Signaling via Water Currents in Behavioral Interactions of Snapping Shrimp (Alpheus heterochaelis)

11 Pages·2001·4.9 MB·

by  Jens Herberholz

Reference: Biol. Bull. 201: 6-16. (August 2001)
Signaling via Water Currents in Behavioral
Interactions of Snapping Shrimp
(Alpheus heterochaelis)
JENS HERBERHOLZ1 * AND BARBARA SCHMITZ2
1Georgia State University, Department ofBiology, P.O. Box 4010, Atlanta, Georgia 30302; and
2LehrstuhlfurZoologie, TU Miinchen, Lichtenbergstr. 4. 85747 Garching, Germany
Abstract. The snappping shrimp Alpheus heterochaelis snapper claw on one (left or right) side and a small pincer
produces a variety of different water currents during in- claw on the other side in both sexes (Williams, 1984). The
traspecific encounters and interspecific interactions with snapper claw allows the animals to produce an extremely
small sympatric crabs (Eurypanopeus depressus). We stud- fastwaterjet(ofupto25 m/s; Versluisetal., 2000) by rapid
ied the mechanismsofcurrent production in tethered shrimp claw closure after cocking the claw in the open position
and the use of the different currents in freely behaving (Ritzmann. 1974). The high velocity ofthe waterjet results
animals. The beating of the pleopods results in strong pos- in a pressure drop below vapor pressure that causes a
mm
teriorly directed currents. Although they reach rather far, cavitation bubble to grow to a size ofabout 3.5 in front
these currents show no distinctions when directed toward ofthe snapper claw. The collapse ofthis bubble (and not as
different opponents. Gill currents are produced by move- previously supposed the mechanical contact of both claw
ments of the scaphognathites (the exopodites of the second surfaces) causes the extremely loud (up to 215 dB re 1 ;u,Pa
maxillae) and can then be deflected laterally by movements at 1 m distance; Schmitz, 2001) and short (about 500 ns)
ofthe exopodites ofthe first and second maxillipeds. These snapping sound (Versluis et al., 2000). The strong effect of
frequent but slow lateral gill currents are most probably the waterjet and the cavitation bubble collapse can be seen
used to enhance chemical odor perception. The fast and during interspecific encounters. Small prey (e.g., worms,
focused, anteriorly directed gill currents, however, represent goby fish,orshrimp)canbe stunnedoreven killedby thejet
apowerful tool in intraspecific signaling, becausetheyreach (MacGinitie, 1937; MacGinitie and MacGinitie, 1949; Mor-
thechemo- and mechanosensory antennules ofthe opponent ris etal., 1980; Suzuki, 1986; Downer, 1989), and interspe-
more often than any othercurrents and also because they are cific opponents (e.g., small sympatric crabs, Eurypanopeus
produced soon after previous contacts between the animals. depressus) can be injured at interaction distances of on
They may carrychemical information aboutthe social status average 3 mm (Schultz et al., 1998). Toward conspecifics
of their producers since dominant shrimp release more the water jet was not observed to cause any damage but
anterior gill currents and more waterjets than subordinate functions as a communicative signal (Herberholz and
animals in intrasexual interactions. Schmitz, 1999), both opponents ensuring an interaction
mm
distance of on average 9 (Schmitz and Herberholz,
Introduction 1998), which is far enough away from danger caused by
implosion ofthe cavitation bubble. This hydrodynamic sig-
Alpheus heterochaelis of the family Alpheidae (Deca- nal is analyzed by the receiving shrimp predominantly with
poda, Caridea) is one ofthe largest snapping shrimp, reach- the help ofmechanosensory hairs on the snapper claw, and
ing abody length ofupto 55 mm. It shows alarge, modified may contain information about the strength, motivation, and
sex ofthe snapper (Herberholz and Schmitz, 1998; Herber-
holz, 1999).
Received 27 November 2000; accepted 10 April 2001.
*To whom correspondence should be addressed. E-mail: biojhh@ The still rather small interaction distance of less than 1
panther.gsu.edu cm in agonistic encounters between two snapping shrimp
WATER CURRENTS IN SNAPPING SHRIMP 7
also favors the exchange of chemical signals between the visualize and quantify biological flow fields in lobsters and
opponents. The literature on chemical orientation and com- crayfish in a series ofexperiments by Breithaupt and Ayers
munication in snapping shrimp is limited: Hazlett and Winn (1996, 1998). Small floating particles ofthe samedensity as
( 1962) tested aggressive and defensive responses ofSvnal- seawater were added to the aquarium water and illuminated
pheus lu'inphilli to crushed male or female extract, and in a horizontal or vertical plane in the vicinity ofa tethered
Schein (1975) and Hughes (1996) investigated the choice of animal. Flow fields were then analyzed by tracking individ-
Alpheus heterochaelis toward extracts of male or female ual particles. It was shown that both lobsters and crayfish
water in Y-maze experiments without clear-cut results. On produce a great variety of flow fields by using the exopo-
the other hand, ablation ofthe chemosensitive antennules in dites of the maxillipeds and by fanning the pleopods. The
Alpheus edwardsii strongly reduced pair formation and sex latter was also discussed with respect to chemical commu-
recognition, which may bedue to impeded distant orcontact nication: male American lobsters commonly fan their pleo-
chemoreception since the pairing frequency remained high pods at the second entrance oftheir shelter, thus creating a
when only the antennae were ablated (Jeng, 1994). strong current that may contain chemical information about
The importance of olfactory signals during hierarchy the female positioned at the first entrance (Atema, 1985,
formation was shown in male American lobsters (Karavan- 1988). The pleopod fanning frequencies in males correlate
ich and Atema. 1998a). In these experiments, the recogni- with the frequencies of females checking the shelter. The
tion ofurine-carried chemical signals, which were received existence of pheromones that control female choice and
by the antennules, allowed the subordinate animal to avoid molting as well as male aggression was therefore assumed
the familiar dominant shrimp, and therefore reduced the (Cowan and Atema, 1990; Atema, 1995; Bushman and
duration and aggression offights. The exchange ofchemical Atema. 1997).
signals is also assumed to play a major role in individual The possibleexchange and use ofdifferent watercurrents
recognition and memory in male and female Homarus during agonistic encounters has rarely been studied; but see
americamts (Karavanich and Atema, 1998b; Berkey and Rohleder and Breithaupt (2000) for a preliminary study in
Atema, 1999). In lobsters, urine is released through a paired the crayfish Astacus leptodactylus. To test the possibility
setofnephroporeson the ventral sides ofthe basal segments that snapping shrimp use guided water currents as signals,
ofthe second antennae (Parry, 1960). Agonistic behavior in we visualized and analyzed all water currents that the
lobsters causes an increase in the probability and volume of shrimp produced during their encounters with conspecifics
urine release (Breithaupt etal., 1999). The released urine is ofthe same or different sex and in encounters with sympa-
then carriedby the powerful anteriorly directed gill currents trically living mud flat crabs (Eurypanopeus depressus).
and may therefore transfer chemical information from one
animal to another (Atema, 1985). In recent studies (Zulandt Materials and Methods
Schneider et al., 1999; Zulandt Schneider and Moore.
2000), chemical cues were also described as an important We analyzed the behavior of 12 adult specimens of
source for recognition of the dominance status or stress Alpheus heterochaelis. a species of snapping shrimp (6
condition of conspecifics in another crustacean, the red males, 6 females; body size: 3.9 0.4 cm. mean SD).
swamp crayfish (Procambarus clarkii). Each animal was tested in an encounter with a conspecific
In light ofthese examples, a similar mechanism ofchem- ofequal size of either the same or different sex, as well as
ical signal exchange via gill currents in snapping shrimp in an encounterwith a small crab (Eurypanopeusdepressus;
seems likely. We cannot, however, exclude the possibility mean length and width ofcarapace: 1.6 0.2 X 1.2 0.2
that the animals also exchange hydrodynamic signals. In cm, mean SD). All animals were caught in waters ofthe
fact, it has been shown that the antennules of crayfish Gulfcoast ofFlorida at the Florida State University Marine
(Mellon, 1996) and lobsters (Guenther and Atema, 1998; Laboratory near Panacea. Prior to the experiments the ani-
Weaver and Atema, 1998) are equipped with both chemical mals were labeled with small numbers designated for mark-
and mechanosensory receptors, and detailed morphological ing queen bees and were kept individually in perforated
studies of antennule sensory hairs favor the same situation plastic containers (1 1 X 11 X 15 cm) containing gravel and
in snapping shrimp (Schmitz, unpubl. obs.). Therefore, oyster shells for shelter. The containers were placed within
snapping shrimp may also perceive hydrodynamic stimuli a large tank (90 X 195 X 33 cm) with 330 1 ofcirculating
as well as chemical stimuli with their antennules. Previous filtered seawater (salinity: 23%c^28%o; temperature: 22-
studies (Herberholz and Schmitz, 1998. 1999) have shown 23C). Proteins were removed from the water, and pH.
that the transfer of hydrodynamic signals is realized by the carbonate, oxygen, CO2. and NO3 were regularly con-
powerful water jet that is formed by rapid closure of the trolled. The shrimp were exposed toan illuminationcycle of
largeclaw. Incontrast, the much weakergill currents appear 12 h light/12 h dark and fed frozen shrimp, fish, or mussels
to be more suitable for transferring chemical information. three times a week.
Suspended plastic particles were successfully used to For visualization of the different water currents, we pre-
J. HERBERHOLZ AND B. SCHMITZ
pared the aquarium water (temperature: 22-24"C, water Salmon (1970). In 11 out of 12 experiments, one animal
level: 5 cm) with small, floating plastic panicles (ABS- produced more aggressive acts and fewer submissive ones
particles, Bayer, Leverkusen, diameter: 500-710 jum; spe- than its opponent and was therefore determined to be the
cific weight: 1.03 kg/1). The aquarium (30 X 24 X 24 cm; winner while the opponent was determined to be the loser.
floor covered with black cloth to facilitate walking) was Statgraphics Plus 6.0 (Manugistics Group, Inc.) and
positioned on a platform isolated from vibrations (Breit- SPSS 6.0.1. (SPSS Science Software GmbH) were used for
haupt et at., 1995). At the level of the interacting animals, statistics. Mean and standard deviation were calculated for
the seawater was illuminated from one side by a slide each variable ofinterest foreach tested individual, and only
projector holding a slide with a thin horizontal slit. Before one value per individual (grand mean) is included in each
each experiment fresh seawater and particles were added, statistical test. The behavior of the respective opponents
and two animals (two snapping shrimp or one snapping (male and female snapping shrimp, and crabs) was not
shrimp and a crab) were placed in the aquarium for 10 min analyzed and is not included in our results (exception: data
for acclimatization: the animals were separated by an presented in Fig. 7). If not otherwise stated, the Friedman
opaque dividerto prevent visual, tactile, and directed-chem- rank test forrepeated measurements (sample size >2) orthe
=
ical contact. After the partition was removed, all interac- Wilcoxon rank test (sample size 2) were used, and values
tions between the animals during the following 20 min were with P < 0.01 and P < 0.05 are indicated in the text. We
videotaped from above (camera: Panasonic AG 455; video used nonparametric statistical tests because most ofthe data
AG
recorder; Panasonic 7355; monitor: Sony Trinitron). did not fulfill the requirements for the use of parametric
The reflexive characteristics ofthe suspended particles then tests i.e., normality or equal variance.
allowed a precise tracking using standard video-frame anal- To gain more insight into the mechanism of gill current
ysis. production and redirection, two snapping shrimp were teth-
Each experiment (interactions between two snapping ered upside down in a small petri dish filled with seawater
shrimp of the same or different sex or between a snapping and floating plastic particles, and the activity ofthe different
shrimp and a crab) was characterized by the number of mouth parts, which produced or deflected the currents, was
physical contacts between the opponents, regardless oftheir videotaped using a CCD camera (Sony XC-77CE) mounted
duration and strength, as well as by the number of water on a binocular microscope with high magnification. In ad-
jets. Three different water currents were characterized, in- dition, small drops of black ink (Brilliant Black 4001.
cluding a lateral gill current, an anterior gill current, and a Pelikan) were placed between the third and fourth walking
pleopod current (Fig. la). The pleopod current was mea- legs of these shrimp as well as of animals tethered dorsal
sured only when the shrimp was not in locomotion, because side up to a vertical holder and standing on a platform so
this current is also likely to be used in supporting the that the gill currents could be visualized. (Fig. Ib).
animal's walking. Moreover, nocurrent was included in our
analysis unless the single-frame video analysis gave clear Results
evidence that it had moved two or more plastic particles. Visualization ofwater currents in tethered shrimp
The following parameters were evaluated for all visualized
water currents: frequency, duration (time between onset of A unique feature of snapping shrimp is the production of
movement ofthe first floating particle and end ofmovement an extremely rapid waterjet by fast closure ofa specialized
of the last particle), range (total distance covered by an snapperclaw. Apart from thiswaterjet. the snapping shrimp
identified particle due to a certain current: possibly under- Alpheus heterochaelis is able to produce fourkinds ofwater
estimated when the current hit an opponent or an aquarium currents (Fig. 1), which can be subdivided into two main
wall), velocity and target of the currents, their potential to categories. Fanning of the pleopods causes a strong, poste-
transfer chemical information (i.e.. entering the area of riorly directed pleopod current, and a gill current is pro-
chemical perception at the receiver's side), the temporal duced by rhythmically beating the scaphognathites as re-
correlation between currents and previous physical contacts, vealed by our visualization experiments in two tethered
and the correlation between produced currents and water shrimp. Beating of the scaphognathites produces a depres-
jets in winners and losersduring intrasexual interactions. To sion in the gill chamber; water is therefore sucked into this
determine a winner or loser, we counted the number of chamber and subsequently released anteriorly through two
aggressiveactsand the numberofsubmissive acts aftereach small openings in the carapace. This "normal" gill current
physical contact between the conspecitic opponents can be visualized with ink in tethered animals, but it is too
throughout the encounter. Aggressive acts include behav- slow and weak to move floating particles and was therefore
iors such as approach, aggressive stance, and grasping and not analyzed during encounters of snapping shrimp and
openingoftheclaws. Submissiveacts include moving back- their opponents. It can, however, be accelerated and de-
wards and turning and tail flipping away from the opponent. flected into a lateral gill current (see Fig. IB) by the
These definitions are largely adopted from Nolan and exopodites ofthe second and third maxillipeds. The exopo-
WATER CURRENTS IN SNAPPING SHRIMP
'normal"gill current lateral gill current
pleopod current antennule
anterior current
gill
Figure 1. (A) Schematized drawing (lateral view) of a snapping shrimp modified after Kim and Abele
(1988)showingfourdifferentwatercurrents(grayarrows): the"normal"gillcurrent,the lateral gillcurrent,the
anteriorgillcurrent,andthepleopodcurrent.Blackarrowsshowthedirectionofwaterenteringthegillchamber.
(B)FrontalviewofanA/pheiishelerochaelissnappingshrimp,tetheredtoaverticalholderbymeansofaplastic
nutglued to the carapace and standing on a textile platform. Black ink was placed with a syringe between the
thirdandfourthleftpereiopods(seeinktrace)tovisualizethegillcurrents.Theshrimpisfanningtheexopodites
ofthe right second and third maxillipeds. thus producing an ink-stained lateral gill current to the right.
ditesofthe first maxillipeddo notparticipate in this process. right side. Tethered snapping shrimp never beat the exopo-
Fanning of the left exopodites results in acceleration and dites of both sides simultaneously, and this was also never
deflection of the released gill current to the left side, and observed during interactions in which the illuminated par-
fanning of the right exopodites results in deflection to the ticles were directed to only one side at a time. Interestingly,
10 J. HERBERHOLZ AND B. SCHMITZ
D 1-gc a-gc The duration of the different water currents (Fig. 3A)
tends to be longest for lateral gill currents, with no signif-
icant differences regarding the type of the opponent. The
duration of anterior gill currents is generally shorter, with
similar values in intraspecific interactions, yet almost twice
as long as in interactions with a small crab. Anterior gill
currents in interspecific encounters are significantly shorter
<
in duration than lateral gill currents (P 0.05). Pleopod
currents, in contrast, reveal very consistent values for all
types of interactions.
Figure 3B shows the range ofthe different currents in all
interaction types. Regardless ofthe opponent, the snapping
homo hetero inter shrimp tend to produce lateral gill currents with small
ranges. Anterior gill currents generally cover larger dis-
type of interaction tances in intraspecific interactions, whereas the mean value
is reduced in interactions with a crab. The most powerful
curFriengtu,rea-2g.c, aFnrteeqruieorncgyillofctuhrrreenetd,ifpfce,repnltewoaptoedrccuurrrreenntt)sp(1r-ogdcu,cleadterbaylgAill-l current is the pleopod current, which covers long distances
pliensheterochaelissnappingshrimpininteractionswithanothershrimpof in all interaction types. Range differences within interaction
the same sex (homo), ofdifferent sex (hetero), and with a Eurypanopeus types are significant atP < 0.05 andP < 0.01, respectively.
depressuscrab (inter). Grand means and standard deviations for 12 snap- The velocity ofthe watercurrents during the first 120 ms
tpyipnegsswhirtihmpP e<ac0h.01areareshionwdni.catSeidgnbiyfictawnotadsitfefreisrkesnc(e*s*)w.ithin interaction (6 video frames) was evaluated for 10 examples for each
current and interaction type (Fig. 3C). There are no signif-
icant differences in the velocities within and between dif-
fare(fealsyt)maonvtienrigorangiimllalcsu;rrietnctowulads nroesttrbiecteeldictioteedncionuntteetrhesreodf ctfhuererernestnltotwayepnsedtstvhoeeflopiclnietteoirpeasocdtiicnonusra.rlleTnethnecsohuloanwtteersraislm.igliTallrhecvuarlarnuetenesrtiaosnrhdogawirlsel
csahlr,imopr.viItssuaplrocdountcatcitonbeotbwvieoeunsltyheraeqnuiimraelss.phAyssicaalre,suclht,emwie- both more powerful than the lateral gill current. Initial
were not able to analyze the producing mechanism; that is, velocities are higher, but their analysis has not proved
we did not identify the involved mouth parts. s2a0timssfac(t5o0ryfbraemcea/uss)e.ofthe standard videotime resolution of
General characteristics ofreleased water currents
Temporal relation ofwater currents to physical contact
Encounters between two snapping shrimpofdifferent sex
(hetero) are characterized by a significantly higher number Figure 4 compares the frequency of water currents that
of physical contacts (23.9 8.3, /; = 287; P < 0.01) than were elicited within 10 s after a physical contact between
seen in encounters between two shrimp of the same sex the opponents with those that were "spontaneously" pro-
=
(homo; 13.8 6, n 165), or between a snapping shrimp duced that is, emitted more than 10 s after a preceding
and a crab (Eurypanopeus depressus) (interspecific; 12.7 contact. As shown in Figure 4A. in all interaction types the
5.3. n = 157). On the other hand, snapping (water jet lateral gill current is significantly more often produced
production) of the tested shrimp is significantly increased spontaneously than following a physical contact (P < 0.01).
after a contact with a crab (38% 16<7r; P < 0.01) when In homo interactions itoccurs in only 6.2% ofallcases (n =
compared to snapping after hetero and homo contacts (5% 10of 162) shortly afteracontact. During hetero interactions
4% and 11% 11%, respectively). this current is elicited by a contact in 11.5% of all cases
=
These differences in mind, we first evaluated the number (n 2\ of 183); in interactions with a crab, the lateral gill
ofwater currents (lateral gill currents, anterior gill currents, currents occur within 10 s afteracontact in only 8.5% ofall
=
and pleopod currents) in each experiment. Figure 2 shows cases (n 13 of 153).
that there are no essential differences between interaction The analysis of the anterior gill current reveals a com-
types (homo, hetero, or interspecific). Within each interac- pletely different frequency pattern, with more elicited cur-
tion type, however, the number of lateral gill currents sig- rents than spontaneous ones (Fig. 4B). In homo interactions
<
nificantly (P 0.01) exceeds thatofanteriorgill currents as the anterior gill current is produced in 65.5% of all cases
=
well as that ofpleopod currents. In addition, in interspecific (/; 19 of 29) within 10 s after a preceding contact.
encounters with a crab, the frequency of anterior gill cur- Similarly, in hetero interactions this gill current is elicited
=
rents is significantly lower than the frequency of pleopod by a contact in 62.5% of all cases (n 15 of 24). Finally,
<
currents (P 0.01). during interactions with a crab, anterior gill currents are
WATER CURRENTS IN SNAPPING SHRIMP II
released within 10 s after a contact in 78.6% of all cases
D =
1-gc a-gc pc <H 11 of 14).
25
In contrast, the pleopod current, like the lateral gill cur-
rent, is significantly more often (P < 0.01) produced with-
20
out an immediately preceding contact in all types of inter-
actions (Fig. 4C). During homo interactions we observed
u1 15 only 7.7% of pleopod currents within 10 s after the last
=
contact (n 4 of 52). In hetero interactions this current is
10 elicited in 16.7% ofall cases (n = 8 of48) by a preceding
contact, and in interspecific interactions there are 13.0% of
=
pleopod currents shortly after a previous contact (n 7 of
-a 54).
homo hetero inter
Possible chemosensory information transfer
by water currents
type of interaction
If any of the water currents were used to transfer chem-
B ical information, one would expect them to be directed
Dl-gc a-gc pc toward the chemoreceptive antennules ofthe opponent. We
20 therefore evaluated the number ofcurrents that reached the
area between the opponents' claws that is, an area mostly
covered by the flicking antennules. This was possible by
15
** ** analyzing the video sequences and identifying the area of
particle dispersion with respect to the animals' position. In
1 10 fact, only the anterior gill current seems qualified to fulfill
U the function of possible information transfer (Fig. 5).
* In all typesofinteractions, the mean numberoflateral gill
M 5 currentsthat missthe antennules is significantly higher(P <
0.01) than the mean number ofthose hitting the target (Fig.
5A). In homo interactions the lateral gill current reaches the
=
homo hetero inter antennule area in only 0.6% of the cases (/; 1 of 162).
During hetero interactions lateral gill currents are never
type of interaction directed toward the opponent's antennules, but hit other
=
targets (n 183). In interactions with a crab, the snapping
=
shrimp produce 0.7% (H 1 of 153) oflateral gill currents,
which could possibly transfer chemical information.
Dl-gc a-gc pc In comparison, a higher percentage of anterior gill cur-
10 rentsreaches the antennule area in all interaction types (Fig.
5B). During homo interactions the anteriorly projected gill
8 current reaches the antennules ofthe opponent in 35.1% of
=
all cases (n 10 of 28). In hetero interactions the percent-
=
6 age (66.7%, n 16 of24) ofanterior gill currents directed
I toward the antennules is even higher than that ofundirected
CJ 4 anterior gill currents. During interspecific interactions the
snapping shrimp projects 35.7% anterior gill currents to-
=
2 ward the antennules of the crab (// 5 of 14).
The frequency pattern for pleopod currents is similar to
<U
homo hetero inter
sex (hetero).andofasnappingshrimpandacrab(inter).Grandmeansand
standard deviations for 12 shrimp are shown in A and B; means and
type of interaction standard deviations ofthe velocity during the first 120 ms of 10 currents
Figure3. Duration (A), range (B), and velocity (C) ofthe lateral gill each are shown in C. A significant difference within an interaction type
current (1-gc). theanteriorgillcurrent(a-gc), andthe pleopodcurrent (pc) with P < 0.05 is indicated by one asterisk (*) and with P < 0.01 by two
ininteractionsoftwosnappingshrimpofthesamesex(homo),ofdifferent asterisks (**).
12 J. HHRBtRHOI
WATER CURRENTS IN SNAPPING SHRIMP 13
homo hetero
C
00
a-gc
of O^
^
number
to
14 J. HERBERHOLZ AND B. SCHMITZ
lobsters (Homarus americanus), the exopodites of the first currents; Fig. 2). Moreover, they are produced for long
maxillipeds do not contribute to these lateral gill currents in intervals but have a short range and a low velocity (Fig. 3).
snapping shrimp, whereas in crayfish (Procambarusclarkii) They are barely elicited by physical contact (Fig. 4A) and
these appendages are also involved (Breithaupt. 1998). hardly ever reach the antennules of their opponents (Fig.
The production mechanism ofthe fast anteriorgill current 5A). These properties of the lateral gill currents do not
remains unclear, since this behavior obviously requires change with different opponents but appear to result from a
physical, chemical, or visual contact during intra- or inter- stereotyped form ofproduction. Thus, obviously lateral gill
specific encounters ofsnapping shrimp, and thus was never currents are not predestinated to play a prominent role in
seen in tethered animals. From our knowledge about the active (chemical) signaling between the animals.
lateral gill current, we assume that the fast anterior gill Still, their function needs explanation. From our obser-
current is created by high-frequency beating ofthe scapho- vations we conclude that the lateral gill current is used to
gnathites without contribution ofthe exopodites ofthe sec- improve the shrimps' ability to sense possible odor signals
ond and third maxillipeds. Since it is difficult to video- that occurat close distance. By redirecting the "normal" gill
record the mouth parts with high magnification during current, the shrimp refreshes the area around its chemical
social interactions, we arecurrently testing othermethodsof receptors from its own smell (released by the slow and
monitoring scaphognathite beating frequencies during en- permanent gill current) and thereby improves the detection
counters to verify this hypothesis. of the chemical surrounding. This idea is supported by our
knowledge that Alpheus heterocliaelis naturally inhabits
Role ofthe fast anterior gill current during social small, oyster-shell-covered areas with little water flow and
interactions that individuals ofthe species appear to be rather stationary
mosTthesuarnparliyssiinsgoafntdheinfatsetreasnttienrgiorresguilltls.cuArrletnhtourgevheaalnetdertihoer wulaistteehdrianltogtihrlaletmcuaorrvreeeantw(aHptererorbdefurcrheoodmlzbtyhaensdnaarSepcaphiamnirgtozsu,hnrdpietmrhpse.saeonbetsm.es)n.ntuoTlhbeees
g(iAltlecmuar,ren1t9s85w.er1e99o5b)searnvdedcraanyfdiswhel(lBrdeeistchraiubpetd, i1n99l8o)b,stewres andto amuch lesserextent todraw watertoward that region
found decisive differences in snapping shrimp. First of all, as proposed for the posteriorly or laterally redirected gill
currents of lobsters and crayfish (Atema, 1995; Breithaupt.
Alpheus heterochaelis produces different types of anterior
griellleacsuerroenftsw.atTerh,ew"hniocrhmawla"sanstuecrkieordctuhrrroeungthisthaesgliolwl,cwheaam-k ow1ne99r8be)o.tnheIvnseircdoeonsbt.sraIesnrtsvtetedoadtl,oobtfshateneyrssbiemaauntldttachrneaeyeofxuiossplhoy,dwsiinttaehpspaoipfnpgoennsedharsgiiemdspe
bcdeuurrc,rteinaotsn,oowpfhpiotchsehedfoacsttcouatrnhsteedrfuiarostir,nggsiltlsrooccniugar,lreaninnttteeirrsiaocrrtaliryoends(i.FriegTc.htee2d)pgbrioul-tl aftroamtitmhee,oapnpodsittheeresiadreetnoowaorbdvitoheusanmiomvael'msenatntseroiforparretgiicolne.s
strongly linked to previous contacts with a conspecific or a
crab (Fig. 4B). Among the observed currents, only the fast Role ofpleopod currents during social interactions
anterior current is created shortly after a preceding contact,
In lobsters (Homarus americanus), pleopod currents are
regardless ofthe typeofopponent. In fact, this current never
occurred before the first contact. Moreover, we show that used for chemical (possibly pheromonal) communication
during courtship at a shelter (Atema. 1985. 1988. 1995;
only this current is suited to transfer chemical information Cowan and Atema, 1990: Bushman and Atema, 1997). The
towards the otheranimal (Fig. 5B): it reaches the antennules
of the opponent in nearly 50% of all cases. snapping shrimpAlpheus heterocliaelis, in addition tousing
psohnoOewfnsta.lslToahmneealnypuzecemudbleicraur,rirtedinuetrssa,twioiontnlh,yratenhsdepefrcaatsntgtaeonttieshreisomsrahlgrililemlrpcsui'rnroeepnn--t ptithlseypflsoeurbosapttortdaastcehfeod(rselagnogdcso,mouorsteimsountdhdaeynm-dsfatoonrdps)rheolvbtiaedcrekdwaiagngriodnxgyb,geefhaninnnsdiunpig-t
(Nolan and Salmon, 1970). These authors also mention
counters with a crab than in interactions with conspecifics
(Figs. 2, 3). We assume that the shrimp collect information (pleopod) fanning as an aggressive act, with a shrimp vig-
about the genus of their opponent and reduce the effort to orously beating its pleopods and directing a water current
communicate accordingly, if it is a crab. ppolsetoeproidorlfyanqnuiintge icslonsoettnootaendotbhyerNsohlrainmpa.ndThSealfmroeqnue(n19c7y0)o,f
but the behavior was described to occur between two fe-
Role oflateral gill currents during social interactions males at the entrance of a shelter. In our experiments, we
During social interactions between snapping shrimp and did not provide a shelter, and all shrimp were in the middle
conspecifics of the same or different sex as well as during of their molt cycle. In view of the finding that the actual
interactions with small crabs, the lateral gill currents are impact of pleopod currents in lobsters depends to a high
most prominent and significantly outnumber all other ob- degree on the molt state of the animals as well as on their
served currents (i.e., pleopod currents and fast anterior gill readiness to mate (Cowan and Atema, 1990), these condi-
WATER CURRENTS IN SNAPPING SHRIMP 15
tions may have affected our results. Though pleopod cur- In any case, the production ofthe fast anteriorgill current
rents were ratheroften produced (Fig. 2) and(in comparison may play a critical role during hierarchy formation in snap-
togill currents) show an averageduration, a largerange, and ping shrimp. We show that in intrasexual encounters the
high velocity (Fig. 3). there is a lack of correlation with numbers of water jets and anterior gill currents are posi-
previouscontacts (Fig. 4C) andalow precision in hitting the tively correlated (Fig. 6) and that both are significantly
antennules ofthe opponent (Fig. 5C). There are hardly any higherin the winnerthan in the loser (Fig. 7). In the present
differences in the characteristics of these currents towards study, winner and loser met in only a single 20-min exper-
different opponents. All this indicates that pleopod currents iment. Preliminary experiments show that repetitive pairing
are of little relevance for (chemical) signaling or commu- ofwinners and losers reduces the number ofwaterjets and
nication among snapping shrimp and between shrimp and anterior gill currents (Obermeier and Schmitz. unpubl.).
sympatric crabs under our conditions. This supports the finding that these behaviors are most
probably correlated with dominance and social status in
A specialized gill currentfor chemical .signaling and snapping shrimp. Although the strength of the water jet
communication? represents the strength of the animal (see Herberholz and
Schmitz, 1999), the signal transferred by the gill current
The transfer ofchemical signals between interacting lob- may then allow recognition ofthe sender. This, in turn, can
sters (see e.g., Atema. 1995; Bushmann and Atema. 1997) prevent two Alpheus heterochaelis shrimp of the same sex
and crayfish (Breithaupt et al., 1999) has been described in from engaging in more severe fighting during subsequent
detail. In lobsters these signals can evoke long-term indi- encounters, thus reducing the number ofthe "costly" water
vidual recognition (Karavanich and Atema, 1998a, b), and jets.
in crayfish they communicate dominance status or stress
condition (Zulandt Schneider et al., 1999; Zulandt Schnei- Acknowledgments
der and Moore, 2000). In all cases, urine-borne signals were
assumed to be the source ofchemical signaling (Breithaupt We would like to thank Maren Laube for help in data
et al., 1999; Breithaupt, pers. comm.). Since the urine is analysis. The experiments comply with the current laws of
released through a paired set of nephropores on the ventral Germany. Supported by a grant of the Deutsche For-
sides of the basal segments of the second antennae (Parry. schungsgemeinschaft (Schm 693/5-2). The work of J.H.
1960). it can be carried toward an opponent by the anterior was additionally supported by a NIH grant (NS26457) to
gill current. Moreover, agonistic behavior in catheterized Donald H. Edwards at Georgia State University.
lobsters increases the probability and volume of urine re-
lease (Breithaupt et al., 1999). Literature Cited
In the present study we show for the first time that the
Atema,J. 1985. Chemoreceptionin the sea: adaptationsofchemorecep-
pattern of water current production actually changes with torsandbehaviourtoaquaticstimulusconditions.Soc.Exp.Biol. Svm/.
respecttothe social situationofanaquatic animal. Although Ser. 39: 387-423.
snapping shrimp have the ability to produce "normal" an- Atema,J. 1988. Distribution ofchemical stimuli. Pp. 29-56 inSensory
taenrtieorriogrillyldciurrercetnetds,giltlhceuyrrcernetasteshdoirftfleyreanftt,ermcoonrteacptoiwnegrtfhueli,r AteWBmia.o,/NoJ..gvT1a9ov9fo5lA.gqau,aCtheidecsm.AincSiapmrlailnssig,genraJ.lVseAritlneamgt,hae,NmRea.wriRnY.eorFekany.v,irAo.nmNe.ntP:opdpiesrpe,rsaanld,
interaction partner. These elicited currents are then more detectionand temporal signal analysis. Proc. Nail.Acad. Sci. USA 92:
likely to reach the opponents' area ofchemical perception. 62-66.
The same may hold true for lobsters and crayfish, but their Berkey,C.,andJ. Atema. 1999. Individual recognition and memory in
currents have not yet been quantified during social interac- Homarus americanus male-female interactions. Biol. Bull. 197: 253-
tions. On the other hand, we still have to prove that the fast 254.
Breithaupt, T. 1998. Flow generation by specialized appendages in
anterior gill current in snapping shrimp actually carries lobsters and crayfish. Pp. 185-186 inBIONA-Repori 13. R. Blickhan.
chemical signals toward the opponent. Although the data A. Wisser, and W. Nachtigall. eds. Gustav Fischer Verlag. Stuttgart.
presented favor this assumption, we cannot exclude the Breithaupt.T..andJ.Avers. 1996. Visualizationandquantitativeanal-
pcousrsriebnitlsitpyartthiactiphaytderiondytnheamciocmmsuignniaclasttiroannsfbeertrweedebnytthheeagniil-l ZyHsaoirostplloiafnneb.kitooJl.no:gEi.cSaelPnufsrlocoerlwyl.fEiecalondlsdougsDyi.nagLn.sduMsPaphceymnsidileoldlaopnga,yr,tiecdPls.e.s.HG.Popr.Ldeo1nn1z,7-B1Dr2.e9acKih.n
mals. Judging by their sensory equipment, snapping Publishers. Amsterdam.
shrimp like crayfish (Mellon. 1996) and lobsters (Guen- Breithaupt, T.,andJ. Avers. 1998. Visualization and quantification of
therandAtema, 1998; Weaverand Atema. 1998) are most biological flow fieldsthroughvideo-baseddigital motion-analysistech-
likely to perceive hydrodynamic stimuli as well as chemical niques. Mar. Fi~esln\'. Bt'lniv. Phvsiol. 31: 5561.
stimuli with their antennules (Schmitz, unpubl.). We plan to Breittahtiaounpto,fT.c,raBy.fiSschhm(iPtrzo,caanmdbaJr.usTauctlzar.ki1i9)95t.o sHwyidmrmoidnygnamfiischorpireeny-.
test this possibility by deactivating the chemical receptors J. Comp. Physio/. A 177: 481-491.
only. Breithaupt,T.,D. P. Undstrom,andJ.Atema. 1999. Urinerelease in