Chemo-Orientation Using Conspecific Chemical Cues in the Stripe-Necked Terrapin (Mauremys leprosa)

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Journal of Chemical Ecology [joec] pp1135-joec-481872 March 1, 2004 20:35 Style file version June 28th, 2002

Journal of Chemical Ecology, Vol. 30, No. 3, March 2004 (©C 2004)

CHEMO-ORIENTATION USING CONSPECIFIC CHEMICALCUES IN THE STRIPE-NECKED TERRAPIN

(Mauremys leprosa)

ALBERTO MUNOZ1,∗

1Departamento de Ciencias Ambientales, Facultad de Ciencias del MedioAmbiente, Universidad de Castilla—La Mancha. Avda. Carlos III s/n. E-45071

Toledo, Spain

(Received May 16, 2003; accepted October 30, 2003)

Abstract—Although chemical communication has been studied intensively inmany reptilian species, little attention has been paid to the role that chemi-cal signals play in aquatic reptiles, such as freshwater turtles. Here, I testedthe hypothesis that the stripe-necked terrapin (Mauremys leprosa), an abundantfreshwater turtle that inhabits the Iberian peninsula, is able to recognize chemi-cal cues from conspecifics in the water and to modify its behavior in response tosuch cues. I compared the time spent by adult males and adult females in cleanwater to the time spent in water that presumably contained their own odor, odorfrom other males, and odor from other females, both during and outside the ma-ting season. Results show that outside the mating season, both males and femalesavoid water that contains chemical cues from conspecifics of the opposite sex.During the mating season, male turtles clearly select water with chemical cuesfrom females. Moreover, males prefer to occupy water from their home contain-ers over clean water, and avoid water with chemical cues from other conspecificmales. Conversely, during the mating season, females prefer to occupy waterwith chemical cues from other females, but do not select water from their homecontainers or water from males. The evolution of chemical communication inturtles, its relation to sexual selection processes, and the implications for turtlebehavior are discussed.

Key Words—Chemical communication, chemo-orientation,Mauremys leprosa,pheromones, sexual selection, turtles.

∗To whom correspondence should be addressed. E-mail: [email protected]

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0098-0331/04/0300-0519/0C© 2004 Plenum Publishing Corporation

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INTRODUCTION

The study of chemical communication is recognized as an integral part of researchon reptilian social behavior (Mason, 1992). Although communication by chemicalcues has been known in Chelonian species for a long time (Neill, 1948; Legler,1960; Rose, 1970), little attention has been paid to the role that chemical signalsplay in turtle behavior in comparison to other groups of reptiles such as lizards(e.g., Alberts and Werner, 1993; Cooper, 1994; Arag´on et al., 2001; L´opez andMartın, 2002; Lopez et al., 2002) or snakes (e.g., Begun et al., 1988; Chiszar et al.,1990; LeMaster et al., 2001).

Chelonians have well-developed nasal olfactory and vomeronasal systems(Halpern, 1992; Hatanaka and Matsuzaki, 1993), and these functional chemosen-sory systems may be used for mediation of turtle behavior (Mason, 1992; Grahamet al., 1996; Quinn and Graves, 1998). In a variety of chelonians, behavioral re-sponses to chemical cues occur in diverse social contexts, including aggrega-tion, aggression, and sexual behavior (reviewed in Mason, 1992; Alberts et al.,1994; Graham et al., 1996; Quinn and Graves, 1998). For example, Rose (1970)suggested that chemicals play a role in aggressive encounters between male tor-toises and may be important in mediating courtship behavior. Eisner et al. (1977)showed that secretions from the axillary glands ofSternotherusmay serve a dualfunction. These secretions are involved in antipredator mechanisms, whereas dur-ing the mating season, the glandular contents serve as sex-recognition cues bywhich courting males discriminate females. Chemicals may also play an im-portant role in turtle homing behavior, home area recognition, and orientation(Grassman, 1993; Graham et al., 1996). Homing by using chemical cues fromconspecifics was demonstrated by Quinn and Graves (1998) in the painted tur-tle (Chrysemys picta). The results indicate thatC. picta discriminate betweenchemical cues from home ponds and other ponds. Moreover, the response ofmales and females to the factors mediating home pond recognition is sexuallydimorphic. FemaleC. picta, but not males preferred to occupy water from homeponds over water from other ponds that contained conspecifics. InTestudo her-manni, experimental elimination of olfactory function resulted in impaired homingability and a 60–70% reduction in reproductive behavior (Chelazzi and Delfino,1986).

Behavioral studies on chemical communication in freshwater turtles are par-ticularly scarce (see Mason, 1992), although chemical communication has beenshown to be widespread among aquatic organisms (Liley, 1982; Dodson et al.,1994; Aragon et al., 2000). Underwater, olfactory detection could be especiallyimportant when visual cues are limited. Most freshwater turtles have several spe-cialized glands in the skin, called Rathke’s glands, which secrete chemical compo-nents into the environment (Ehrenfeld and Ehrenfeld, 1973). Although the func-tion of these gland secretions remains unknown, and the substances are not well

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CHEMO-ORIENTATION USING CONSPECIFIC CHEMICAL CUES 521

characterized, they may serve as signals in social interactions, like chin glandsecretions of some terrestrial tortoises (Alberts et al., 1994). Moreover, in se-veral species of freshwater turtles, feces may serve, alone or in combination withglandular secretions, as a source of chemical components (Harless, 1979; Mason,1992).

The stripe-necked terrapin,Mauremys leprosa(Schweiger, 1812) is a riverineemydid turtle that inhabits the center and south of the Iberian Peninsula (Andreuand Lopez-Jurado, 1998). It seems that olfactory communication could be partic-ularly important in this species for many reasons: (1) It often inhabits quiet andtroubled waters (unpublished data), asM. caspica rivulatadoes (see Gasith andSidis, 1984), where dense vegetation and turbidity can make visual cues unreli-able, thus favoring chemical detection of conspecifics. (2) It possesses a pair ofinguinal Rathke’s glands (Loveridge and Williams, 1957; Ehrenfeld and Ehren-feld, 1973), whose secretions have an intense odor. (3) Sniff behavior is a frequentand conspicuous habit inM. leprosa, as in other turtle species (Ernst, 1971; Seigel,1980; Kramer and Fritz, 1989; Kaufmann, 1992). The mating system of the stripe-necked terrapin is not well characterized, but the mating season occurs in spring(unpublished data), as in most temperate-zone turtles (Moll, 1979). During sum-mer (July–August), activity ofM. leprosais particularly low because many creeksin central Spain dry up partially or completely.

Here, I report on a 2-year laboratory experiment that tested the hypothesisthat M. leprosais able to recognize chemical cues from conspecifics in water. Icompared time spent by male and female turtles in clean water vs. time spent inwater presumably containing their own odor, odor from other males, and odorfrom other females, both during and outside the mating season. Results showedthat preferences for different types of water vary between sexes and betweenseasons.

METHODS AND MATERIALS

Study Animals.I captured a total of 32 individuals ofMauremys leprosaduring two consecutive years of experimental study. In the first year (2001), exper-iments were carried out outside the mating season of the species. In July, once themating season had ended, I captured 16 turtles, eight adult males and eight adultfemales of similar size (Males: carapace lengthX ± SE= 150.4± 3.1 mm, range:132–160 mm; weightX ± SE= 386.2± 26.6 g, range: 240–460 g. Females: cara-pace lengthX ± SE= 180.9± 3.9 mm, range: 169–205 mm; weightX ± SE=762.5± 52.2 g, range: 610–1070 g). In the second year (2002), I carried outthe same experiments as in 2001, but in this case during the mating seasonof the species. Another 16 turtles, eight adult males and eight adult femalesof similar size, were captured in May, which coincided with the turtle mating

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season in their original natural populations (Males: carapace lengthX ± SE=156.5± 2.5 mm, range: 145–166 mm; weightX ± SE= 390.3± 27.2g, range:245–498 g. Females: carapace lengthX ± SE= 179.6± 5.2mm, range: 153–200 mm; weightX ± SE= 756.7± 50.3g, range: 608–1030 g).

To ensure that turtles had not been in previous contact, which might haveaffected the outcome of the experiments, in both years I captured them in severalcreeks over the same large area (more than 1000 km2) in the Toledo province(central Spain). Turtles were hand-captured or creel-captured using sardines asbait, under licence from the Consejer´ıa de Medio Ambiente de Toledo. They wereindividually housed in containers (60× 40× 20 cm) filled to a depth of 15 cm withwater, and located in outdoor conditions. They were fed twice per week with deadfish and chicken liver, and were held in their home-containers for at least 10 d sothat they would become familiarized with their new environment prior to testing.At the end of experiments, turtles had been in captivity for 30 d. All animals werehealthy during the trials and were released at the capture sites at the end of theexperiments.

Experimental Design.I conducted the experiments under outdoor conditionsusing experimental aquaria consisting of two plastic containers (73× 57× 17cm) joined by two ramps, which made it possible for a turtle to cross easily fromone container to the other. Each turtle was given the choice between two contain-ers that had been previously filled with water from different origins. I performedthree types of trials for each turtle; it was allowed to stay in (1) clean water vs.water from its own home-container, (2) clean water vs. water from one home-container of an individual of its own sex, and (3) clean water vs. water from onehome-container of an individual of the opposite sex. Water with chemical scents ofindividual turtles used in each test was taken from the home-containers in whicheach turtle had been maintained for 3 d. I filled home containers of the “odordonor turtles” with 20 l of clean water, and during these 3 d, other unoccupiedcontainers were filled with 20 l of clean water. Trials started at 1030 GMT whenwater (clean and stimulus) was poured into the experimental aquaria, and the ex-perimental turtles were located between the two ramps in a neutral position notbiased towards any container. Turtles were manipulated by using fresh gloves toavoid odor contamination. Aquaria were covered with pieces of opaque fabric,2 m in height, in order to avoid solar or visual cues that might affect orientationduring trials. I checked during each trial that the water temperature was similar inboth containers, and leveled the aquaria to control possible effects of positive geo-taxis (DeRosa and Taylor, 1980). I randomly chose which male or female was usedin each trial, and the side in which clean water was placed was also randomizedwithin a treatment. Each turtle participated in only 3 trials (clean vs. its own odor,clean vs. odor from another turtle of its own sex, and clean vs. odor from anotherturtle of the opposite sex). The three trials were spaced at least 6 d apart to avoid

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turtle-stress during the experiments. At the start of each trial, turtles typically ex-plored the two containers, frequently entering the water of one and changing tothe other, then remaining in one and occasionally changing to the other. Each triallasted 8 hr (from 1100 to 1900 GMT). I used the instantaneous scan samplingmethod; turtles were monitored every 20 min from a hidden point, recording theirlocation in the experimental aquaria. Thus, the locations observed on each of the24 scans were considered to be representative of a turtle’s use of space in theaquaria. In each scan, if a turtle was situated in either of the two containers, it wasdesignated as having chosen that container, whereas if it was located out of thewater (i.e., on the ramps), it was designated as having made no choice. At least tworecordings in each container within the first 2 hr were considered necessary for atrial to be valid, in order to ensure that individuals were exposed to both samplesof water. After each trial, the containers were drained and thoroughly rinsed withclean water and odorless soap to avoid odor contamination. At the end of trials,I determined the choice of a given turtle based on the time spent in each container(see Arag´on et al., 2000). I considered that an experimental turtle had chosenthe water placed in one of the two containers if it spent more than 60% of itstime (excluding time spent in the no-choice area) in that container, whereas if thepercentage of time spent in any container was between 40 and 60%, I consid-ered that the turtle had had no preference for either container. At the end of thetrials, each turtle was classified as having chosen the container filled with cleanwater, the container filled with stimulus water, or as having shown no preferencefor either container. To assess the preference of a group of turtles, I calculatedthe number out of the total that preferred a particular stimulus (i.e., spent greaterthan 60% of the time) and compared it to an expected binomial distribution, as-suming frequencies to be equiprobable on each side (for a similar procedure seeChivers et al., 1997; Arag´on et al., 2000). If the distribution of individuals that pre-ferred one container or the other deviated significantly from the expected binomialdistribution, that group was considered to have chosen one sample of water. Previ-ous analyses demonstrated that there are no preferences between two clean-watertests.

RESULTS

Results show that preferences for different types of water vary between sexesand between seasons. Table 1 shows the number of turtles that spent greater than60% of their time in either container for each treatment outside the mating season,and the correspondingP values from two-tailed Binomial tests. Outside the matingseason, both males and females significantly avoided water that contained chemicalsignals from individuals of the opposite sex, but they had no preferences for water

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TABLE 1. TIME SPENT BY MALES AND FEMALES OFM. LeprosaIN

CONTAINERSOUTSIDE THEMATING SEASON

Clean water vs.

Outside the mating season Own water Male water Female water

Malesa (clean/other) 2/6 6/2 8/0P value 0.289 0.289 0.008Femalesa (clean/other) 6/1 7/0 4/3P value 0.125 0.015 0.99

aThe number of turtles that spent>60% of their time in each container foreach treatment (clean water vs.: own water/water from a male/water from afemale), and the correspondingP values from two-tailed Binomial tests areindicated.

from their home-containers or water with chemical cues from individuals of thesame sex (Table 1). Table 2 shows the number of turtles that spent greater than 60%of their time in either container for each treatment during the mating season, and thecorrespondingP values from two-tailed Binomial tests. During the mating season,males responded actively to the different water types. They clearly selected waterwith chemical cues from female turtles (Table 2), but they preferred water from theirhome-container over clean water, and avoided water with chemical cues from othermales (Table 2). Conversely, females preferred water with chemical cues fromother females during the mating season, but did not choose water from their home-containers or water from males (Table 2). Figures 1 and 2 show differences inresponses to chemicals of both males and females during and outside the matingseason, highlighting the preference of males for female odors during the matingseason and the avoidance of such odors outside the mating season.

TABLE 2. TIME SPENT BY MALES AND FEMALES OFM. LeprosaIN

CONTAINERSDURING THE MATING SEASON

Clean water vs.

During the mating season Own water Male water Female water

Malesa (clean/other) 0/7 7/0 0/7P value 0.016 0.016 0.016Femalesa (clean/other) 4/4 3/3 0/6P value 0.99 0.99 0.031

aThe number of turtles that spent>60% of their time in each container foreach treatment (clean water vs.: own water/water from a male/water from afemale), and the correspondingP values from two-tailed Binomial tests, areindicated.

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FIG. 1. Comparison of the time percentage spent by males in the containers for each treat-ment (¤ clean water;¥ odor water) in the mating (M) and non-mating (N-M) seasons.Signed (*) treatments indicate trials in which turtles significantly chose one type of water.

DISCUSSION

Four functions of movements by turtles have been documented: feeding,mating activities, basking, and hibernation or hiding (Gibbons et al., 1990). Nu-merous environmental cues such as temperature, water current, visual cues, theearth’s magnetic field, or positive geotaxis have been implicated in the mediationof turtle movements and turtle orientation (Casteel, 1911; Sexton, 1959; Emlen,1969; DeRosa and Taylor, 1980; Yeomans, 1995; Lohmann et al., 1999). Chemicalcues from conspecifics may also play a role in the mediation of such movementsand behaviors, as indicated by this study. Outside the mating season, when ma-ting activities of freshwater turtles do not occur, access to different resources suchas food or basking sites may result in aggressive interactions between the sexes(Rovero et al., 1999). Avoidance of these kinds of interactions could be the reasonthat males and females tend to avoid water with chemical cues from individuals ofthe opposite sex outside the mating season. In other turtles, competition for foodbetween males and females has evolved sexual differences in head proportionspromoting niche divergence (Lindeman and Sharkey, 1999). InM. leprosa, there

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FIG. 2. Comparison of the time percentage spent by females in the containers for eachtreatment (¤ clean water;¥ odor water) in the mating (M) and non-mating (N-M) seasons.Signed (*) treatments indicate trials in which individuals significantly chose one type ofwater.

is no evidence that niche divergence or variation in head proportions occurs (un-published data). Thus, spatial segregation of the sexes could be a means wherebymales and females avoid competition for resources outside the mating season.

The results suggest that males ofM. leprosaare able to identify chemicalcues from females in the mating season. During courtship and mating, extensivemale sniffing and head bobbing have been reported in apparent response to femalegland secretions in a number of turtles, e.g.,Gopherus berlandieri, Geocheloneradiata, or Clemmys insculpta(Rose, 1970; Auffenberg, 1978; Kaufmann, 1992).MaleM. leprosaprobably use female scents to detect and locate prospective matesby chemotaxis when vision is limited. Berry and Shine (1980) suggest that mate-searching is important for freshwater male turtles, and that sexual size dimorphismin this group may have been selected for. Thus, small size may be favored in malesbecause it allows greater mobility and because so much of their available energyis devoted to searching for females rather than to growth (Berry and Shine, 1980).I have found that maleM. leprosaare smaller than females and that both theiractivity and mobility are higher than that of females during the mating season(unpublished data). The efficient location of sites that contain conspecific females

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saves the males time and energy, and probably reduces exposure to predatorsduring mate-searching (Magnhagen, 1991). In other groups, such as frogs or newts,chemical cues from conspecifics are used to assess whether potential mates arepresent (Wabnitz et al., 1999; Arag´on et al., 2000).

MaleM. leprosapreferred water from their home containers over clean water,and avoided water with chemical cues from other males during the mating season.This indicates that they were able to distinguish between their own odors and thoseof other males. Several studies have suggested that freshwater turtles have homeranges but are not territorial, and that home ranges of males show interindividualoverlapping but that fighting between them is frequent (Lebboroni and Chelazzi,1991; Kaufmann, 1992; Arvisais et al., 2002). High activity and mobility of malesduring the mating season and male–male competition for mates may increase theprobability of interaction. The ability to discriminate and avoid chemical stim-uli from other males, and to recognize their home area by their own odors mayminimize agonistic encounters (see Gosling, 1990; Arag´on et al., 2001).

The preference of females for water that contains chemical stimuli from otherfemales during the mating season could be responsible for a grouping strategy usedby them during reproduction. Gathering in certain areas would make it easier formales to find them, thus favoring the possibility of being fertilized by more thanone male. Several studies show the existence of both multiple paternity and spermcompetition in turtles (Galbraith et al., 1993; Valenzuela, 2000; Pearse et al.,2002). In evolutionary terms, it might be advantageous for female turtles to befertilized by several males, promoting sperm competition (Galbraith, 1993). Inthis experiment, females responded actively to the odors of other females, but theydid not to their own. This indicates that, similarly to the males, females were alsoable to discriminate between their own odors and those of other individuals of thesame sex.

In aquatic organisms, there is no evidence that chemical cues are used to sig-nal boundaries of territories. However, chemical communication could be used inclose-range interactions. Turtles with the ability to recognize and locate chemicalcues from conspecifics near them might have a selective advantage over turtles lack-ing such ability, because the ability to recognize and locate particular conspecificswithout physical contact could be energetically advantageous. Thus, communi-cation using conspecific chemicals may reduce time and energy costs for maleand femaleM. leprosa. Since the reproductive interests are different for male andfemale turtles, and since conflicting strategies may have evolved between sexes(Berry and Shine, 1980; Galbraith, 1993), it is expected that they would showsex-specific responses to chemicals from other conspecifics in the mating season.Murphy et al. (2001) have suggested that sex-specific behaviors ofSternotherusodoratuscould be due to sexual dimorphism in the transduction of chemosignalsin the vomeronasal organ. In any case, the evolution of chemical communica-tion in turtles and its implications for turtle behavior may have come from sexual

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selection processes (see Rose, 1970; Eisner et al., 1977), like sexual size dimor-phism (Berry and Shine 1980), and from other natural selection processes, such asfor niche divergence (Lindeman and Sharkey, 1999). I suggest that communicationusing chemical cues may have a greater importance in turtle spatial orientation andsexual behavior than previously considered.

Acknowledgments—I thank the Universidad de Castilla—La Mancha for use of their facilities,and the Consejer´ıa de Medio Ambiente de Toledo for permission to carry out the study. I am gratefulto Borja Nicolau for his assistance in capturing of turtles.

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Chemo-Orientation Using Conspecific Chemical Cues in the Stripe-Necked Terrapin (Mauremys leprosa)

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