The Tactile Communication between Cryptocentrus steinitzi (Pisces, Gobiidae) and Alpheus purpurilenticularis (Crustacea, Alpheidae)

2. Tierpsychol., 49, 173-196 (1979) @ 1979 Verlag Paul Parey, Berlin und Hamburg ISSN 0044-3573 I ASTM-Coden: ZETIAG

The Heinz Steinitz Marine Biology Laboratory, T h e Hebrew University of Jerusalem, Elat, Israel

The Tactile Communication between Cryptocentru~ steinitzi (Pisces, Gobiidae)

and Alpheus purpurilenticularis (Crustacea, Alpheidae)

By ILAN KARPLUS

With 13 figrrres

Received: June 20,1978

Accepted: August 16,1978

Abstract The tactile alarm system between the symbiotic goby Cryptocentrus steinitzi and its

burrowing shrimp partner Alpheus purpurilentrcularrs was investigated by underwater observations in the northern Red Sea. Warning signals by the goby which elicit the retreat of the shrimp into its burrow consist mainly of rapid tail flicks transmitted to the shrimp through its long antenna. No warning signals are given without that contact. The daily rhythm of the antenna1 contacts was described. Warning signals are emitted by the goby in a selective manner only in response to the approach of certain species of fish to the burrow entrance. The response of the shrimp to warning signals was described. The goby-shrimp conimunica- tion system was used to study predator recognition in a series of controlled experiments. The sequence of the acts of the goby and shrimp was analyzed.

1.1. General Introduction

The associations between burrowing alpheid shrimp and gobiid fish have a wide circumtropical distribution. They were first*discovered 20 years ago in the Palau Islands of the Pacific (BAYER and HARRY-ROFFEN 1957). Since then they have been reported in many other localities, including the Red Sea (LUTHER 1958; KLAUSEWITZ 1969, 1964, 1974a, b; MAGNUS 1967), the Persian Gulf (PALMER 1963), Japan (HARADA 1969, 1971), the Hawaiian Islands (MOEHRING 1972) and the tropical Atlantic (RANDALL 1968).

These associations are mutually beneficial paitnerships in which the fish uses the burrow excavated by the shrimp as shelter while providing the shrimp, who has poor vision, with a tactile alarm system. A constant antenna1 contact is maintained between shrimp and fish while the shrimp is outside the burrow (MAGNUS 1967; KARPLUS et al. 1972a, b). The warning signals from the fish which elicit the retreat of the shrimp into the burrow consist mainly of rapid

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174 ILAN KARPLUS

tail flicks transmitted to the shrimp through its long antenna (MAGNUS 1967; HARADA 1969; MOEHRING 1972). Both field observations (MAGNUS 1967; HARADA 1969; MOEHRING 1972) and observations in aquaria (KARPLUS et al. 1972a) describe the immediate retreat of the shrimp into the burrow in response to the retreat of the goby. The only quantitative study of this communication system has dealt with the communicatory value of different acts of the symbiotic goby Psilogobius mainlandi and its partners Alpheus rapax and A. rapadica (MOEHRING 1972).

I n order to investigate the goby shrimp communication system a three year field study (1972-1975) was carried out in the northern Red Sea on associations of Cryptocentrus steinitzi and Alpheus purpurilenticularis. The main points of this study were the rhythm of antenna1 contacts, the occurrence of warning signals under natural conditions, predator recognition, and the comniunicatory value of the acts of the partners. The structure of the signals and the details of the rapid interactions between the partners as revealed through film analysis will be presented in another publication.

1.2. The Study Area The study was carried out in the shallow (max. depth 2 m ) and sandy lagoon of the

Elat Nature Reserve. This lagoon which is between 20-50 m wide separates the narrow fringing reef from the shore which is composed of beach rock slabs. Inside the lagoon and close to the shore are dead coral boulders 1-2 m in diameter covered mainly with algae and some living corals of the species Stylophora pistillata. Closer to the reef table are larger coral patches which partly merge with the reef. The sediment inside the lagoon is not uni- form, close to the reef table and among the larger coral boulders finer sediment is found whereas in the more open areas of the lagoon the sediment is coarser. I t is within this sediment that the associations between Cryptocentrrrs steinitzi and Alpheus purpurilenticularis are found. These associations are very abundant reaching densities of up t o 2-3 associations per m?.

1.3. The Goby and the Shrimp

C.steinitzi is a small gobiid fish (Fig. 1). Measurements of 40 specimens revealed mean standard length to be 59.5 mm (s.d. = 8.5). This goby was first identified as Cryptocentrrrs sungarni by Prof. W. KLAUSEWITZ (KARPLUS et al. 1974), but in a later revision was identified by KLAUSEWITZ as a new species. A detailed description of the species morphology, coloration and distribution was given by KLAUSEWITZ (1974a) and POLUNIN and LUBBOCK (1977).

Alpheus purpurilenticularis is a small alpheid shrimp (Fig. 1). Measurements of 25 in- dividuals (measured from tip of rostrum to telson) revealed a mean length of 37 mm (s.d. = 4.5). Its colour is greenish grey. There are brownish-yellow patches on the abdomen and carapace and two large brown spots on each side of the carapace. The sbrimp has very long antennae that are almost twice as long as its length. A detailed description of the shrimp and its distribution will be given by Dr. Y. MIYA who identified this species.

1.4. The Association

C. steinitzi and A. purpurilenticularis remain in close contact during the entire day since the goby does not move away from the burrow entrance. It either sits very close to the burrow or a t the end of a groove which is formed and constantly used by its partner the shrimp. These associations are usually composed of a single goby and a pair of similar sized shrimps. Paired gobies were observed at a low frequency throughout the entire year. The positive size correlation between goby and shrimp is probably the result of competition between gobies for the larger burrows which are constructed by the larger shrimp (KARPLUS et al. 1974). These associations seem obligatory, since the partners are only observed in association. A shrimp deprived of its goby

Tactile Communication between Cryptocentrus steinitzi and Alpheus purpurifenticuluris 175

Fig. I : Alpheus ptrrptrrilenticufuris maintaining antenna1 contact with Cryptocentrus steinitzi (Photo J. WINKELFELD)

retreats into its burrow, gradually almost completely blocking its opening. It resumes its activity outside its burrow only after a goby inserts its tail into the burrow opening and the antenna1 ccntact is renewed. In addition, gobies spend only very short periods of time without their partners. The conspiciously coloured goby, when isolated from the shelter of its burrow, is under heavy predatory pressure. Gobies introduced into glass tubes at some distance from their burrows were rapidly and intensively attacked by several species of predatory fish.

Cooperation between partners is not limited to the sharing of a common shelter and warning system. In a study on the structure and dynamics of the burrows of A . purpurilenticularis and C. steinitzi i t was found that although the goby does not actively dig, i t regulates both the formation of a new opening every morning and the daily shifts of the opening which may reach 80 cm per day. The gobies regulate the densities of the burrow openings through their aggressive intraspecific interactions with their neighbours (KARPLUS et al. 1974).

The partners do not compete for food. The shrimp is a detritus feeder, cating organic material found within the sediment, whereas the goby feeds on small invertebrates found both in the plankton and the sediment close to the burrow opening.

The partner specificity of C. steinitzi and A . purpurilenticularis was investigated in a comparative study carried out in the Elat Nature Reserve and aquaria. The goby and shrimp are mutually attracted. The goby is optically attracted to the shrimp and the shrimp is chemically attracted to the goby. When presented in a choice situation with other species of symbiotic gobies or shrimp, A . purpurilenticularis and C. steinitzi showed a strong mutual pre- ference (KARPLUS, in prep.).

11. General Methods Observations were carried out with SCUBA and immediately recorded on underwater

slates. Most of the study was carried out from behind an observation shield. In this study, the observation shield turned out to be very useful since the goby focused most of their attention on objects moving close to the substrate. For example, a model of a predatory fish

176 ILAN KARPLUS

approached to a goby 20 cm above the ground was less effective in releasing warning signals then the same model close to the ground. Thus, the use of the observation shield assured that no movement would be perceived by the goby at ground level. The goby would ignore a diver behind the shield and would adopt its black colour phase which is typical for low levels of fear. Since the Elat Nature Reserve and especially the lagoon are visited by hundreds of bathers all the summer months, the coral fish tend to pay very little attention to humans. Similar observations were made by FRICKE (1975) in the same locality for the anemone fish Amphiprion bicinctus.

The procedure used in all observations and experiments began with the installation of the Observation shield and experimental equipment near the burrow entrance. % h later the shield was slowly and gradually approached from behind. Observation and experiments were started only after 10 min of acclimatization. Such a period required that no warning signals would be given by the goby, except those which were clearly released by species of fish coming close to the burrow entrance. The detailed methods and procedure for the different sections of this study will be presented below.

111.1. The Daily Rhythm and Antenna1 Contacts

The tactile contacts between shrimp and goby are one of the most important features of their communication system. Symbiotic shrimp maintain a constant antennal contact with their fish partners when outside their burrows both in the sea (MAGNUS 1967) and when living in artificial burrows in aquaria (KARPLUS et al. 1972a). Experiments in aquaria with the shrimp Atpheus djiboutensis with damaged antennae demonstrated that without the contact the shrimp do not respond to the retreat of its partner the goby Cryptocentrus cryptocentrus into its burrow. Normally, this act always brings about the rapid retreat of the shrimp. Thus, the contacts are essential for the transfer of information between goby and shrimp (KARPLUS et al. 1972a). Therefore, as a first study, observations were carried out on the daily rhythm of antennal contacts.

111.2. Methods

Observations on the daily rhythm of antennal contacts were carried out during 12 consecutive days from 22 July 75 to 2 August 75 on 12 different associations of C.steinitzi and A . purpurilenticularis. Observations were carried, out inside the lagoon from behind large coral boulders at a distance of about 2 m from the associations. Each association was observed for 10 min during six observation periods covering the entire day: 5.40-6.20; 8.40-9.20; 11.40-12.20; 14.40-15.20; 16.10-16.50; 17.40-18.20 h (The length of each observation period was longer than 10 min since during the same interval additional species were investigated). The following events were recorded using two stopwatches: 1) The duration of the antennal contact between a single shrimp and the goby. 2) The duration of the simulta- neous contacts between two shrimps and the goby. 3) The number of exits of the shrimp from the burrow.

Water temperature near the associations was recorded. Information concerning wind speed and direction, cloud coverage and wave level were obtained from the Israel Meteoro- logical Service.

111.3. Results

During the entire observation period the sea was very calm, only weak northern winds were blowing (average 4.2 knot) and the cloud coverage was usually 0 and only during two days 1/8. The changes of temperature during the day were minor and did not exceed 3 OC.

The duration of contacts between the goby and shrimp (contacts with either one or both shrimps) changed very markedly during the day (Fig. 2). Changes in the duration of antennal contacts could be the result of changes in the number of exits and the duration of the time the shrimps spent during

Tactile Communication between Cryptocentrus steinitzi and Alpheus purpurilenticularis 177

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each exit outside their burrows. Since the shrimp maintains a constant antennal contact with the goby while outside its burrow the duration of exits are equivalent to the duration of antennal contacts.

However, the number of exits of the shrimps from the burrow did not change significantly during the day (Fig. 3; Friedman analysis of variance - Xr2 = 9.755, df = 5 , p > 0.05). On the other hand, the average duration of each contact changed from about 15 s per exit early in the morning to about 5 s a t noon. A six-fold increase was observed in the late afternoon when the shrimps spent about 30 s during each exit outside their burrows (Fig. 4). Simul- taneously with the changes in the duration of the antennal contacts, there also was a shift in the predominant activity of the shrimp. I n the morning the shrimps left the burrows mainly with their chela filled with. sediment, deposited it near the entrance and returned quickly to their burrows with

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178 ILAN KARPLUS

empty chela without digging or feeding on the sediment outside the burrow. In the afternoon the majority of exits were with empty chela. The shrimps dug and fed on the sediment and carried it back into their burrows in most entrances (KARPLUS, in prep.).

The shrimp forms especially during the late afternoon a narrow groove 40-50 cm long and 1-2 cm deep. These grooves facilitate the acquisition of food by the shrimp since all digging and feeding activity outside the burrow is directed toward the upper thin layer of the undisturbed sediment, while the sediment removed from the inner parts of the burrow is not touched again. The grooves also direct the movement of the partners. Both goby and shrimp

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A rapid retreat of the goby would warn the shrimp in spite of temporary lack of contact, since the goby also moves in the groove on its way to shelter. On the rare occasions when the goby moves forward i n the groove while the shrimp is inside its burrow, the shrimp does not move over the point where during the previous exit i t has sensed the goby, but retreats immediately to its burrow. After a goby is left alone at the end of the groove for several min it returns to the burrow entrance, inserting its tail into the opening. As soon as antennal contact is renewed both partners move forward together in the groove.

Both fish and shrimp are active only during the day. During the night they stay inside their burrows, whose openings usually collapse. Activity usually starts early in the morning before sunrise but on rare occasions may start at noon. Activity is renewed by the goby, who protrudes its head and body through the collapsed opening, followed rapidly by its partner, the shrimp. The activity outside the burrow is terminated after sunset with the retreat of the goby and shrimp into their burrows.

IV. 1. Communication under natural conditions

Observations on communication systems in the natural environment with minimal interference of the observer are essential for the understanding of their function. The occurrence of warning signals until now has only been

move in tfie grooves, with the fish lying often at their end. In these cases the shrimp moves out of the burrow towards the goby without antennal contact. These very short periods are the only ones when the shrimp is outside its burrow without antennal contact with its partner.

F i g . 4 : The rncan duration of each antennal contact between A . . purpurrteri:icrrlaris and C. steinrtzi throughout the ilav (for

further explanations see Fig. 2 )

Tactile Communication between Cryptocentrus steinitzi and Alphews purpurilenticwlaris 179

observed during the approach of a diver to the goby-shrimp association (MAGNUS 1967; MOEHRINC 1972). Nothing was known as to the occurrence of warning signals in the sea i n a natural undisturbed setting. Thus, the following observations were aimed to clarify the functioning of the goby-shrimp communication system.

IV.2. Methods

In order to estimate distances of approaching fish from the burrow entrance, concentric iron rings were placed on the sand around the burrow entrance. The radius of these rings was 10, 20, 30, 40, 70 and 100 cm. Observations were made from behind an observation shield. Each observation session started with an acclimatization period of 10 min, and lasted 1 or 2 h. The following events were recorded: 1) The approach of any fish into the space within the rings, including its identity, size and route. Fish were classified as either small (< 10 cm), medium (10-25 cm) o r large (> 25 cm). 2) The position of the shrimp inside or outside the burrow during the approach of the intruder. 3) The warning signals given by the goby. Signals spaced less than 5 s apar t were grouped into one series. 4) Retreats of the goby into the burrow. 5) The response of the shrimp to warning signals and to retreats of the goby.

35 h of observations on 20 different associations were carricd out. All observations were carricd out in the later afternoon during August and September 1973.

IV.3. Results

The Intruding Species

During 35 h of underwater observations, 598 fish of different species were recorded within 1 m of the burrow entrance. The average intruding rate was 17.1 fish/h (S.D. = 6.5). The frequency of intrusion for each species has been calculated as the percentage of the total number of fish recorded within 1 m of the burrow entrance. The intrusion frequency of the following species was higher than 2 % : Parupeneus barbarinus and P. macronema (41.8 %); other species of the family Mullidae (2.8 %); Gerres sp. (31.1 %); Chaetodon chrysurus (9.3 %); Parapercis hexophthalma (6.0 %); Acanthurus nigrofuscus (2.8 %); Thalassorna ruppelli (2.0 %). The intrusion frequency of the following species was lower than 2 %: Cheilinus lunulatws; Lethrinus sp.; Siganus sp.; Synodus sp.; Dascyllus trimaculatus; Abudefduf saxatilis; fish of the family Scaridae; Diplodus noct; Pardachirus marmoratus; Ostracion cubi- cus; Torpedo sp.; Hemibalistes chrysoptera; Gomphosus sp.; Coris angulata; Pteros volitans; Fistularia petimba, fish of the family Apogonidae; and Meia- canthus nigrolineatus.

The Warning Signals

A total of 162 warning signals were recorded during 20 h of observations. Signals were only given by the goby while antenna1 contact was maintained between goby and shrimp. The number of signals per series varies from 1 to 9 with a mean of 1.7 signals per series (S.D.El.1). 93 % of all the signals (7.4 signaldh) were given in response to the approach of a fish to the burrow entrance. During the remaining 7 % of the signals no intruding fish were observed. These signals were probably given in response to intruders not noticed by the observer.

The approach of any small fish, such as M . nigrolineatus and fish of the family Apogonidae, did not release warning signals. Neither did the approach

180 ILAN KARPLUS

Table 1: The signaling of C. steinitzi upon the appearance of several common reef fish close to their burrows (in all observations, the shrimp was outside the burrow)

Species of fish

of medium sized fish which are not piscivorous or goatfish, even when very close to the burrow entrance. The three most common species belonging to this category were: Gerres sp., A . nigrofuscus and C. chrysurus (Table 1).

The species of fish releasing warning signals can be grouped into three main categories (covering 98 % of all recorded signals):

Group I. Fish of the family Mullidae. Medium sized non-piscivorous fish which regularly stir up sediment while feeding on organic matter. These fish are responsible for 61.9 % of all warning signals. 59.2 % of all signals were given in response to the two common goatfish species Parupeneus barbarinus and P. macronema, while only 2.7 % were given in response to other members of this family. P. barbarinus and P. macronema released warning signals in 78.3 % of their occurrence within 40-0 cm from the burrow entrance and only in 28.5 % of their occurrence within 100-40 cm from the entrance.

Group II. Large sized nonpiscivorous fish. These fish are responsible for 18.4 % of all warning signals. 14.3 % of all signals were given in response to Coris angulata and 4.1 % in response to C. lunulatus. The occurrence of adults (longer than 50 cm) of C. angulata within 100-40 cm of the burrow always caused the release of warning signals.

Group 111: Medium sized piscivorous fish. These fish are responsible for 17.7 % of all warning signals. 14.3 % of all signals were given in response to P. hexophthalma, 2.7% Synodus sp. and 0.7% in response to P. volitans. P. hexophthalma released warning signals in 78.5 % of its occurrence within 100-40 cm from the burrow entrance.

Warning signals were given in response to intruding fish when at a mean distance of 52 cm from the burrow entrance. This distance differs for different species. P. barbarinus and P. macronema released warning signals by C. steinitzi while at a mean distance of only 43 cm. Two other species released signals from a greater distance, P. hexophthalma - 82 cm, C. angulata - 85 cm. Only six of all the signals were given in response to fish more than 1 m away from the burrow entrance.

The Response of the Shrimp

The response of the shrimp to a warning signal was classified as either a retreat or no retreat into the burrow. The shrimp responded differently to a series of signals than to the individual signal. The shrimp retreated into the burrow in response to only 61 % of the 147 single warning signals, while it retreated in response to 92% of the 78 series composed of the same signals.

Tactile Communication between Cryptocentrus steinitzi and Alpheus purpurilenticularis 18 1

The seven series not eliciting retreat of the shrimp were further examined. In two of these series, warning signals were caused by fish already leaving the neighbourhood of the burrow. The average distance of the fish from the burrow in these seven series was 71 cm, which is further away than the mean distance of intruders releasing signals. In these seven series all the intruding fish were nonpiscivorous: P. barbarinus, P. macronema, P. mnrmoratus, C. an- pulata and C. lunulatus. It appears therefore that when the dan, aer was relatively low these series did not elicit a retreat of the shrimp.

The Retreat of the Goby into the Burrow

C. steinitzi emerges from its burrow shortly before sunrise and stays in front of its burrow during all hours of the day until it retreats into its shelter after sunset. During the day the fish enters its burrow only rarely and then only in order to obtain shelter. During 35 h of observation the symbiotic fish retreated into their burrows only 12 times. Most of these retreats were in response to approaching P. barbarinus and P. macronema (9 retreats) and only one retreat in response to the approach of each of the following species: Synodus sp., P. volitans and C. lunulatus. In no case did the goby retreat in response to the approach of small or medium sized fish which are not piscivorous or goat fish.

Despite the fact that few observations were available on the distances from which intruding species cause retreat and the time the goby spent in their burrows after an intruder's approach, it seems that these two parameters are different for different intruding species.

In all the retreats of the goby, its shrimp partner also disappeared into the burrow.

Observations on Additional Interactions with Predators and Goatfish

Several times, fish of the family Mullidae and especially P. barbarinus and P. macronema were observed blocking the burrow entrances by their digging activity. A P. hexophthalma was observed to attack from a distance of 20 cm a C. steinitzi which succeeded in disappearing into its burrow in timc. A goby artificially isolated from its burrow by blocking the opening was seized within seconds by a Synodus sp. which was lying buried in the sand near the burrow entrance. Moray eels of two species, Myrichthys maculosus and Gymnothorax gviseus were observed to enter the burrows of goby shrimp associations. They disappeared completely inside and remained in the burrows frorn several min to ' / z h. As opposed to other predators who can be avoided by retreating into the burrow, these eels are particularly dangerous for both fish and shrimp since they can also prey on them underground inside their shelter.

V.l. The Experimental Analysis of Predator Recognition

To date, few studies have dealt with the problem of predator recognition by fish. For example, Amphiprion bicinctus have been observed to attack predators selectively (FRICKE 1975). In addition both Ophistognathus aurifrons and Chromis cyanea were found to retreat into their shelters when approached by predators (COLIN 1971 ; HURLEY and HARTLINE 1974). Further- more, interspecific recognition has been experimentally demonstrated only in two species. A . bicinctus selectively attacks Chaetodon fasciatus which is the

182 ILAN KARPLUS

24

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predator of its host, the sea anemone Stochactis sp., while responding less to other species of similar size (FRICKE 1975). The territorial pomacentrid Eupornacentrus planifrons also has been observed to respond differently to different species of intruders (MYRBERG and THRESHER 1974; THRESHER 1976). Field observations on the occurrence of warning signals demonstrated in a preliminary way that C. steinitzi, the subject of this study, responds differently to the approach of a predatory and non-predatory fish. This ability to discriminate waj further tested in a series of controlled experiments.

T A . nigrofuscus (~(0 .002; Mann- Whitney U-test two-tailed). No significant difference was found between the number of signals given in response to A . nigrofuscus or the empty box (0-5 min: p>0.05; 6-10 min: p>O.l ; 11 to 15 min: p>O.l; Mann-Whit- ney U-test, two-tailed).

.

.

I

Ftg. ls: The number of warning signals of C.steznitzt given in response to: Pa-

A rapercts hexophthalma ( 0 ) ; Acanthurus 5 10 ISn l ln ntgrofuscus (m); the empty box (0).

V.2. Methods

The experimental analysis of predator recognition was based on a comparison of the number of warning signals of C.steinitzi given in the presence of a predatory and of a non- predatory fish of similar body length. Parapercis hexophthalma, a piscivorous fish and Acan- thurus nigrofuscus, a fish feeding exclusively on algae, were used in these experiments. Each of these fish was placed in a transparent perspex box 24 X 16 X 1 8 cm positioned 55 cm from the entrance to the burrow. In control experiments, the response towards the empty box was examined.

Before the start of each experiment, the box was covered by an opaque screen which could be removed from a distance by means of a wire. Observations were again carried out from behind the observation shield 70 cm from the burrow entrance. After a period of 1 0 m i n of acclimatization the opaque screen was ,removed and the fish in the box was exposed for 15 min. The following events were recorded: the number of exits of the shrimp from its burrow and the number of warning signals emitted by the goby.

All three experiments, each consisting of 10 trials, were carried out in October and November 1975. Every association was examined once only. Thus there was a total of 30 associations examined.


15 min I.

5 10

TI ME Fig. 6 : Thc number of exits of Alpheus prrrprrrilenticularis during the exposure to: Para- percis hexophthalrna ( 0 ) ; Acanthurus nigrofuscus ( w ) ; the cmpty box (0 ) (for further ex-

planations see Fig. 5)

Since warning signals are only given during antenna1 contact with the shrimp, the similarity of the three test series was examined by comparing the activity of the shrimp outside the burrow. The activity level was determined by counting the number of exits by the shrimps from their burrows (Fig. 6 ) . NO significant difference was found between the number of exits of shrimps in the three test series (0-5 min: p > 0.2; 6-10 min: p > 0.2; 11-15 min: p > 0.5; Kruskall Wallis H-test). Therefore, the different signaling rates are the result of the enemy recognition of the goby and are not the result of different levels of activity of the shrimp in the three test series.

VI.1. Sequence Analysis of the Acts of the Goby and Shrimp

In a field study carried out in Hawaii, MOEHRING (1972) found that in addition to the tail flick warning signal four other acts of the goby Psilogobius mainlandi cause the retreat of the shrimp into its burrow. She also found that the behaviour of the shrimp directs or inhibits the release of the tail flick warning signal. I n order to investigate the communicatory value of the acts of C. steinitzi and A . purpurilenticularis, the sequence of the acts of these partners was recorded and analyzed. Since observations in the sea demonstrated that the goby-shrimp communication system is activated by the approach of predatory fish, the sequence of the acts of the goby and shrimp were recorded in the presence of a living predator Parapercis hexophthalma (Fig. 7) . Models of predators were not used because the goby habituates very rapidly to them (KARPLUS, in prep.).

VI.2. Methods

A Parapercis hexopbthaha 20.5 cm long was introduced into a transparent box 5 X 6 X 21 cm. The cntire box, except for onc large panel, was perforated with holes in order to facilitate water exchange. The intensity of stimulation was varied by presenting the predator at a distance of 40, 80 and 120 cm from the busrow entrance. Observations were carried out from behind an observation shield 7 0 c m from the burrow entrance. After 10min of accli-

184 ~ L A N KARPLUS

matization the acts of the partners were recorded during 4 min while the predator was covered by an opaque plastic sheet. In the following 12 min the predator was exposed. The acts were recorded in the order of their occurrence. The acts of the shrimp were only recorded when one shrimp was outside the burrow. When two shrimps were outside the burrow only the acts of the goby were recorded.

Fig. 7: Parapercis hexophthalma, the predatory fish used to stimulate C. steinitzi (Photo C . KROPACH)

24 experiments, each with a different association, were carried o u t during July and August 1974. Each association was only tested a t one distance. A two-act sequence analysis was conducted. The relationship between the acts was classified as random, directive or inhibitive, using the method developed by HAZLETT and BOSSERT (1965) and DINGLE (1969). I n the obtained matrix an expected value of 0 was avoided by compiling certain acts and not including rarc acts. The xz value of a single cell of the matrix had very slightly less than one degree of freedom. For all practical purposes it could be taken as one unless the value was border-line for significance (mx WESTBY 1975).

VI.3. Results

The Acts of the Goby and Shrimp

The 12 recorded acts of the goby were classified into two categories:

A . Acts with no change in position (The goby is at the burrow entrance with its tail directed towards the opening)

2. E - Erect = the dorsal fins are either erect or half erect (Fig.1). 3. L - Lifting = the dorsal fins are erect. With its pelvic fins the fish lifts several times the anterior par t of its body above the ground (Fig.8). 4. M - Mouth Gaping = the dorsal fins are erect, the mouth is maximally opened with a lowering of the bucal cavity. The operculi are opened while the anterior par t of the body is lifted by the pelvical fins (Fig.9). - Tail movements: 5. T F - Tail flick = a rapid movement of the caudal fin with a very narrow amplitude of less than a cm. 6. TI3 - Tail Beat = a (rapid movement of the tail with a wide amplitude of several cm. 7. T M - Tail Move = a slow movement of the tail in a wide amplitude of several cm.

1. F - Folded = the dorsal fins are folded.

8, Acts with changes in position 8. H E - Head Entry = the goby retreats very rapidly, entering the burrow head first.

9. T E - Tail Entry = the goby retreats, with its tail entering first. 10. PTE = Partial Tail Ent ry = a partial retreat of the goby with its tail entering first. 11. Q F - Quidc Food

Tactile Communication between C r y p t o c e ~ ~ t r u s steinitzi and Alpheus purpurilenticularis 185

= a rapid and short movement either forward or sideways which terminates in collecting sediment with its mouth (probably for catching prey), 12. QP - Quidr Position = a rapid and short movement either forward or sideways.

Fig. 8: C. steinitzi lifting at the entrance of its burrow (Photo J. WINKELFELD)

Fig . 9: C. steinitzi mouth gaping a t the entrance of its burrow (Photo J. WINKELFELD)

The rapidly changing head colouration of the goby was recorded for each act. The following head colour phases were recorded: 1) B - Black phase - The black area reaches forwards to the lower jaw and backwards to the preorbital area. The iris is completely black (Fig. 11). - 2) G - Grey phase - The black area is limited mainly to the area between

186 ILAN KARPLUS

and around the eyes. The iris is grey with black borders. - 3) W - White phase - The head is entirely white. The iris is white except for black areas at its borders (Fig. 12).

Several acts which were limited to interactions between very close gobies, such as parallel swimming with erect fins and biting, were not included in the list of the acts of the goby because these interactions were not observed in the presence of a predator close to the burrow entrance.

The acts of the shrimp recorded were: E X - Exit = the shrimp leaves its burrow and stays outside it while maintaining

antennal contact with the goby (Fig. 1). EN - Entry = the shrimp enters its burrow while maintaining antennal contact with the goby. M - Massive = a massive contact between shrimp and goby while the shrimp exits or enters its burrow. The goby is pushed by the body and chelae of the shrimp while the antennal contact with the goby is maintained. P - Pinch = the goby is pinched a t the burrow cntrance while antennal contact is maintained. B - Burrow = the shrimp is inside its burrow.

No change in the behaviour of either goby or shrimp after a change in the behaviour of its partner was designated as N.

Head Colouration, Warning Signals and Fear

The three experimental series differed in the level of stimulation because in each series the predator was located at a different distance from the burrow entrance. The closer the predator to the burrow entrance, the more intense the stimulation. Each association was tested only at one distance.

In the first series (predator 40cm from the entrance) prior to the exposure, the mean frequency of the white phase of the zobv relative to the u z

other colour phases was low - 0.20. In the first 4 min of the exposure the mean frequency of the white phase increased to 0.97 and gradually decreased in the following two time intervals (5-8 min, 9-12 min) to 0.68 and 0.76.

In the second series (predator 80 cm from rhe entrance) the mean frequency of the white phase increased from 0.12 prior to the exposure to 0.64 during the first time interval after exposure. In the following time intervals a decrease in the white phase was again observed - 0.44; 0.30.

Fig . 10: C. s;elnitzi displaying its black he-d co!ouration (Photo J.

. . WINKELFELD)

Tactile Communication between Cryptocentrus steinitzi and Alpheus purpurilenticufaris 187

Fig. 11: C. s te in i t t i displaying its white head coloura-

tion (Photo J. WINKELFELD)

In the third series (predator 120 cm from the entrance) prior to the exposure of the predator the relative frequency of the white phase was low - 0.11. During the three following time intervals only a slight change in the relative frequency of the white phase occurred - 0.28; 0.31; 0.26.

The tail flick warning signals were given during all colour phases. Out of 196 observed tail flicks 172 were given while the head colouration was white, 20 when it was grey and only 4 while it was black. Thus most warning signals were given during the white phase.

The proximity of a predatory fish and the novelty of its exposure to the goby are positively correlated with the occurrence of the white head colour which is similarly correlated with the release of warning signals. As- suming that the closer a predatory fish is to a goby, and the more recent its exposure, the more intense the fear it evokes, cne can sug- gest that fear is positively correlated with the white head colour and the release of warning signals (Fig. 12).

Fig. 12: Head colouration, fear and warning signals of C. s te in i t z i . WS = the tail flick-warning signal; W = white head; G = grey

head; I3 = bladc head -

188 ILAN KARPLUS

Sequence Analysis of the Acts of the Goby

The frequency with which the acts of the goby carry over to one another are demonstrated in three flow diagrams (Fig. 13). Percentage frequencies of less than 1 "/o were not included in the diagrams. Only for the most common act of the goby - E - were the different phases of the head colour separately analyzed.

In the first series where the predator is very close to the burrow the level of fear of the goby was probably very high. The two most common. acts were: The goby positioned at the burrow entrance with erect fins and white head (E-W) - 32 % and the tail flick (TF) - 28 %. The connection hetween these two acts was the strongest of all transitions.

The second series is characterized by a medium level of stimulation (predator 80 cm from the entrance). Five dominant acts were found: Lifting (L) - 21 %, E-W - 18 %, E-G - 18 %, E-B - 16 9% and tail flick (TF) - 13 %. Between E-W, E-G and E-B were mutual transitions of equal strength,

Q A

%

C - Correction Fig. 1 3 : In sections A and B, P T F should read PTE

F i g . 13: Flow diagrams of the acts of C. steinitzi during 12 min of exposure to a predatory fish. The circles represent the acts of the fish. Each act is represented by a code discussed within the text. The line connecting each two circles represents their connection; the width, the strength of the connection. The upper par t of each diagram should be read from right to left and its lower par t f rom keft to right. In each diagram the predator was positioned a t a different distance from the burrow entrance A. = 40 cm; B. = 80 cm; C. = 120 cm; n =

total number of recorded acts


F

E

the transition between L and E-B was higher (9.3 %) than that between E-B and L (2%). Mouth gaping (M) - although not one of the dominant acts, had a 6.4 % transition with Lifting (L).

The third series is probably characterized by the lowest level of fear of the goby. Three dominant acts were found: E-B - 28%; L - 2 3 % and E-G - 21 %. The two dominant acts of the first series E-W and T F which are connected to high levels of fear occurred only at low frequency, in this series 8 % and 0.9% respectively. Similarly the partial tail entry (PTE) occurred a t very low frequencies and was not included in the flow diagram. Tail beat (TB) had a reduced frequency in the second series and disappeared completely in the third. BetweenE-B and E-G were higher transitions (10.2 76) than between E-G and E-B (6.3 %). E-B and E-G were both connected with L. As in all series mouth gaping (M) was strongly connected with L (5.1 %).

Sequence Analysis of the Goby-Shrimp Acts

The statistical analysis of the effects of the initial acts of the goby on the following acts of the shrimp were combined for the four time intervals and the three experimental series, since only 1088 transitions were recorded (Tables 2 and 3).

Table 2 : Interaction of Cryptocent?us sternrtzz and Alpheus purpurilentudaris. Distribution of T w o Act Sequences observed in 1088 interactions

Following Act of Shrimp

EX EN M R N Totals

18)' 11 (5) 9 11) 1 12) 0 15) 1 22

12L5) 325 05L) 221 (35) 5L (73) 0 (135) 45 6L 5

Code

F

I Totals I LIL I 261 I 60 1 12L I 229 I 1088 I

Dir. behav. Inhib. behav. of Shrimp of Shrimp

Behaviour Pattern of Fish xz

Folded Fins 10.52 <0.05

x. Values in parentheses are expected values.

E

L

M TF

Erect Fins 198.57 <0.001 EX, EN R, N

Lifting 65.74 c 0.00 1 N

Mouth Gaping 78.12 <0.001 N

Tail Flick Ll0.LL -= 0.00 1 R. N EX. EN

TB

TM

PTE

QF + QP

~~ ~~

Tail Beat 71.80 c 0.001 R

Slow Tail Movement 28.39 c 0.001

Partial Tail Entry 30.30 -= 0.001 R

Quick and short movement 126.75 co.001 R

190 ILAN KARPLUS

The following four acts of the goby which direct the retreat of the shrimp were the tail flick (TF), tail beat (TB), partial tail entry (PTE) and a rapid short movement of the entire body - QF and QP. The tail flick “directs” (HAZLETT and BOSSERT 1965) both retreat of the shrimp (R) and no reaction (N). It inhibits both the exit (EX) and the entrance of the shrimp into its burrow (EN). TB, PTE, QF and QP all direct the retreat of the shrimp (R). The goby lying at the burrow entrance with erect fins (E) both directs the exit (EX) and the entrance of the shrimp to its burrow (EN) and inhibits R and N. Lifting (L) and mouth gaping (M), typical for intraspecific interactions of the gobies, d o not play any part in the goby shrimp communication system and both direct no change in the behaviour of the shrimp (N). The acts of the goby, F and TM, have an overall significant effect on the acts of the shrimp but with no significant effect on a particular act of the shrimp.

The presence of the goby close to the burrow is essential both for the exit and activity of the shrimp outside its burrow. When the goby leaves its previous position at the burrow entrance, the shrimp remains inside the burrow. When the goby leaves its previous position at the end of the groove (40-50 cm from the burrow entrance), the shrimp, as previously described, retreats after reaching the point where i t sensed the goby during the previous exit.

In addition to the above-mentioned acts of the goby which direct the retreat of the shrimp, additional acts, although occurring at low frequencies, preceded the retreat of the shrimp. All these acts can be divided into two categories.

I . Rapid Movements of the Goby This category preceded 21.8 % of all recorded retreats. These movements

occurred also without the presence of the shrimp outside its burrow. This group included both head entries (HE) and tail entries (TE) of the goby into its burrow. In our experiments, the predator was positioned at such a distance from the entrance that it would not bring about the retreat of the goby, thus terminating the observation. Additional acts of this category are partial tail entry (PTE), a rapid collecting of sediment with its mouth (QF), a rapid small change in position (QP) and lifting (L.). The shrimp responded always with retreat to HE, TE and QP while only sometimes in response to QF (80 %), PTE (75 %) and L (0.9 %).

I I . Warning Signals The warning signals occur only in the presence of the shrimp outside the

burrow. These signals included the tail flicks (TF) and tail beats (TB). 78.2 % of all the retreats of the shrimp were preceded by these acts. The tail flick (71 % of retreats) is given while only antennal contacts are maintained or both antennal and massive contacts. Tail beats (7.2% of retreats) are only given while in addition to the antennal contact also a massive contact is maintained between shrimp and fish.

Sequence Analysis of the Shrimp-Goby Acts

The statistical analysis of the effects of the initial acts of the shrimp on the following acts of the goby were combined for the four time intervals and the three experimental series since only 15 19 transitions were recorded (Tables 4 and 5).

Tactile Conirnunlcation between Cryptocentrus steinitzi and Alpheus purpurifenticufaris 191

Code

EX

Table 4: Interaction of Alpheus purpurilenticularis and Cryptocentrus steinitzi. Distribution of Two Act Sequences observed in 1519 interactions

I Followino Act of Fish 1

Dir. behav. Inhib. behav. of Fish of Fish

Antenna1 Contact During Exit 128.38 <0.001 TF TM

Behaviour pattern of Shrimp xz

zL Values in parentheses are expected values.

Table li: Tntcraction of Alpheus purpurilenticularis and Cryptocentrus steinitzi. Analysis of Interspecific T w o Act Sequences

M

R

8

Massive Contact 1288.50 <0.001 TM, TB N

Retreat 3L8.95 <O.OOI E L, N

Inside Burrow 181.15 <0.001 L. TF

I EN 1 Antenna1 Contact During Entrance I 270.L9 I <0.001 I N I L. E I.

The occurrence of the shrimp inside the burrow (B) inhibits the tail flick (TI;) of the fish. This act occurs only in the presence of the shrimp. The occurrence of the shrimp inside the burrow does direct mouth gaping (M) and lifting (L) of the goby. It seems that under conditions of high levels of fear tail flicks have priorities over other acts. Therefore, when the shrimp is inside its burrow some acts are directed. The exit of the shrimp from its burrow while only maintaining antenna1 contacts (EX) directs tail flicks (TF) and inhibits the occurrence of a slow movement of the tail (TM). Massive contacts between shrimp and goby (M) direct TM and TB.

The shrimp which emerges from its burrow with sediment and coral fragments, prior to its entry to the burrow (EN) deposits the sand at some distance from the entrance and places the coral fragments and stones very carefully above the burrow entrance. When retreating (R) the sand and stones are dropped a t the entrance. EN directs no change in the acts of the fish (N) and inhibits the occurrence of E and L. The retreat of shrimp (R) directs E of the goby and inhibits the occurrence of L and N. One of the acts of the shrimp - pinching of the goby (P) - was only twice observed and therefore was not included in the statistical analysis.

Discussion

The goby and shrimp association provides a rare example of a tactile alarm communication system. Most alarm communication systems are acoustic or chemical and only a minority of systems are visual or tactile (MARLER 1968;

192 ILAN KARPLUS

WILSON 1975). While chemical and acoustic systems are effective during both day and night, visual systems are only effective during the day, under conditions of good visibility. Tactile communication systems are even more restrictive, since they require the communicating animals to be very close to each other. In our case the goby and shrimp completely fulfil the condition for using a tactile alarm system, since they maintain an antennal contact.

The major environmental factors regulating the rhythmicity in the activity level of the shrimp outside its burrow during the day seem to include:

1) Light intensity, which is negatively correlated with activity level. An increase in activity was observed a t low light intensities, especially in the late afternoon.

2) The collapse of the underground system of burrows which is affected by wave action, the character of the sediment and the occurrence of hard objects within it. Most of the exits of the shrimp from the burrow with chela loaded with sediment occur in the morning and probably are due to the collapse of the burrows during the night.

. . . .

3) The occurrence of the food of the shrimp outside its burrow. It is important that this entire study was carried out in the sea. Studies

on the antennal contacts of A . purpurilenticularis and C. steinitzi in aquaria either with artificial burrows or with rock and sediment yielded different results from those obtained in the sea. The shrimp in aquaria spent only very short periods of time outside the burrows, mainly clearing them from sediment. Similar results were obtained for A. djiboutensis and Cryptocentrus cryptocentrus in aquaria (KARPLUS et al. 1972 a).

The goby-shrimp communication system is characterized by a high rate of warning signals displayed by the goby, much higher than the low rate of retreats of the goby into its burrow. Only when certain species of intruding fish cross a critical distance, and a high level of danger is reached, do goby retreat. Thus, there is a wide range within which the goby is aware of low danger, and warning signals are transmitted to the shrimp without the goby retreating. For the alert goby the disadvantage of being exposed to low danger while staying outside the burrow is small, and compensated for by the advantage of longer access to food. The shrimp, which has poor vision and is completely dependent on the goby outside its burrow, has the advantage of being warned both from danger of low intensity by warning signals and from danger of high intensity by the retreat of the goby.

The high rate of signaling reported in this study occurred only during the late afternoon, since these hours are characterized by an increase of both the activity of reef fishes and the time the shrimp spent outside their burrows.

There are many factors which determine whether a fish close to the burrow entrance elicits warning signals from the goby. The size of an approaching fish seems to be of importance. Big fish such as C. lunulatus, C. angulata and members of the family Scaridae elicit warning signals although they are neither piscivorous nor diggers. In contrast no small fish cause the release of warning signals. There are some fish which elicit warning signals although they endanger the associations only indirectly. Goat fish for example do not threaten either goby or shrimp by direct predation but they occasionally do block the burrow entrances completely by stirring up the sediment. If the goby and shrimp would not retreat into the burrows in time they would become exposed to predators due to that blockage.

The ability of C. steinitzi to discriminate between a predatory and non- predatory fish was indicated from observations in the field and confirmed by

Tactile Communication between Cryptocentrus steinitzi and Alpheus purpwrilenticutaris 193

controlled experiments. It is possible that the very small, young goby respond initially by emitting signals and retreating into their burrow a t the approach of all fish. Only by a gradual process of habituation do they cease to respond to common non-predatory fish. Also FRICKE (1975) has suggested for A . bicinctus that a learning process is envolved in predator recognition.

C. steinitzi was found to change its head colouration rapidly. Close to a predator, the head was white, whereas a t a greater distance from the same predator the head was black. Assuming that the closer a predatory fish is to a goby and the more recent its exposure, the more intense is the fear i t evokes, then white head colouration is correlated with fear. Other situations typical for the white phase also point in this direction. Gobies which left their burrows for either reaching another burrow or for acquiring food at some distance always adopted the white colour phase, while when they returned to their own burrow or reached another burrow their head colour became black again. Probably the advantage for these colour changes is that in the white phase the goby is less conspicuous to predators because it blends well with the light coloured sand. The conspicuous black colour phase is advantageous in intraspecific interactions, the black phase facilities the rapid location of a mate and thus during the breeding season the exposure to predators is minimal.

In numerous species of the family Gobiidae the light colour phase is also typical for a submissive individual, while a dominant and aggressive goby is darker (WEBB 1974; KINZER 1960). A similar relationship was observed in C. steinitzi. The black colour is typical for mouth gaping and lifting which are very common in aggressive intraspecific interactions. The mouth gaping is a typical threat display observed in numerous species of Gobiidae (WEBB 1974; KINZER 1960; MORRIS 1954; TAVOLGA 1954). The lifting display is common in aggressive interactions of low intensity especially between gobies of adjacent burrows. The common transition from mouth gaping to lifting is thus a shift from higher to lower aggression.

The goby-shrimp communication system is an open system constantly responding to external stimuli. The system is activated by various disturbances, usually approaching fish of different species. In the experimental analysis of the sequence of the acts of the partners the communication system was activated by a living predator positioned close to the entrance. The response of the goby to the predator changes with distance, with time and probably also in response to the predator movements. It is therefore possible that some of the changes in the acts of the goby which followed the occurrence of a new act by the shrimp were the result of some acts of the predator. The presence of the predator had probably no effect on the shrimp because of its poor vision. Therefore the goby-shrimp interaction can be analyzed without this restraint.

The most important effect of the shrimp on the goby is that i t either directs or inhibits the release of warning signals. No 4ignals are released while the shrimp is inside its burrow and the antennal contact between shrimp and fish is not maintained. Warning signals are directed by occurrence of antennal contact under conditions of high levels of fear of the goby (white head colouration). At low levels of fear (black head colouration) no warning signals are released despite the antennal contact.

The most important communicatory acts of the goby are those which direct the retreat of the shrimp. The two types of acts which direct i t are rapid body movements and special warning signals. The first one occurs both in the absence and presence of the shrimp. Some of the rapid body movements HE, TE and PTE are connected to situations of danger, while QF and QP and L

2. Tierpsychol., Bd. 49, Heft 2 13

194 ILAN KARPLUS

are not. Probably the shrimp responds to the latter group because of their similarity to the initial part of the former. The shrimp always retreats in response to the retreat of the goby to its burrow while only in response to part of the typical warning signals. When the shrimp does not respond to a warning signal two additional options for warning are left, the reception of an additional signal and the retreat of the goby. A shrimp not responding to the retreat of the goby is left exposed to predators without its warning system.

This tactile alarm system is essential in an environment which is, on one hand, rich with predators and, on the other hand, poor in hiding places. The alert goby provides the alarm system against any intruding fish which is potentially dangerous and the shrimp provides the shelter.

Summary

The tactile alarm system between the goby Cvyptocentvus steinitzi and its burrowing shrimp partner Alpheus puvpurilenticularis was investigated in the northern Red Sea.

Warning signals by the goby which elicit the retreat of the shrimp consist mainly of rapid tail flicks transmitted to the shrimp through its long antennae. Antenna1 contacts between shrimp and goby are maintained as long as the shrimp is outside its burrow. Without this contact no signals are generated. The duration of the antennal contacts varies according to the time of the day.

The warning signals are given selectively in response to the approach of certain species of fish to the burrow. All big fish and medium-sized predatory and digging fish trigger the release of warning signals. The goby does not respond to the approach of other medium sized or small sized fish. Predator recognition by the goby as revealed by its signaling response was experimentally demonstrated.

The head colour of the goby which is either black, grey or white is an indication of different levels of fear. High levels of fear are positively correlated with the generation of warning signals.

The sequence of the acts of goby and shrimp were recorded in the presence of a living predator (Pavapevcis hexophthalma). Certain acts of the goby direct the retreat of the shrimp. These acts include two types: (1) Rapid movements of the goby which occur also in the absence of the shrimp; (2) Special warning signals which occur only in the presence of the shrimp outside its burrow.

The main information transferred from the shrimp to the goby is its occurrence outside the burrow. No warning signals are emitted when the shrimp is inside its burrow. Warning signals are directed by the antennal contact under conditions of a high level of fear. At low levels of fear no warning signals are released despite the antennal contact.

Zusammenfassung

Das taktile Warnsystem zwischen der Grundel Cryptocentvus steinitzi und ihrem Partner, der grabenden Garnele Alpheus puvpurilenticulavis, wurde im nordlichen Teil des Roten Meeres untersucht.

Warnsignale der Grundel, die den Ruckzug der Garnele auslosen, be- stehen hauptsachlich in kleinen schnellen Ausschlagen des Schwanzes, die die

Tactile Communication between Cryprocentrus sternrtzr and Alpheus purpurilentrcularrs 195

Garnele durch ihre langen Antennen wahrnimmt. Wann immer die Garnele sich auflerhalb des Baues befindet, beruhrt sie die Grundel mit ihren Antennen; ohne diese Beruhrung warnt die Grundel ihren Partner nie. Die Dauer der Beriihrung zwischen der Garnele und der Grundel schwankt mit der Tageszeit.

Die Warnzeichen werden selektiv dann gegeben, wenn sich bestimmte Fischarten dem Bau der Garnele nfhern. Alle groflen Fische sowie auch bestimmte mittelgrofle Raub- und Wuhlfische sind reizwirksam, doch reagiert die Grundel bei Annaherung anderer mittelgrofler und kleiner Fische nicht. Das selektive Erkennen von Raubfischen durch die Grundel, gemessen an der Anzahl von Warnzeichen, wurde experimentell gezeigt.

Die Kopffarbe der Grundel, schwarz, grau oder weifl, zeigt verschiedene Grade ihrer Furcht an. Die vermehrte Aussendung von Warnsignalen ist mit einem hohen Grad von Furcht verbunden.

Die Folge der Bewegungen der Grundel und der Garnele wurde in An- wesenheit eines lebenden Raubfisches (Parapercis hexophthalma) registriert. N u r bestimmte Bewegungen der Grundel fuhren zum Ruckzug der Garnele. Zwei Gruppen von Bewegungen sind hier zu unterscheiden: 1. Schnelle Be- wegungen der Grundel, welche auch auftreten, wenn sich die Garnele nicht auflerhalb des Baues befindet, 2 . spezielle Warnsignale der Grundel, die sie nur gibt, wenn die Garnele aui3er Hauses ist.

1st die Garnele im Bau, gibt die Grundel keine Warnsignale ab. Bei grofler Furcht warnt die Grundel, bei geringer Furcht, trotz Antennenkontak- tes, hingegen nicht.

Acknowledgements

I wish to thank Prof. W. KLAUSEWITZ, Senckeriberg Museum, Frankfurt, for the identification of Cryptocentrus steinitzi, and Dr. Y. MIKA, Nagasaki University, Japan, for the identification of Alpheus purpurilenticulat~s. I am very grateful to Mr. J. WINKELFELD and Dr. C. KROPACH for their excellent photographs. I also wish to thank Drs. R. SZLEP, A. LESHNER, D. SAMUEL and H. SZECHTMAN for their critical remarks on the manuscript.

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Author's address: Dr. ILAN KARPLUS, Department of Isotope Research, Weizmann In- stitute of Science, Rehovot, Israel.

Documents

The Tactile Communication between Cryptocentrus steinitzi (Pisces, Gobiidae) and Alpheus purpurilenticularis (Crustacea, Alpheidae)