Behavioral Ecology Advance Access originally published online on August 5, 2004
Behavioral Ecology 2005 16(1):188-195; doi:10.1093/beheco/arh150
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Do "sperm trading" simultaneous hermaphrodites always trade sperm?
Department of Evolutionary Biology, Institute of Animal Evolution and Ecology, University of Münster, Hüfferstr. 1, D-48149 Münster, Germany
Address correspondence to N. Anthes. E-mail: anthes{at}uni-muenster.de.
Received 31 January 2004; revised 9 June 2004; accepted 30 June 2004.
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ABSTRACT |
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Sperm trading can be a mechanism to solve the conflict over sex roles in hermaphrodites with copulation, sperm competition, and sperm digestion. If present, sperm donation depends on sperm receipt, resulting in conditional reciprocal inseminations. Conditional reciprocity can involve three traded commodities: penis intromissions on a yes-or-no basis, intromission durations (indicating ejaculate size), or sperm transfer. If present, animals that refuse to donate (cheaters) should be deserted by their partner or receive smaller ejaculates. We tested whether any of these commodities is traded in the simultaneously hermaphroditic sea slug, Chelidonura sandrana. Matings involve a stereotypic single sex role alternation. As a result, reciprocity was more frequent than expected under random mating, supporting trading of penis intromissions. Contrary to the predictions under trading of ejaculate sizes, intromission durations were not balanced between mating partners. To test trading of sperm transfer itself, we interrupted the sperm groove that transports sperm into the penis during copulation. Treated animals (experimental cheaters) could still copulate normally but could not transfer sperm. When paired to a cheater, sham-treated control animals did not respond to the absence of sperm receipt, neither by desertion nor by shortening intromission. We thus reject trading of insemination durations and sperm transfer in C. sandrana. Although trading of intromissions may be present, we discuss why reciprocity in this species may also be a by-product of the mutual willingness of both partners to donate as well as receive sperm, and not an indicator of sperm trading.
Key words: Chelidonura sandrana, conditional reciprocity, internal fertilization, mating behavior, opisthobranch, sexual conflict, sex role alternation.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Nonselfing simultaneous hermaphrodites are prone to develop conflicts over gender roles during mating as a result of unequal costs to reproduce through male and female function (Charnov, 1979
; Michiels, 1998). "Trading" sperm or eggs can resolve this conflict by enforcing reciprocal insemination. Egg trading was originally described for the black hamlet, Hypoplectrus nigricans, an externally fertilizing reef fish (Fischer, 1980). Here, mating partners repeatedly alternate donation of a small parcel of unfertilized eggs, which is then immediately fertilized by their mate, who subsequently assumes the female role. Because shedding sperm is cheaper than depositing eggs, partners exchange limited but accumulating opportunities to be male for as long as the cooperation lasts (Fischer, 1980, 1984, 1987; Petersen, 1995; Sella, 1985, 1988; Sella et al., 1997). Trading of male gametes (sperm trading) was first described in an internal fertilizer, the opisthobranch sea slug, Navanax inermis. In Navanax, mating partners alternate sperm donation repeatedly during a single mating encounter (Leonard and Lukowiak, 1984, 1985). The investigators suggested that sperm trading is driven by a preference for the female role. By donating small sperm amounts, the partner is encouraged to reciprocate. If it does, further role alternations may follow. Although this is the pattern expected for special cases such as sperm-dependent parthenogens (Michiels and Kuhl, 2003), its presence in outcrossing sexual species remains controversial. Recent theoretical and empirical studies suggest that in most internal fertilizers, sperm trading serves male rather than female interests (Greeff and Michiels, 1999; Michiels et al., 2003). As an important difference with egg trading, in which fertilizations are traded, internally fertilizing sperm traders have only limited control over the fate of their sperm in their partner. This lack of control over fertilization implies that resources (e.g., through sperm digestion), not fertilization opportunities, are the driving force behind sperm trading (see Angeloni, 2003; Pongratz and Michiels, 2003).
A key characteristic of sperm trading is that partners should only donate sperm when there is a high likelihood of receiving some. Otherwise, they should refuse sperm donation. Sperm exchange must therefore be conditional. Whether sperm donation is really conditional on sperm receipt, however, has not yet been shown in species with single or multiple sex role alternation. Observational and experimental data from opisthobranch sea slugs suggest that reciprocal sperm exchange indeed serves to balance sperm donation and sperm receipt (Angeloni, 2003; Karlsson and Haase, 2002; Michiels et al., 2003). However, the presence of reciprocal insemination patterns per se does not prove trading. Simultaneous or alternating reciprocity as well as balanced sperm amounts may also arise because both mating partners are willing to donate sperm and do not object to receiving sperm in an unconditional fashion (Landolfa, 2002; Puurtinen and Kaitala, 2002). Other costly traits such as predation risk may also be involved, but they do not reflect a trading system. Trading implies that each partner has something to offer that the other does not have. In the case of sperm trading, this is the access to unfertilized eggs and the nutritional value of sperm.
Three commodities with increasing complexity may serve to enforce the conditional exchange of sperm: (1) the act of penis intromission, (2) intromission duration as an indirect indicator of transferred sperm amounts, or (3) effective sperm transfer. Trading of penis intromissions occurs when sperm donation depends on sperm receipt in an all-or-nothing pattern, irrespective of ejaculate size (Michiels and Streng, 1998). It predicts that most matings either involve reciprocal insemination or no insemination in either direction, whereas unilateral insemination is rare. When the mating pattern does not differ from the random expectation, intromissions are considered nonconditional (Michiels and Bakovski, 2000; Michiels and Kuhl, 2003). In a more advanced trading system, animals should also trade the amount of sperm (Baur et al., 1998; Vreys and Michiels, 1998). Sperm amounts can be balanced either by using intromission duration as an honest indicator of insemination duration or by directly measuring the amount of sperm transferred. In both cases, individuals give more sperm when receiving more, but also give less when receiving less. Hence, to result in true trading, all three commodities require a specific response to cheaters, that is, a "punishment" of animals that do not cooperate as expected. Cheaters should either be deserted without copulation, or receive fewer sperm. This also indicates that sperm trading is only possible when abandoning a partner represents a small cost measured in lost mating opportunities, for example, when mate encounters are frequent. At lower densities, and hence lower mating rates, individuals are known to mate more indiscriminately (Michiels and Bakovski, 2000; Michiels et al. 2003).
We first describe the mating behavior of a new study species. The sea slug Chelidonura sandrana belongs to the same family as Navanax inermis, in which sperm trading was first described (Leonard and Lukowiak, 1984; Michiels et al. 2003). Because of the presence of dense mating aggregations, sperm storage, and a sperm digesting bursa copulatrix, sperm trading is expected (Leonard, 1991; Michiels and Bakovski, 2000). We first describe reciprocity patterns and test whether penis intromissions or intromission durations are a traded commodity. In the second part, we produced cheaters by disabling sperm donation in one set of animals, and we compare the response of their mating partner with that of individuals mated with sham-treated controls. This experiment was designed to test whether sperm itself serves as the traded commodity, and whether the absence of sperm donation (cheating) reduces the willingness to reciprocate. Hence, for the first time, we directly manipulated sperm donation in a hermaphrodite without affecting its general mating behavior in order to verify or falsify the sperm trading hypothesis.
Study species
Chelidonura sandrana Rudman, 1973 belongs to the family Aglajidae (Opisthobranchia, Cephalaspidea). This group of opisthobranch sea slugs is characterized by a monaulic hermaphroditic system (Ghiselin, 1965); that is, autosperm, allosperm, and eggs all pass through the same duct when entering or leaving the reproductive system. All aglajids possess both a gametolytic sac (bursa copulatrix), which is used for sperm digestion in other gastropods (Beeman, 1970; Baur, 1998), and a sperm storage organ (receptaculum seminis; Klussmann-Kolb, 2001; Rudman, 1974). As most other opisthobranchs, aglajids are nonselfing (Baur, 1998). Importantly, male and female copulatory organs are spatially separated. The common genital aperture with the female genital opening (FGO) is located at the right lateroposterior mantle cavity and is covered by the posterior mantle and the right parapod when not mating. An external sperm groove leads from the genital opening along the right side of the animal to the penial papilla on the right front of the head (Beeman, 1977). The groove, a ciliated tissue fold, remains open to the tip of the penial papilla (Rudman, 1974), which we shall call penis hereafter. In C. sandrana the penis is comparably large and structured (Figure 1a). During copulation, it is twisted into the FGO (Figure 1b). Sexually mature C. sandrana have a total body length of 10.2 ± 2.77 mm (4–21 mm, n = 127).
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METHODS |
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Sampling and maintenance
Chelidonura sandrana (black color morph, occasionally with orange and white spots) were collected with plastic pipettes on sandy bottoms from 0.5–9 m depth around Lizard Island (Great Barrier Reef, Cairns Section, Australia) in January and February 2003 and January 2004. Animals were immediately isolated and kept in 75-ml plastic vials under constant water temperature (26°C), and natural day length without direct exposure to the sun. Water was exchanged once per day. Observations and experiments took place within 48 h after collection. After the experiments, individuals were released at the place of collection. Field and laboratory work were conducted in accordance with the Great Barrier Reef Marine Park Authority (GBRMPA) permit G02/2868.1 to N.A.
Mating behavior observations
An initial series of five single observations was used to create a qualitative description and ethogram of the mating behavior. Quantitative data were collected during a single observation session of 18 freshly collected pairs (23–27 January 2003). Partners were matched for size in order to avoid additional variance caused by size differences within pairs (see Angeloni and Bradbury, 1999; Angeloni et al., 2002, 2003; Otsuka et al., 1980; Peters and Michiels, 1996; Switzer-Dunlap et al., 1984; Yusa, 1996). Pairs were placed in a watch glass (32 mm Ø, maximum depth = 5 mm) and observed under a stereomicroscope. Observations were stopped after a successful mating sequence, that is, both slugs had fully separated after a copulation and reached opposite sides of the observation vial, or when no mating attempt took place within 30 min. For each mating we recorded and exactly timed the following behavioral patterns: first body contact type (head-to-head, head-to-side, head-to-tail), behavioral patterns prior to copulation (penis eversion, probing with penis on FGO, unfolding parapod), penis intromission (penis fully inserted into FGO), insemination duration (where visible), body movements during copulation including gliding, penis retraction, and behavioral patterns between subsequent intromissions during the same mating sequence. Only one pair was observed at a time in order to time behavioral patterns precisely.
Intromission and insemination duration
If intromission durations serve as a commodity for sperm trading, they must be a reliable indicator of insemination duration. In previous studies with Navanax inermis, penis intromission duration was used as an estimate of sperm transfer (Michiels et al., 2003), although this correlation was not demonstrated. Sperm donation is correlated with copulation duration in the sea hare Aplysia parvula (Yusa, 1994), but this is not the case in the spermatophore-donating land snail Arianta arbustorum (Baur et al., 1998). Because sperm transfer in C. sandrana can occasionally be observed without disturbing the mating animals, we checked whether intromission durations are a reliable predictor of insemination durations.
Trading of penis intromissions and intromission durations
For this analysis we combined data from the mating behavior observations (n = 18) with the sham-treated NxN pairs from the sperm transfer experiment (n = 51, see below) to increase sample size. Both groups did not differ in their frequencies of null, unilateral and reciprocal matings (likelihood ratio test, 
2 = 4.08, n = 69 pairs, Exact p = .164). Intromissions tended to last longer in the mating behavior observations (t test t = –1.78, df = 101, p = .077), but pooling the data did not affect the results presented here. To test if penis intromissions are traded, we compared observed numbers of intromissions within a pair with the expected random distribution of intromissions over all observed pairs by using a Poisson distribution. To test trading of intromission durations, we checked whether the second sperm donor adjusted its insemination duration to the insemination duration received from its partner during the first copulation. This implies a positive correlation between first and second intromission duration in pairs with a single sex role alternation. As body size varied strongly between pairs, we first checked for the effect of body size on intromission durations.
Trading of sperm transfer
To test if animals use effective sperm receipt and not simply penis intromission to decide on later sperm donation, we produced individuals that were incapable of donating sperm (cheaters). In these treatment animals (T), we interrupted the sperm groove. Treatment animals were relaxed in a 7 % MgCl2 solution (freshwater/seawater ratio = 1:1) for 30 min and gently dried with soft paper tissue. We unfolded the right parapod to expose the sperm groove. By using a thin hot needle, we cauterized it at the connection of cephalic and posterior shield under a stereo-microscope. Animals were allowed to recover for 24 h. This treatment disables sperm transfer to the penis. During copulation sperm are now discharged into the water through the (open) sperm groove just before the point of cauterization. Control animals (N) received a sham treatment by cauterizing the skin of the inner right parapod beneath the sperm groove. As indicated above, the number of sex role alternations and intromission durations did not differ significantly between sham-treated (NxN) and nontreated pairs, suggesting that the treatment procedure did not alter the general mating behavior of C. sandrana. Pairs were assembled in size-assorted treatment pairs (NxT and TxN; n = 98 pairs) and sham-treated control pairs (NxN, n = 51 pairs) in January 2004. Observations were blind for treatment, and pairs were randomly assigned with respect to body size and treatment to two observers. We registered the same variables as in the mating behavior observations.
To assess the response to cheating we compared reciprocating NxN pairs with pairs that contained one cheater (T). Mating order in pairs with a cheater was not predetermined but depended on the animals themselves. It could thus only be defined a posteriori for treatment pairs with at least a single copulation (n = 90 pairs). Pairs in which the treatment individual was the first "male" will be referred to as TxN pairs (n = 46 pairs), whereas the treatment individual was second "male" in NxT pairs (n = 44 pairs). Trading of sperm transfer predicts that sham-treated control individuals in TxN pairs should respond to their cheating partner either by deserting or by reducing their own subsequent intromission duration. For the former, we tested whether cheating increased the likelihood of the partner deserting after the first intromission. For the latter we measured second male response to cheating as the difference between second and first penis intromission duration in reciprocating pairs. Being the second "male" in the TxN-group, a treatment individual should reduce its intromission time (negative response value). Being second "female" in the NxT group the control individual should either prolong copulation, while waiting for sperm receipt, or shorten copulation, because it detects the failing insemination attempt of its treated partner.
Statistical analysis
For comparisons between pairs (e.g., penis, intromission duration and body size), we used average values of both partners to avoid pseudoreplication. Because of a skewed distribution intromission and insemination durations were log-transformed for parametric statistical tests. Values are given as mean ± SD where possible. Differences between treatment groups were tested by using one-way ANOVA. Box-plots show median (bold lines), interquartile range (gray boxes), range (flags), outliers (circles), and extremes (asterisks). Standard statistical analysis was performed by using SPSS 11.0 statistical package.
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RESULTS |
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Mating behavior of C. sandrana
Out of 18 pairs, 13 mated (73 %). Of these, 10 (77%) changed sex roles exactly once. The remaining pairs mated unilaterally (n = 2) or changed sex roles twice (n = 1). A typical mating sequence consisted of the following phases (Figure 2; Table 1).
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Contact
Animals find partners accidentally rather than through active searching. Mucus-trail following, as known from other opisthobranchs under both field and laboratory conditions, was not observed. The type of first contact did not determine the likelihood of a mating sequence starting (Figure 2a).
Intertwining
Both partners glide clockwise around each other in a "yin-yang" position (Figure 2b). Each has its penis everted and probes the FGO of the other. Nine of 13 mating sequences were preceded by this behavior. Intertwining is terminated when one partner leaves the circle and accepts the female mating role. Sometimes intertwining is resumed, but eventually always leads to successful copulation.
Attaining the mating position
Copulation occurs invariably in a tail-gaiting position, in which the anterior animal assumes the female role and the posterior animal the male role. Simultaneously reciprocal intromissions were not observed, although they appear physically possible. Before intromission the female-acting partner slightly unfolds the posterior part of its right parapod to expose the swollen, balloon-shaped FGO (Figure 2c). This "inviting" behavior suggests female receptiveness. Before intromission, the FGO shows pulsating movements of unknown function. The "male" partner probed the FGO with its penis before attaining intromission in 22 out of all 25 intromissions in 13 copulating pairs (Figure 2d).
Penis intromission
Sperm transfer was often visible. Orange-colored sperm strains were transferred in regular intervals of approximately 5–10 s from the common genital aperture through the ciliated sperm groove into the penial papilla (Figure 2e). Sperm were not stored in the penis but immediately transferred into the partner's FGO. Intromission duration did not differ between first (10.3 ± 2.9 min) and second intromission (10.3 ± 4.9 min) in reciprocating pairs (paired t test t = 0.34, df = 9, p = .73). Female acting partners started gliding while being inseminated in 13 cases (54 %) shortly after the start of intromission. In such cases the "male" follows while maintaining penis insertion. Pairs always stop gliding before sex role alternation after the first intromission. Female gliding occurred in similar frequencies during first or second intromissions (Fishers Exact test, n = 24, exact p = .44). The pattern of sperm transfer did not differ between gliding pairs and motionless pairs. Likewise, intromission duration did not differ between gliding (10.4 ± 5.7 min) and nongliding pairs (10.7 ± 4.7 min; t test t11,13 = –0.29, p = .77).
Retraction
First indications for the approaching end of intromission are occasionally visible about 3 min before retraction: the "male" starts to move and retracts its head to initiate penis retraction, often stretching the penial papilla to some extent. Females do not show obvious movements that suggest female termination of intromission. Hence, penis retraction may represent a "male decision." With a final strong pull, the penis is released and immediately retracted into the body cavity.
Sex role alternation
Immediately after the first intromission, mating partners show a stereotypic behavioral sequence that initiates sex role alternation (Figure 2f). The former "female" turns its head to the right, the former "male" to the left in order to accomplish the reversed position. Only in two out of 13 mating pairs, did both partners turn to the right after the initial copulation ended but nevertheless eventually changed copulatory position successfully. Two unsuccessful role changes were preceded by the standard behavioral sequence, but partners failed to remain in contact and appeared to have lost each other. Even when the previous "female," now "male," failed to find its partner, the previous "male," now "female," usually waited motionless for several minutes, presumably for its partner to approach. After sex role alternation, the next intromission starts immediately (Figure 2g). Only in one out of 11 cases did partners go through the intertwining position after the first intromission. The second intromission is not different from the first one.
Gliding away
After the second penis withdrawal, partners glided away without any further mating attempt. Only in one instance did a second probing and brief intromission (4 min) by the first "male" occur.
Intromission and insemination duration
Penis intromission consists of three distinct phases: preinsemination, insemination, and postinsemination, respectively (Figure 3). Only during insemination are sperm strains transferred in regular intervals. The duration of the preinsemination and postinsemination phases was observed for 21 (preinsemination only), 17 (postinsemination only), and 14 (both) penis intromissions (Table 1). Both preinsemination and postinsemination durations contributed significantly to the variation in total penis intromission duration (Figure 4a). Insemination duration increased with penis intromission durations (Figure 4b), indicating that intromission duration can be used as a good predictor of insemination duration.
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Trading of penis intromissions and intromission durations
Across nonmanipulated pairs, the number of sex role alternations differed significantly from a random (Poisson) distribution (Figure 5). Reciprocal matings with one sex role alternation were overrepresented, whereas other types occurred less frequently than expected. It suggests, but does not prove, that penis intromissions may be traded.
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In reciprocating, nonmanipulated pairs with single sex role reversal, mean intromission duration per pair was independent of mean body size per pair (rP = –.001, n =44, p = .99). First and second intromission duration did not differ significantly (paired t test t = 1.14, df = 43, p = .26). But there was no within-pair correlation between the duration of first and second intromissions (rP = –.086, n = 44, p = .578). This indicates a lot of variation within pairs, with no asymmetry between first and second inseminations. Combined, these data suggest that intromission durations are not traded in C. sandrana.
Trading of sperm transfer
After sperm groove manipulation sperm transfer could be confirmed in all sham-treated individuals, whereas all treated slugs released sperm in the water before the point of cauterization. Contrary to the expectations, "cheated" individuals did not hesitate to transfer sperm: All sham-treated animals donated sperm to their "cheating" treatment partners. More importantly, cheating did not increase the likelihood of a treatment individual being deserted in the TxN group (Figure 6). The likelihood of desertion was also independent of the first penis intromission duration (binary logistic-regression, all p > .17 in the NxN, NxT, and TxN group with n = 46, 44, and 46, respectively). Cheated animals did not reduce or prolong intromission durations as predicted as a response to cheating in the NxT and TxN pairs (Figure 7).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In C. sandrana reciprocity is characterized by a stereotypic pattern of a single sex role alternation. Unilateral or repeated inseminations are possible but are avoided behaviorally. Sex role alternation consists of three major elements: turning around to reach the reversed mating position, waiting for the partner to assume intromission, and second intromission without conflict over reversed roles. As a result, reciprocal copulations are significantly more frequent than expected by chance, suggesting conditional reciprocity (Michiels and Bakovski, 2000
). This is the first description of such a strict alternating mating system for an opisthobranch sea slug. Comparable mating sequences are known from the pulmonate land snails Partula suturalis, P. taeniata (Lipton and Murray, 1979), and the fresh water snail Stagnicola elodes (Rudolph, 1979). In contrast to C. sandrana, however, each intromission in Partula is preceded by full courtship and hence has to be considered a separate mating sequence. In Stagnicola single sequential reciprocation is stereotypic (Rudolph, 1979), as in C. sandrana. The pond snail Lymnaea stagnalis also occasionally alternates sex roles (van Duivenboden and Ter Maat, 1988). In contrast to Chelidonura, however, matings are predominantly unilateral, and reciprocal matings only occur after isolation in the laboratory and not in the field. Despite the presence of all classic elements of a sperm trading system, especially a high rate of reciprocity, we could not confirm that sperm exchange is conditional in C. sandrana. Neither were intromission durations of mating partners correlated, nor did animals reduce intromission duration when they received no allosperm during intromission from a cheating partner. This suggests that neither penis intromission durations nor the presence of sperm transfer serve as a commodity for trading in this species. As intromission durations are tightly linked with insemination durations, we also conclude that insemination durations are not traded. It remains to be shown, however, how insemination duration translates into sperm amounts. Regular transfer of equally sized sperm strains in all animals in which sperm transfer was observed indicates a linear correlation.
Irrespective of the exact relationship of intromission durations and sperm amounts, the missing response to the absence of sperm receipt in the cauterization trial is a strong indication that sperm is not the commodity for trading in C. sandrana and raises doubts whether there is trading at all. Our results can be interpreted in two ways: First, commodities other than sperm receipt and penis intromission durations may maintain this trading system. The high level of reciprocity in the present study is in line with a trading system based on the act of intromission only. Intromissions could serve as an honest indicator of insemination, as we never observed penis intromissions without sperm transfer. However, as in previous studies, this pattern cannot prove that reciprocal matings are conditional. Reciprocity can also arise whenever both individuals are generally prepared to donate and receive sperm. Copulations would then implicitly reflect a mutual willingness to act in both sexual functions (Puurtinen and Kaitala, 2002), but without desertion of a cheating partner. This maintains reciprocity, which may appear conditional without being so. It may evolve when both sex roles offer a net fitness pay-off for their reproductive investment, eliminating the need for trading (see Leonard, 1990). This is in line with anecdotal observations showing that C. sandrana can copulate almost unlimited (up to nine times in short succession) in either male or female function (data not shown).
Landolfa (2002) suggested an additional explanation for sex role alterations in hermaphrodites. He predicted that conventional sexual signaling indicating phenotypic viability and/or sexual attractiveness could result in apparent "trading" patterns without conditionality of gamete exchange. This is because both mating partners intend to send and receive sexual signals, and are mutually attracted to donate and receive sperm. For internal fertilizers he predicts that sperm amount serves as the sexual signal. This is apparently not the case in C. sandrana, in which sperm donation did not affect the partners' mating decisions. Hence, similar to sperm trading theory, sexual signaling cannot satisfactorily explain the mating behavior shown by C. sandrana.
Conclusion
On a behavioral basis, our data are in line with the prediction that the simultaneously hermaphroditic sea slug C. sandrana has a sperm trading system in which the number of penis intromissions is the traded commodity. However, we did not find decreased rates of sex role alterations after being cheated or a reduction in sperm donation to cheaters who mated normally but were prevented from transferring sperm. This suggests that C. sandrana does not trade sperm and may not even insist on reciprocation. Sperm trading may therefore not occur in all cases in which it is suspected on a purely behavioral basis. Hence, further studies clearly separating behavioral patterns and the underlying copulatory mechanisms are necessary to clearly contrast sperm trading and nonconditional reciprocity. In this context cephalaspid sea slugs such as C. sandrana offer the unique opportunity to manipulate the male function without influencing male mating behavior (cf. de Visser et al., 1994).
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ACKNOWLEDGEMENTS |
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We thank Shireen Fahey and Annika Putz for their enthusiastic assistance during fieldwork, and our hosts at Lizard Island Research Station, Anne Hoggett, Lyle Vail, and Marianne and Lance Pearce, for their steady support and the pleasant working conditions. Comments by Anders Berglund, Gilianne Brodie, Thomas G. D'Souza, Shireen Fahey, Anne Houde, Joris M. Koene, Peter Sandner, Lukas Schärer, Hinrich Schulenburg, Claus-Peter Stelzer, Heike Wägele, and three anonymous referees improved previous drafts of the manuscript. Martina Fasel did an excellent job drawing mating slugs and penial structures. This study was funded by a grant from the German Science Foundation (DFG) to N.K.M. (DFG Mi 482/7–2). The German Academic Exchange Service (DAAD) additionally supported one field trip (grant D/02/28302 to N.A.).
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