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Three types of head movement associated with premounting courtship displays in freshwater turtles. A) Head bobbing: vibrating the head and neck vertically (modified from Hidalgo 1982). B) Swaying: vibrating the head and neck horizontally (modified from Bels and Crama 1994). C) Swaying on the female’s carapace: vibrating the head and neck horizontally on the female’s carapace (modified from Baker and Gillingham 1983). 

Three types of head movement associated with premounting courtship displays in freshwater turtles. A) Head bobbing: vibrating the head and neck vertically (modified from Hidalgo 1982). B) Swaying: vibrating the head and neck horizontally (modified from Bels and Crama 1994). C) Swaying on the female’s carapace: vibrating the head and neck horizontally on the female’s carapace (modified from Baker and Gillingham 1983). 

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Freshwater turtle courtship is an exciting and potentially phylogenetically important field of study. Scattered data exist from the past century of research, yet no recent summary is available. Courtship in freshwater turtles includes a number of common behaviors, which usually involve visual, tactile, olfactory, and auditory signals. These signals...

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Context 1
... which are common in chelonid courtship, may be involved with visual, tactile, and chemical signals. Head movements can be placed in 3 general categories: 1) head bobbing (vibrating the head and neck vertically); 2) swaying (swinging the head and neck horizontally without contacting the female); and 3) head movement on the female's carapace (Fig. 2). Table 3 lists variations on courtship-related head ...
Context 2
... only recently become a topic of organized research. Vocalizations have been reported in Table 3. Variable forms of head movement in male freshwater species. Head movements are classified into 3 types: HB, head- bobbing; S, swaying; and SOFC, swaying on the female's carapace. Details of the classification and descriptions are provided in text and Fig. 2 Pseudemys concinna suwanniensis (Rose 1950), but at the time of this publication, turtles were generally considered incapable of giving or receiving auditory stimuli (Pope 1955). Weaver and Vernon (1956) confirmed that many turtle species are, in fact, sensitive to airborne sounds, particularly sounds below 1000 Hz. Vocalizations are ...

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... Emydid turtles have highly developed tetrachromatic UV/VIS vision and colour discrimination abilities (Arnold and Neumeyer 1987), based on the most complex cone system found in vertebrates (Grotzner et al. 2020), with good ability to detect bright colours such as yellow and red in shallow water (Hall et al. 2018a). Both visual and olfactory cues play important roles in freshwater turtles' food recognition abilities (Vieyra 2011), sexual selection (Lovich et al. 1990;Liu et al. 2013) and intra and interspecific communication (Brejcha and Kleisner 2016). ...
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Recent studies showed that freshwater turtles display inter-individual differences in various behavioural traits, which may influence their health and welfare in captivity due to differences in response to husbandry and enrichment strategies and in ability to cope with the limitations of the captive environment. This study investigated a possible correlation between individual level of escape behaviour under standard enrichment conditions and level of interest in coloured objects in a group of cooters Pseudemys sp. and sliders Trachemys scripta ssp. on display at a public aquarium. Interest in different colours, colour preference and individual differences in behavioural changes in the presence of the new enrichment were also studied. Turtles categorised as 'high' and 'moderate escape behaviour' (17-34% of behavioural budget) showed more interest in coloured objects and tended to display less escape behaviour in their presence, while turtles categorised as 'low escape behaviour' (<10% of behavioural budget) were less interested in coloured objects and tended to display more escape behaviour in their presence. Overall, there was more interest in yellow than in red, white or green objects, with more contacts with coloured objects before feeding and at the start of each observation period and a preference for yellow against red objects. The individual differences in behavioural changes in the presence of the new enrichment suggested that more studies into colour preference and response to novelty in turtles would be beneficial to ensure that no individuals are unduly stressed by new enrichments.
... During courtship, these species perform head bobbing, used as a visual display to other conspecifics, but that may also serve to disperse chemicals from MG secretions during sexual encounters 60 . Head bobbing as well as other head movements displayed during courtship are widespread in chelonians [61][62][63] , including both species with and without MGs that are phylogenetically distant. This would argue against courtship head movements mediating chemical signaling as a primary function. ...
... Therefore, the loss of MGs in a given lineage could be mitigated by development of other channels of communication. Besides chemical signals, chelonians may also use tactile, auditory and visual cues to communicate 62,68 . Available data on turtle communication is scarce (see 62,64 for a review), which hinders an understanding of how and if signaling channels could be compensated by one another. ...
... Besides chemical signals, chelonians may also use tactile, auditory and visual cues to communicate 62,68 . Available data on turtle communication is scarce (see 62,64 for a review), which hinders an understanding of how and if signaling channels could be compensated by one another. Many turtle species possess sexually dichromatic color patches, stripes and dots on their bodies, especially on the head and limbs [69][70][71][72] . ...
Article
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Despite the relevance of chemical communication in vertebrates, comparative examinations of macroevolutionary trends in chemical signaling systems are scarce. Many turtle and tortoise species are reliant on chemical signals to communicate in aquatic and terrestrial macrohabitats, and many of these species possess specialized integumentary organs, termed mental glands (MGs), involved in the production of chemosignals. We inferred the evolutionary history of MGs and tested the impact of macrohabitat on their evolution. Inference of ancestral states along a time-calibrated phylogeny revealed a single origin in the ancestor of the subclade Testudinoidea. Thus, MGs represent homologous structures in all descending lineages. We also inferred multiple independent losses of MGs in both terrestrial and aquatic clades. Although MGs first appeared in an aquatic turtle (the testudinoid ancestor), macrohabitat seems to have had little effect on MG presence or absence in descendants. Instead, we find clade-specific evolutionary trends, with some clades showing increased gland size and morphological complexity, whereas others exhibiting reduction or MG loss. In sister clades inhabiting similar ecological niches, contrasting patterns (loss vs. maintenance) may occur. We conclude that the multiple losses of MGs in turtle clades have not been influenced by macrohabitat and that other factors have affected MG evolution.
... Available literature hints that the behavior and social systems of Testudines are complex (e.g., Kramer 1989;Pearse and Avise 2001;Davis and Burghardt 2007, 2011Burghardt 2013;Hites et al. 2013;Brejcha and Kleisner 2016); however, preconceived, albeit unfounded, notions of behavioral simplicity in this taxon and difficulties associated with studying the cryptic habits of aquatic species have hampered detailed behavioral investigations of wild Testudines. There have been longstanding appeals for published studies of testudine reproductive biology and behavior (Carpenter and Ferguson 1977;Harless 1979;Berry and Shine 1980;Liu et al. 2013), but most reports are anecdotal and lack the replication necessary for rigorous hypothesis testing. ...
... The mating tactics of Testudines are highly variable, spanning a spectrum from apparently amiable courtship to coercion (Berry and Shine 1980;Liu et al. 2013). Male aggression may be an effective mating tactic if coercive behaviors (e.g., chasing, biting, forced submergence) facilitate female receptivity or acquiescence through demonstration of male dominance or strength (Gibbons and Lovich 1990;Liu et al. 2013). ...
... The mating tactics of Testudines are highly variable, spanning a spectrum from apparently amiable courtship to coercion (Berry and Shine 1980;Liu et al. 2013). Male aggression may be an effective mating tactic if coercive behaviors (e.g., chasing, biting, forced submergence) facilitate female receptivity or acquiescence through demonstration of male dominance or strength (Gibbons and Lovich 1990;Liu et al. 2013). Tortoises (Testudines: Testudinidae) are reputed for their coercive tactics (Hailey 1990;Sacchi et al. 2003;Golubović et al. 2018) and use of sexual weaponry (Auffenberg 1977;Tuma 2016). ...
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Males and females have divergent reproductive interests arising from their unequal investments in offspring. This sexual conflict drives an antagonistic arms race that influences sex-specific reproductive success. Alternative reproductive tactics are expected in long-lived species for which the reproductive strategy that maximizes mating success could differ across body sizes. The mating strategy of the painted turtle (Chrysemys picta) has been characterized as an elaborate and amiable male courtship display during which males use their elongate foreclaws to stroke females, coupled with female mate choice. Contrary to this long-held understanding, in situ field observations and experimental trials from our long-term study in Algonquin Provincial Park, Canada, demonstrate that males also exhibit an alternative, coercive mating strategy. Males are equipped with sexually size dimorphic tomiodonts, tooth-like cusps of the beak, as well as a weaponized anterior shell, with which they wound the head and neck of females. Behavioral trials during the breeding periods showed that male reproductive tactics shift from courtship (foreclaw display) to coercion (striking, biting, and forced submergence) across ontogeny, and male size predicts the occurrence and frequency of coercive behavior. We found phenotype-behavior matching whereby small males invest in putatively ornamental foreclaws used for courtship and large males invest in weaponry for coercion, challenging existing knowledge of this well-studied species. As a group with a long evolutionary history and varied mating systems, Testudines are a particularly interesting taxon in which to ask questions about mating system evolution. Significance statement Alternative reproductive tactics are hypothesized for long-lived species. We quantified a shift from apparent courtship to coercive tactics during the reproductive lifespan of a well-studied freshwater turtle. Male painted turtles (Chrysemys picta) have sexual weapons that are used to promote female acquiescence. Using behavioral trials with turtles from a long-term study population, we demonstrate that males match their morphology (ornament/weapons) to reproductive behavior (courtship/coercion) as their reproductive tactics shift. Our findings hint at the behavioral complexity of aquatic turtles, a challenging and often-overlooked group in behavioral studies.
... species and sex) but should eliminate individual bias (Apps et al. 2015), and no tortoises ever experienced their own secretions, even with pooling. b Painted resin tortoise model, like that used in this study Behaviours (16) observed and timed included a priori behaviours identified from prior tortoise-tortoise interactions (similar to those found in other chelonian behaviour studies: Bels and Crama 1994;Ruby and Niblick 1994;Kazmaier et al. 2001;Liu et al. 2013;Sacchi et al. 2013;Cutili et al. 2014), including sniffing, head extension, doubleback to a treatment, eating or resting near a treatment, head bobbing, biting at model, nose-to-nose interactions, carapace alignment, charging or shoving model, mounting/climbing on model, tasting or biting at air near a model, scratching/rubbing, pulling into shell, and direct approach (e.g. sudden vigilance of model, leading to direct advance and confrontation of model from across the arena without other behaviours exhibited). ...
Article
Multimodal signalling reinforces specific messages in communication. In gopher tortoises, similar to other reptilian species, visualization of conspecific and chemical exudates from the skin may serve as a multimodal display advertising information about conspecific species, sex, or individual qualities, but this has not been fully elucidated. For gopher tortoises, one such possible source of chemical cues could be secretions from seasonally enlarged mental glands (MG). Here, we used both sexes of gopher tortoises in a paired choice presentation of MG secretions vs. distilled (DI) water on resin tortoise models to assess visual presence with tortoise-specific secretions. We examined behaviours to treatments to examine if MG secretions are recognizable olfactory cues and if visual cues alone are sufficient to maintain social interactions using a simple visual presentation vs. a complex visual and olfactory presentation. Tortoises of both sexes spent more total time (p < 0.001) and performed a greater number of behaviours (p < 0.001) towards the MG-treated model, relative to the neutral control (DI-treated model), suggesting that olfactory MG secretions are also required, along with visual presence of a tortoise, to engage in social behaviours. Our results are among the first for this species suggesting that pheromone usage may drive social interactions in social behaviours.
... This behavior is followed by a second phase that involves smelling the cloacal region to identify conspecific females (Auffenberg 1965(Auffenberg , 1977. Most studies on the reproductive behavior of Testudines have focused on the stages after males and females have already detected one another and on the act of copulation (Niblick, Rostal and Classen 1994;Pellitteri-Rosa et al. 2011;Liu et al. 2013;Cutuli et al. 2013). Very little attention has been given to how solitary species, such as tortoises, find each other in the wild during the pre-copulatory stage. ...
Article
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The pre-copulatory behavior of the Mediterranean Spur-thighed Tortoise (Testudo graeca), especially the means by which males and females find each other in the breeding season, has been poorly addressed. We conducted behavioral experiments to investigate the pre-copulatory behavior of sexually mature T. graeca males and females under semi-natural and restrictive captive conditions. We found that when females were kept under constraining captive conditions, they were no longer approached by males during the breeding season. However, when the females were under semi-natural conditions during the breeding season, males displayed significantly more sniffing, patrolling, and climbing events toward the opposite sex. Moreover, males, that were located inside an enclosure where they could move freely toward surrounding conspecifics, which they could not see, showed a clear preference for the female side of the enclosure. During the non-breeding season, none of these behaviors were displayed. It seems that the mating season begins with males sensing, most likely through a chemo-orientation, the location of females but not vice versa. We suggest that restrictive captivity in females could lead to suppressed reproductive behavior in both sexes, including the pre-copulatory searching behavior that males normally exhibit in the wild. This study presents novel information on the pre-copulatory behaviors of this vulnerable tortoise and emphasizes the importance of housing T. gracea individuals under semi-natural rather than restrictive captive conditions during the breeding season.
... Background-matching coloration is likely to represent camouflage (Rowe, Clark, Ryan, & Tucker, 2006;Rowe et al., 2014), while more conspicuous colors may play a role in species recognition and courtship (Brejcha & Kleisner, 2016;Liu, Davy, Shi, & Murphy, 2013). ...
Article
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Like coloration of the integument, eye color can be a significant but understudied component of communication and reproductive behavior. Eye color can change with sexual maturation and become sexually dimorphic, but in a few birds and fish, eye color can also change rapidly in response to the environment. There are few cases of the latter, and we report here several instances of such change in eye color in the Eastern box turtle (Terrapene carolina carolina), the first non‐avian tetrapod in which this capability has been reported. In male turtles, the iris changed from a pale yellow color (often characteristic of juveniles) to a bright red color (characteristic of mature males) in a period of <5 s. The nature of the color change is similar to that observed in some birds and suggests a common mechanism and/or adaptive role, which could be further explored in Eastern box turtles. Box turtles have the ability to rapidly change iris color, the first time this has been observed in a non‐bird reptile. The function may relate to intraspecific communication, given the differing eye colors of adult box turtles and developmental change in eye color.
... Males of bottom-walking and semi-aquatic species predominantly demonstrate forced copulation (Berry and Shine 1980). Coercive mating tactics are associated with male-biased size dimorphism, limited mobility, and the inability of females to escape male sexual advances (Berry and Shine 1980;Liu et al. 2013;Keevil et al. 2017). Conversely, in aquatic free-swimming species, male precoital courtship behaviour and (or) use of nuptial structures are the principle mating strategy, coupled with female mate choice (Berry and Shine 1980). ...
... Conversely, in aquatic free-swimming species, male precoital courtship behaviour and (or) use of nuptial structures are the principle mating strategy, coupled with female mate choice (Berry and Shine 1980). Members of this latter group typically demonstrate a larger female body size, male nuptial structures (e.g., elongate foreclaws) with associated courtship behaviour, and high mobility (Berry and Shine 1980;Gibbons and Lovich 1990;Liu et al. 2013). ...
... In Testudines, harassment by males can include chasing, biting, ramming (shell clapping, clattering, butting), and tail prodding (Thomas 2002;Liu et al. 2013). As is consistent with sexually coercive behaviour among animals, male Testudines direct biting on the soft tissue of the head, neck, and shoulders (Comuzzie and Owens 1990), but may also direct attacks at the shell, limbs, or tail (Evans 1953;Legler 1955;Davis and Jackson 1973;Auffenberg 1977;Kauffmann 1992;Bels and Crama 1994;Lee and Hays 2004;Schneider et al. 2010). ...
Article
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Sexually coercive reproductive tactics are widespread among animals. Males may employ specialized structures to harass, intimidate, or physically harm females to force copulation, and injuries to the head and neck are reported in taxa with sexually coercive mating systems. The mating tactics of Painted Turtles (Chrysemys picta (Schneider, 1783)) are typically described as involving male courtship and female choice. In contrast, female Painted Turtles in our study population display injuries on the head and neck indicative of bite wounds inflicted by sexually dimorphic tomiodonts and weaponized shell morphology of males during reproductive interactions. Using a 24-year dataset, we demonstrate population-level trends in soft tissue wounds inflicted by conspecifics. Adult females experienced more wounding than adult males or juveniles, and larger females had a greater probability of wounding than smaller females. Wounding was concentrated on the dorsal head and neck of females, consistent with expectation of sexual coercion. Furthermore, elevated rates of fresh wounding occurred during late summer, concurrent with the breeding period. By assessing wound demographics, we provide indirect evidence that the tomiodonts and shell of male Painted Turtles inflict injury and function as sexual weapons. These findings shed new light on our understanding of mating system complexity in an often-overlooked and difficult-to-observe taxonomic group.
... Colour ornaments are designed to maximize their conspicuousness only in certain, ethologically relevant contexts [39], e.g. when exposed to rivals during contests or to mates during courtship [40,41]. Courtship in freshwater turtles takes place underwater and males adopt characteristic positions relative to the female [42]. Deirocheline turtles are characterized by elaborate courtship behaviour including a complex forelimb display known as titillation [42]. ...
... Courtship in freshwater turtles takes place underwater and males adopt characteristic positions relative to the female [42]. Deirocheline turtles are characterized by elaborate courtship behaviour including a complex forelimb display known as titillation [42]. Males in most species of deirocheline turtles perform the titillation display facing the female while swimming backwards in front of her, close to the water surface; however, males of the genus Pseudemys titillate while swimming above and parallel to the female, facing the same direction as her [42][43][44][45][46][47]. ...
... Deirocheline turtles are characterized by elaborate courtship behaviour including a complex forelimb display known as titillation [42]. Males in most species of deirocheline turtles perform the titillation display facing the female while swimming backwards in front of her, close to the water surface; however, males of the genus Pseudemys titillate while swimming above and parallel to the female, facing the same direction as her [42][43][44][45][46][47]. Thus, depending on the position adopted during courtship (face-to-face versus swim above) males of different species expose different body areas to females. ...
Article
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Animal body coloration is a complex trait resulting from the interplay of multiple mechanisms. While many studies address the functions of animal coloration, the mechanisms of colour production still remain unknown in most taxa. Here we compare reflectance spectra, cellular, ultra- and nano-structure of colour-producing elements, and pigment types in two freshwater turtles with contrasting courtship behaviour, Trachemys scripta and Pseudemys concinna. The two species differ in the distribution of pigment cell-types and in pigment diversity. We found xanthophores, melanocytes, abundant iridophores and dermal collagen fibres in stripes of both species. The yellow chin and forelimb stripes of both P. concinna and T. scripta contain xanthophores and iridophores, but the post-orbital regions of the two species differ in cell-type distribution. The yellow post-orbital region of P. concinna contains both xanthophores and iridophores, while T. scripta has only xanthophores in the yellow-red postorbital/zygomatic regions. Moreover, in both species, the xanthophores colouring the yellow-red skin contain carotenoids, pterins and riboflavin, but T. scripta has a higher diversity of pigments than P. concinna. Trachemys s. elegans is sexually dichromatic. Differences in the distribution of pigment cell types across body regions in the two species may be related to visual signalling but do not match predictions based on courtship position. Our results demonstrate that archelosaurs share some colour production mechanisms with amphibians and lepidosaurs (i.e. vertical layering/stacking of different pigment cell types and interplay of carotenoids and pterins), but also employ novel mechanisms (i.e. nano-organization of dermal collagen) shared with mammals.
... A seleção fenotípica tem possibilitado a observação de algumas particularidades em níveis especíe-específico, populacional e até mesmo entre os diferentes gêneros sexuais (Licht, 1984;Ceballos et al., 2013;Liu et al., 2013). Muito dessas diferenças na história de vida e na capacidade de quelônios em se adaptar às condições ambientais distintas está associado aos diferentes aspectos reprodutivos do grupo . ...
... Apenas a LRC dos filhotes não diferiu entre os substratos de nidificação (P = 0.1781), como também não foi observado efeito do tamanho das fêmeas sob os tamanhos dos filhotes na areia (F = 1.038, df = 27, P = 0.317) e nos barrancos (F = 0.277, df = 37, P = DISCUSSÃO A seleção fenotípica tem possibilitado a observação de diferenças substanciais na história de vida e na capacidade de diferentes espécies de quelônios em se adaptar a condições ambientais distintas Refsnider e Janzen, 2012). Esta plasticidade muitas vezes está associada a diferentes aspectos reprodutivos do grupo, como observadas particularidades em nível específico, populacional e até mesmo entre os diferentes gêneros sexuais (i.e., ciclo reprodutivo dissociado:Licht, 1984; evidentes caracteres sexuais secundários:Ceballos et al., 2013; ou ainda fêmeas e machos tendo poder de escolha durante a coorte:Liu et al., 2013). No caso das fêmeas de tracajá (P. ...
Thesis
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When one observes the life history of any organism, in addition to the physiological, behavioral, and morphological adaptations modified over time, there are also individual adjustments in response to environmental changes, and ecological interactions in the environment. This doctoral thesis documents important information on the life history of the Yellow-Spotted Amazon River Turtle (Podocnemis unifilis), describing some aspects of biology focusing on the nests associated with different incubation substrates, and the consequences of a generalist nesting on the success of the offspring, sex ratio, and possible interspecific interactions. How the investment of females was different for each type of substrate, potentially different was the life history of nests incubated under different environmental conditions (i.e., clutch size, time of incubation, eclosion success, and success incubation, and hatchlings size). As the heat retention generally showed distinct between the incubation substrates the incidence of females was higher than that of males in the sandy substrate. Even with a global trend of feminization of the hatchlings of turtles temperature-dependent sex, the sex ratio was balanced, since the incidence of males was higher in the clayey substrates. For remaining in specific areas throughout the development of the embryos nests are susceptible, and under the influence of various biotic and abiotic factors in the incubation period of the eggs, this being the most vulnerable and critical part of the life cycle of the species. Multiple interactions between consumers and their resources make it possible the occurrence of different relationships among species, and the competitive suppression among ants Nylanderia sp.1 and Solenopsis geminata, generated a positive effect on the hatching success of P. unifilis. As they are a group with hierarchical competitive system, ants usually do not share resources, and how different forms of interactions can occur simultaneously, the competitive suppression between them generated a positive effect on a hatching rate of the P. unifilis, through facilitation. The Yellow-Spotted Amazon River Turtle is the species of resident turtles more general in the basins where it occurs. These differences found in life history may be partly reflective of a plastic response also associated with the use of different habitats of nesting, which would result in increased resilience of populations P. unifilis extreme climatic events and associations with other organisms. An approach centering on nests will bring new perspectives to knowledge about biology, ecology and vulnerability of turtles in the face of environmental change in progress in the Amazon.
... In addition to favoring multiple paternity, sperm storage would allow for postcopulatory selection such as sperm competition and female cryptic choice (Stockley 1997;Jennions and Petrie 2000). The sperm of high quality males or more compatible males may then be used for several years while allowing the female to avoid the potential cost of remating caused by aggressive interactions (Evans 1961;Uller and Olsson 2008;Ernst and Lovich 2009;Liu et al. 2013). Furthermore, the temporal asynchrony between the mating and fertilization events allowed by long-termed sperm storage can be an advantage for female wood turtle, in particular, for those that may not nest on a yearly basis. ...
Article
Mating system characteristics are of great importance as they may influence male and female reproductive success and reproductive isolation. The wood turtle (Glyptemys insculpta) is a terrestrial freshwater species listed as endangered by the International Union for Conservation of Nature. Considering its conservation status and the paucity of information currently available on parentage relationship for the species, we performed a microsatellite analysis to study the mating system of wood turtles in the Shawinigan River (Québec). We sampled 38 clutches over two years (14 in 2006 and 24 in 2007), for a total of 248 offspring genotyped with seven microsatellite loci. The reconstructed genotypes of the fathers revealed that reproductive success in the sampled clutches varied greatly between males and are positively correlated with the number of mates and clutches sired. Frequency of multiple paternity was estimated at 37% through a consensus of three different estimation methods. Positive correlation was observed between the genetic diversity of clutches and the number of fathers. Repeat paternity, however, was observed in 88% of the clutches by the same female in successive years, which suggests either a frequent use of sperm storage, or re-mating with the same partner in successive years.