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1 Georgia State University, Department of Biology, P.O. Box 4010, Atlanta, Georgia 30302
2 Lehrstuhl für Zoologie, TU München, Lichtenbergstr. 4, 85747 Garching, Germany
* To whom correspondence should be addressed. E-mail: biojhh{at}panther.gsu.edu
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Abstract |
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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The still rather small interaction distance of less than 1 cm in agonistic encounters between two snapping shrimp also favors the exchange of chemical signals between the opponents. The literature on chemical orientation and communication in snapping shrimp is limited: Hazlett and Winn (1962) tested aggressive and defensive responses of Synalpheus hemphilli to crushed male or female extract, and Schein (1975) and Hughes (1996) investigated the choice of Alpheus heterochaelis toward extracts of male or female water in Y-maze experiments without clear-cut results. On the other hand, ablation of the chemosensitive antennules in Alpheus edwardsii strongly reduced pair formation and sex recognition, which may be due to impeded distant or contact chemoreception since the pairing frequency remained high when only the antennae were ablated (Jeng, 1994).
The importance of olfactory signals during hierarchy formation was shown in male American lobsters (Karavanich and Atema, 1998a). In these experiments, the recognition of urine-carried chemical signals, which were received by the antennules, allowed the subordinate animal to avoid the familiar dominant shrimp, and therefore reduced the duration and aggression of fights. The exchange of chemical signals is also assumed to play a major role in individual recognition and memory in male and female Homarus americanus (Karavanich and Atema, 1998b; Berkey and Atema, 1999). In lobsters, urine is released through a paired set of nephropores on the ventral sides of the basal segments of the second antennae (Parry, 1960). Agonistic behavior in lobsters causes an increase in the probability and volume of urine release (Breithaupt et al., 1999). The released urine is then carried by the powerful anteriorly directed gill currents and may therefore transfer chemical information from one animal to another (Atema, 1985). In recent studies (Zulandt Schneider et al., 1999; Zulandt Schneider and Moore, 2000), chemical cues were also described as an important source for recognition of the dominance status or stress condition of conspecifics in another crustacean, the red swamp crayfish (Procambarus clarkii).
In light of these examples, a similar mechanism of chemical signal exchange via gill currents in snapping shrimp seems likely. We cannot, however, exclude the possibility that the animals also exchange hydrodynamic signals. In fact, it has been shown that the antennules of crayfish (Mellon, 1996) and lobsters (Guenther and Atema, 1998; Weaver and Atema, 1998) are equipped with both chemical and mechanosensory receptors, and detailed morphological studies of antennule sensory hairs favor the same situation in snapping shrimp (Schmitz, unpubl. obs.). Therefore, snapping shrimp may also perceive hydrodynamic stimuli as well as chemical stimuli with their antennules. Previous studies (Herberholz and Schmitz, 1998, 1999) have shown that the transfer of hydrodynamic signals is realized by the powerful water jet that is formed by rapid closure of the large claw. In contrast, the much weaker gill currents appear to be more suitable for transferring chemical information.
Suspended plastic particles were successfully used to visualize and quantify biological flow fields in lobsters and crayfish in a series of experiments by Breithaupt and Ayers (1996, 1998). Small floating particles of the same density as seawater were added to the aquarium water and illuminated in a horizontal or vertical plane in the vicinity of a tethered animal. Flow fields were then analyzed by tracking individual particles. It was shown that both lobsters and crayfish produce a great variety of flow fields by using the exopodites of the maxillipeds and by fanning the pleopods. The latter was also discussed with respect to chemical communication: male American lobsters commonly fan their pleopods at the second entrance of their shelter, thus creating a strong current that may contain chemical information about the female positioned at the first entrance (Atema, 1985, 1988). The pleopod fanning frequencies in males correlate with the frequencies of females checking the shelter. The existence of pheromones that control female choice and molting as well as male aggression was therefore assumed (Cowan and Atema, 1990; Atema, 1995; Bushman and Atema, 1997).
The possible exchange and use of different water currents during agonistic encounters has rarely been studied; but see Rohleder and Breithaupt (2000) for a preliminary study in the crayfish Astacus leptodactylus. To test the possibility that snapping shrimp use guided water currents as signals, we visualized and analyzed all water currents that the shrimp produced during their encounters with conspecifics of the same or different sex and in encounters with sympatrically living mud flat crabs (Eurypanopeus depressus).
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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–28; temperature: 22°–23°C). Proteins were removed from the water, and pH, carbonate, oxygen, CO2, and NO3 were regularly controlled. The shrimp were exposed to an illumination cycle of 12 h light/12 h dark and fed frozen shrimp, fish, or mussels three times a week. For visualization of the different water currents, we prepared the aquarium water (temperature: 22°–24°C, water level: 5 cm) with small, floating plastic particles (ABS-particles, Bayer, Leverkusen, diameter: 500–710 µm; specific weight: 1.03 kg/l). The aquarium (30 x 24 x 24 cm; floor covered with black cloth to facilitate walking) was positioned on a platform isolated from vibrations (Breithaupt et al., 1995). At the level of the interacting animals, the seawater was illuminated from one side by a slide projector holding a slide with a thin horizontal slit. Before each experiment fresh seawater and particles were added, and two animals (two snapping shrimp or one snapping shrimp and a crab) were placed in the aquarium for 10 min for acclimatization; the animals were separated by an opaque divider to prevent visual, tactile, and directed-chemical contact. After the partition was removed, all interactions between the animals during the following 20 min were videotaped from above (camera: Panasonic AG 455; video recorder: Panasonic AG 7355; monitor: Sony Trinitron). The reflexive characteristics of the suspended particles then allowed a precise tracking using standard video-frame analysis.
Each experiment (interactions between two snapping shrimp of the same or different sex or between a snapping shrimp and a crab) was characterized by the number of physical contacts between the opponents, regardless of their duration and strength, as well as by the number of water jets. Three different water currents were characterized, including a lateral gill current, an anterior gill current, and a pleopod current (Fig. 1a). The pleopod current was measured only when the shrimp was not in locomotion, because this current is also likely to be used in supporting the animal’s walking. Moreover, no current was included in our analysis unless the single-frame video analysis gave clear evidence that it had moved two or more plastic particles. The following parameters were evaluated for all visualized water currents: frequency, duration (time between onset of movement of the first floating particle and end of movement of the last particle), range (total distance covered by an identified particle due to a certain current; possibly underestimated when the current hit an opponent or an aquarium wall), velocity and target of the currents, their potential to transfer chemical information (i.e., entering the area of chemical perception at the receiver’s side), the temporal correlation between currents and previous physical contacts, and the correlation between produced currents and water jets in winners and losers during intrasexual interactions. To determine a winner or loser, we counted the number of aggressive acts and the number of submissive acts after each physical contact between the conspecific opponents throughout the encounter. Aggressive acts include behaviors such as approach, aggressive stance, and grasping and opening of the claws. Submissive acts include moving backwards and turning and tail flipping away from the opponent. These definitions are largely adopted from Nolan and Salmon (1970). In 11 out of 12 experiments, one animal produced more aggressive acts and fewer submissive ones than its opponent and was therefore determined to be the winner while the opponent was determined to be the loser.
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Results |
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General characteristics of released water currents
Encounters between two snapping shrimp of different sex (hetero) are characterized by a significantly higher number of physical contacts (23.9 ± 8.3, n = 287; P < 0.01) than seen in encounters between two shrimp of the same sex (homo; 13.8 ± 6, n = 165), or between a snapping shrimp and a crab (Eurypanopeus depressus) (interspecific; 12.7 ± 5.3, n = 157). On the other hand, snapping (water jet production) of the tested shrimp is significantly increased after a contact with a crab (38% ± 16%; P < 0.01) when compared to snapping after hetero and homo contacts (5% ± 4% and 11% ± 11%, respectively).
These differences in mind, we first evaluated the number of water currents (lateral gill currents, anterior gill currents, and pleopod currents) in each experiment. Figure 2 shows that there are no essential differences between interaction types (homo, hetero, or interspecific). Within each interaction type, however, the number of lateral gill currents significantly (P < 0.01) exceeds that of anterior gill currents as well as that of pleopod currents. In addition, in interspecific encounters with a crab, the frequency of anterior gill currents is significantly lower than the frequency of pleopod currents (P < 0.01).
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The velocity of the water currents during the first 120 ms (6 video frames) was evaluated for 10 examples for each current and interaction type (Fig. 3C). There are no significant differences in the velocities within and between different types of interactions. The lateral gill current shows the slowest velocities in all encounters. The anterior gill current and the pleopod current show similar values and are both more powerful than the lateral gill current. Initial velocities are higher, but their analysis has not proved satisfactory because of the standard video time resolution of 20 ms (50 frame/s).
Temporal relation of water currents to physical contact
Figure 4 compares the frequency of water currents that were elicited within 10 s after a physical contact between the opponents with those that were "spontaneously" produced—that is, emitted more than 10 s after a preceding contact. As shown in Figure 4A, in all interaction types the lateral gill current is significantly more often produced spontaneously than following a physical contact (P < 0.01). In homo interactions it occurs in only 6.2% of all cases (n = 10 of 162) shortly after a contact. During hetero interactions this current is elicited by a contact in 11.5% of all cases (n = 21 of 183); in interactions with a crab, the lateral gill currents occur within 10 s after a contact in only 8.5% of all cases (n = 13 of 153).
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In contrast, the pleopod current, like the lateral gill current, is significantly more often (P < 0.01) produced without an immediately preceding contact in all types of interactions (Fig. 4C). During homo interactions we observed only 7.7% of pleopod currents within 10 s after the last contact (n = 4 of 52). In hetero interactions this current is elicited in 16.7% of all cases (n = 8 of 48) by a preceding contact, and in interspecific interactions there are 13.0% of pleopod currents shortly after a previous contact (n = 7 of 54).
Possible chemosensory information transfer by water currents
If any of the water currents were used to transfer chemical information, one would expect them to be directed toward the chemoreceptive antennules of the opponent. We therefore evaluated the number of currents that reached the area between the opponents’ claws—that is, an area mostly covered by the flicking antennules. This was possible by analyzing the video sequences and identifying the area of particle dispersion with respect to the animals’ position. In fact, only the anterior gill current seems qualified to fulfill the function of possible information transfer (Fig. 5).
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In comparison, a higher percentage of anterior gill currents reaches the antennule area in all interaction types (Fig. 5B). During homo interactions the anteriorly projected gill current reaches the antennules of the opponent in 35.7% of all cases (n = 10 of 28). In hetero interactions the percentage (66.7%, n = 16 of 24) of anterior gill currents directed toward the antennules is even higher than that of undirected anterior gill currents. During interspecific interactions the snapping shrimp projects 35.7% anterior gill currents toward the antennules of the crab (n = 5 of 14).
The frequency pattern for pleopod currents is similar to that of lateral gill currents: the undirected currents significantly exceed the antennule-directed ones in each interaction type (P < 0.05 or 0.01, respectively; Fig. 5C). In homo interactions an average of only 11.5% (n = 6 of 52) of all pleopod currents are projected towards the chemoreceptive antennules, and during hetero interactions 16.7% (n = 8 of 48) of all pleopod currents reach the antennule area. Finally, in interspecific interactions no pleopod current is aimed towards the antennules of the crab, but all (n = 54) are directed elsewhere.
Anterior gill currents and water jets
In view of the prominent role of the anterior gill current with respect to its timing after a physical contact and the increased possibility of chemosensory information transfer, we tested the correlation between these gill currents and emitted water jets (Fig. 6). As mentioned before, in comparison to intraspecific interactions, encounters with crabs are characterized by an increased number of water jets and a reduced number of anterior gill currents (Fig. 6C). In addition, more water jets are emitted in homo interactions between snapping shrimp (Fig. 6A) than in hetero encounters (Fig. 6B). Thus, the number of anterior gill currents significantly increases with an increasing number of water jets only in interactions between two snapping shrimp of the same sex (Spearman rank correlation coefficient: rs = 0.9, P < 0.01; Fig. 6A). This is not the case in interactions between two shrimp of different sex (rs = 0.5, P > 0.05), though a noticeable trend is shown and the overall low number of water jets may have prevented a significant result. An even lower degree of correlation is seen in interactions with a crab (rs = 0.4, P > 0.1).
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Discussion |
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Mechanisms of gill current production
Our experiments in tethered snapping shrimp show that water is sucked into the gill chamber due to a depression elicited by the beating scaphognathites (Fig. 1A). A "normal" gill current is then released anteriorly with low velocity through two small openings of the carapace. Once the left or right expodites of the second and third maxillipeds start fanning, the current is accelerated and deflected laterally to that side (Fig. 1B). As previously described in lobsters (Homarus americanus), the exopodites of the first maxillipeds do not contribute to these lateral gill currents in snapping shrimp, whereas in crayfish (Procambarus clarkii) these appendages are also involved (Breithaupt, 1998).
The production mechanism of the fast anterior gill current remains unclear, since this behavior obviously requires physical, chemical, or visual contact during intra- or interspecific encounters of snapping shrimp, and thus was never seen in tethered animals. From our knowledge about the lateral gill current, we assume that the fast anterior gill current is created by high-frequency beating of the scaphognathites without contribution of the exopodites of the second and third maxillipeds. Since it is difficult to video-record the mouth parts with high magnification during social interactions, we are currently testing other methods of monitoring scaphognathite beating frequencies during encounters to verify this hypothesis.
Role of the fast anterior gill current during social interactions
The analysis of the fast anterior gill current revealed the most surprising and interesting results. Although anterior gill currents were observed and well described in lobsters (Atema, 1985, 1995) and crayfish (Breithaupt, 1998), we found decisive differences in snapping shrimp. First of all, Alpheus heterochaelis produces different types of anterior gill currents. The "normal" anterior current is a slow, weak release of water, which was sucked through the gill chamber, as opposed to the fast, strong, anteriorly directed gill current, which occurs during social interactions. The production of the fast anterior gill current is rare (Fig. 2) but strongly linked to previous contacts with a conspecific or a crab (Fig. 4B). Among the observed currents, only the fast anterior current is created shortly after a preceding contact, regardless of the type of opponent. In fact, this current never occurred before the first contact. Moreover, we show that only this current is suited to transfer chemical information towards the other animal (Fig. 5B): it reaches the antennules of the opponent in nearly 50% of all cases.
Of all analyzed currents, only the fast anterior gill current shows some peculiarities with respect to the shrimps’ opponent. The number, duration, and range is smaller in encounters with a crab than in interactions with conspecifics (Figs. 2, 3). We assume that the shrimp collect information about the genus of their opponent and reduce the effort to communicate accordingly, if it is a crab.
Role of lateral gill currents during social interactions
During social interactions between snapping shrimp and conspecifics of the same or different sex as well as during interactions with small crabs, the lateral gill currents are most prominent and significantly outnumber all other observed currents (i.e., pleopod currents and fast anterior gill currents; Fig. 2). Moreover, they are produced for long intervals but have a short range and a low velocity (Fig. 3). They are barely elicited by physical contact (Fig. 4A) and hardly ever reach the antennules of their opponents (Fig. 5A). These properties of the lateral gill currents do not change with different opponents but appear to result from a stereotyped form of production. Thus, obviously lateral gill currents are not predestinated to play a prominent role in active (chemical) signaling between the animals.
Still, their function needs explanation. From our observations we conclude that the lateral gill current is used to improve the shrimps’ ability to sense possible odor signals that occur at close distance. By redirecting the "normal" gill current, the shrimp refreshes the area around its chemical receptors from its own smell (released by the slow and permanent gill current) and thereby improves the detection of the chemical surrounding. This idea is supported by our knowledge that Alpheus heterochaelis naturally inhabits small, oyster-shell-covered areas with little water flow and that individuals of the species appear to be rather stationary within that area (Herberholz and Schmitz, pers. obs.). The lateral gill current produced by snapping shrimp seems to be used to remove water from the area around the antennules and to a much lesser extent to draw water toward that region as proposed for the posteriorly or laterally redirected gill currents of lobsters and crayfish (Atema, 1995; Breithaupt, 1998). In contrast to lobsters and crayfish, snapping shrimp were never observed to fan simultaneously with appendages on both sides. Instead, they beat the exopodites of one side at a time, and there are no obvious movements of particles from the opposite side toward the animal’s anterior region.
Role of pleopod currents during social interactions
In lobsters (Homarus americanus), pleopod currents are used for chemical (possibly pheromonal) communication during courtship at a shelter (Atema, 1985, 1988, 1995; Cowan and Atema, 1990; Bushman and Atema, 1997). The snapping shrimp Alpheus heterochaelis, in addition to using its pleopods for locomotion and to provide an oxygen supply for attached eggs, uses them for shelter digging, fanning the substrate (sand or muddy-sand) backward behind it (Nolan and Salmon, 1970). These authors also mention (pleopod) fanning as an aggressive act, with a shrimp vigorously beating its pleopods and directing a water current posteriorly quite close to another shrimp. The frequency of pleopod fanning is not noted by Nolan and Salmon (1970), but the behavior was described to occur between two females at the entrance of a shelter. In our experiments, we did not provide a shelter, and all shrimp were in the middle of their molt cycle. In view of the finding that the actual impact of pleopod currents in lobsters depends to a high degree on the molt state of the animals as well as on their readiness to mate (Cowan and Atema, 1990), these conditions may have affected our results. Though pleopod currents were rather often produced (Fig. 2) and (in comparison to gill currents) show an average duration, a large range, and high velocity (Fig. 3), there is a lack of correlation with previous contacts (Fig. 4C) and a low precision in hitting the antennules of the opponent (Fig. 5C). There are hardly any differences in the characteristics of these currents towards different opponents. All this indicates that pleopod currents are of little relevance for (chemical) signaling or communication among snapping shrimp and between shrimp and sympatric crabs under our conditions.
A specialized gill current for chemical signaling and communication?
The transfer of chemical signals between interacting lobsters (see e.g., Atema, 1995; Bushmann and Atema, 1997) and crayfish (Breithaupt et al., 1999) has been described in detail. In lobsters these signals can evoke long-term individual recognition (Karavanich and Atema, 1998a, b), and in crayfish they communicate dominance status or stress condition (Zulandt Schneider et al., 1999; Zulandt Schneider and Moore, 2000). In all cases, urine-borne signals were assumed to be the source of chemical signaling (Breithaupt et al., 1999; Breithaupt, pers. comm.). Since the urine is released through a paired set of nephropores on the ventral sides of the basal segments of the second antennae (Parry, 1960), it can be carried toward an opponent by the anterior gill current. Moreover, agonistic behavior in catheterized lobsters increases the probability and volume of urine release (Breithaupt et al., 1999).
In the present study we show for the first time that the pattern of water current production actually changes with respect to the social situation of an aquatic animal. Although snapping shrimp have the ability to produce "normal" anterior gill currents, they create different, more powerful, anteriorly directed gill currents shortly after contacting their interaction partner. These elicited currents are then more likely to reach the opponents’ area of chemical perception. The same may hold true for lobsters and crayfish, but their currents have not yet been quantified during social interactions. On the other hand, we still have to prove that the fast anterior gill current in snapping shrimp actually carries chemical signals toward the opponent. Although the data presented favor this assumption, we cannot exclude the possibility that hydrodynamic signals transferred by the gill currents participate in the communication between the animals. Judging by their sensory equipment, snapping shrimp—like crayfish (Mellon, 1996) and lobsters (Guenther and Atema, 1998; Weaver and Atema, 1998)—are most likely to perceive hydrodynamic stimuli as well as chemical stimuli with their antennules (Schmitz, unpubl.). We plan to test this possibility by deactivating the chemical receptors only.
In any case, the production of the fast anterior gill current may play a critical role during hierarchy formation in snapping shrimp. We show that in intrasexual encounters the numbers of water jets and anterior gill currents are positively correlated (Fig. 6) and that both are significantly higher in the winner than in the loser (Fig. 7). In the present study, winner and loser met in only a single 20-min experiment. Preliminary experiments show that repetitive pairing of winners and losers reduces the number of water jets and anterior gill currents (Obermeier and Schmitz, unpubl.). This supports the finding that these behaviors are most probably correlated with dominance and social status in snapping shrimp. Although the strength of the water jet represents the strength of the animal (see Herberholz and Schmitz, 1999), the signal transferred by the gill current may then allow recognition of the sender. This, in turn, can prevent two Alpheus heterochaelis shrimp of the same sex from engaging in more severe fighting during subsequent encounters, thus reducing the number of the "costly" water jets.
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Acknowledgments |
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Footnotes |
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0.01 are indicated by two asterisks (**).
