter, C.C., and G.W. Ferguson. 1977. Variation and evolution of stereotyped behavior in reptiles. Pp. 335–554, In C. Gans and D.W. Tinkle (Eds.). Biology of the Reptilia. Academic Press, New York, NY. 722 pp. Cash, W.B. 2000. Behavioral and physiological ecology of the Slider Turtle: Laboratory and field studies integrating hormonal and behavioral aspects. Unpublished Ph.D. Dissertation. University of Mississippi, Oxford, MS. 153 pp. Conover, W.J. 1971. Practical Nonparametric Statistics. John Wiley and Sons, Inc., New York, NY. 462 pp. Davis, J.D., and C.G. Jackson, Jr. 1970. Copulatory behavior in the Red-eared Turtle, Pseudemys scripta elegans (Wied). Herpetologica 26:238–240. Ernst, C.H. 1971. Observations of the Painted Turtle, Chrysemys picta. Journal of Herpetology 5:216–220. Ernst, C.H., J.E. Lovich, and R.W. Barbour. 1994. Turtles of the United States and Canada. Smithsonian Institution Press, Washington, DC. 578 pp. Foster, S.A., and J.A. Endler. 1998. Geographic Variation in Behavior: Perspectives on Evolutionary Mechanisms. Oxford University Press, New York, NY. 352 pp. 234 Southeastern Naturalist Vol. 5, No. 2 Fritz, U. 1991. Balzverhalten und systematik in der subtribus Nectemydina 2. Vergleich oberhalb des artniveaus und anmerkungen zur evolution. Salamandra 27:129–142. Gibbons, J.W., and J.L. Greene. 1990. Reproduction in the Slider Turtle and other species of turtles. Pp. 124–134, In J.W. Gibbons (Ed.). Life history and Ecology of the Slider Turtle. Smithsonian Institution Press, Washington, DC. 368 pp. Gross, M.R. 1996. Alternative reproductive strategies and tactics: Diversity within sexes. Trends in Ecology and Evolution 11:92–98. Jackson, Jr., C.G. 1977. Courtship observations on Chrysemys nelsoni (Reptilia, Testudines, Testudinidae). Journal of Herpetology 11:221–222. Jackson, Jr., C.G., and J.D. Davis. 1972a. A quantitative study of courtship display of the Red-eared Turtle, Chrysemys scripta elegans (Wied). Herpetologica 28:58–64. Jackson, Jr., C.G., and J.D. Davis. 1972b. Courtship display behavior of Chrysemys concinna suwanniensis. Copeia 1972:385–387. Kramer, M., and G.M. Burghardt. 1998. Precocious courtship and play in emydid turtles. Ethology 104:38–56. Kramer, M., and J. Schmidhammer. 1992. The chi-squared statistic in ethology: Use and misuse. Animal Behaviour 44:833–841. Lovich, J.E., W.R. Garstka, and W.E. Cooper, Jr. 1990a. Female participation in courtship behavior of the turtle Trachemys s. scripta. Journal of Herpetology 24:422–424. Lovich, J.E., C.J. McCoy, and W.R. Garstka. 1990b. The development and significance of melanism in the Slider Turtle. Pp. 233–254, In J.W. Gibbons (Ed.). Life History and Ecology of the Slider Turtle. Smithsonian Institution Press, Washington DC. 368 pp. Morris, M.A. 1976. Courtship-like behavior of immature turtles. Herpetological Review 7:110–111. Rives, J.D. 1978. A comparative study of courtship-related behavior in immature emydid turtles of two species. Unpublished M.Sc. Thesis. University of Southwestern Louisiana, Lafayette, LA. 114 pp. Seidel, M.E., and U. Fritz. 1997. Courtship behavior provides additional evidence for a monophyletic Pseudemys, and comments on Mesoamerican Trachemys (Testudines: Emydidae). Herpetological Review 28:70–72. Sokal, R.R., and F.J. Rohlf. 1994. Biometry. W.H. Freeman and Company, New York, NY. 887 pp. Taylor, E.H. 1933. Observations on the courtship of turtles. University of Kansas Science Bulletin 21:269–271. Thomas, R.B. 2002. Conditional mating strategy in a long-lived vertebrate: Ontogenetic shifts in the mating tactics of male Slider Turtles (Trachemys scripta). Copeia 2002:456–461. Thomas, R.B., N. Vogrin, and R. Altig. 1999. Sexual and seasonal differences in behavior of Trachemys scripta (Testudines: Emydidae). Journal of Herpetology 33:511–515. Tucker, J.K., R.J. Maher, and C.H. Theiling. 1995. Melanism in the Red-eared Slider (Trachemys scripta elegans). Journal of Herpetology 29:291–296. Wahlquist, H. 1970. Sawbacks of the Gulf Coast. International Turtle and Tortoise Society Journal 4:10–13. Zappalorti, R.T. 1976. The Amateur Zoologist’s Guide to Turtles and Crocodilians. Stackpole Books, Harrisburg, PA. 208 pp.