Concurrent Signals and Behavioral Plasticity in Blue Crab (Callinectes sapidus Rathbun) Courtship

9 Pages·1999·4.2 MB·English

by  P J Bushmann

Reference: Biol. Bull. 197: 63-71. (August 1999)
Concurrent Signals and Behavioral Plasticity in Blue
Crab
(Callinectes sapidus Rathbun) Courtship
PAUL BUSHMANN*
J.
Smithsonian Environmental Research Center. 647 Coulee's WharfRoad, Edgewater, Maryland 21037
Abstract. Behavioral flexibility and behavioral regulation crab courtship, chemical signals from other sites appear to
through courtship signals may both contribute to mating carry sufficient information to elicit a full range of behav-
success. Blue crabs (Callinectes sapidus} form precopula- ioral responses in males and females.
tory pairs after courtship periods that are influenced by
female and perhaps male urine-based chemical signals. In Introduction
this study, male and female crabs were observed in 1.5-in
circular outdoor pools for 45 min while the occurrence and Courtship and mating success depend upon correct be-
sequence ofcourtship behaviors and pairing outcomes were havioral responses by both males and females. One might
recorded. These results were then compared with trials in expect a degree of plasticity in these behaviors (Hazlett,
which males or females were blindfolded; lateral antennule 1995). Because behavior can quickly track changes in en-
(outer flagellum) ablated; blindfolded and lateral antennule vironmental conditions (West-Eberhard, 1989). flexibility in
ablated; or had received nephropore blocks. The relative the occurrence and timing of reproductive behaviors might
importance of visual and chemical sensory systems during help insure successful mating. Many invertebrates do ex-
blue crab courtship were then determined and urine and hibit plasticity in their behaviors (Carlson and Copeland.
non-urine based chemical signals for both males and fe- 1978; Dejean, 1987; Elner and Beninger, 1995) and this
males were examined. Courtship behaviors varied consid- variability may be the rule for most animal species (Lott,
erably in occurrence and sequence; no measured behavior 1991).
was necessary for pairing success. Male or female blind- Conversely, one might also expect courtship and repro-
folding had no effect on any measured behavior. Males and ductive behaviors to be controlled and regulated by conspe-
females required chemical information for normal courtship cific communication signals. By eliciting appropriate be-
behaviors, yet blocking male orfemale urine release did not havioral responses, these signals could enhance mating
affect courtship behaviors. Males required chemical infor- success and help to prevent interspecies mating. Courtship
mation to initiate pairing or to maintain stable pairs. Male and mating in a fluctuating environment could be aided by
urine release was necessary for stable pairing, suggesting multiple or redundant signals, which would make the trans-
that male urine signals may be involved in pairmaintenance mission of adequate and correct information more likely.
rather than pair formation. Females that could not receive Multiple or redundant signals have been found in both
chemical information paired faster and elicited fewer male invertebrate and vertebrate species (van den Hurk and Lam-
agonistic behaviors. The results demonstrate a great vari- bert. 1983; Linn </ /., 1984; Rand et /., 1992).
ability and flexibility in blue crab courtship, with no evi- Chemical communication signals appear to be nearly
dence forstereotypedbehavioral sequences. However, these universal in the animal world. For aquatic crustaceans,
behaviors appear regulated by urine- and nonurine-based chemical communication signals have been well docu-
redundant chemical signals emanating from both males and mented in courtship and reproduction (Ryan, 1966; Atema
females. Although urine-based signals play roles in blue and Engstrom, 1971; Bales, 1974; rev. in Dunham. 1978,
1988; Gleeson, 1980; Borowsky, 1984, 1985), while visual
Received 30 March 1998; accepted 1 June 1999. (Christy and Salmon, 1991) and acoustic (Salmon and
*Current address: Anne Arundel Community College, 101 College Horch, 1972) signals have received less study. Recent stud-
Parkway. Arnold. MD 21012. E-mail: [email protected] ies with a variety of animal taxa have begun to examine
63
64 P. J. BUSHMANN
multiple signals and signal interactions (Hazlett, 1982; chemical signal has not been firmly established, although
Waas and Colgan, 1992; Stauffer and Semlitsch, 1993; Gleeson (1991) showed female attraction to water that con-
Hughes, 1996). tained males and Gibbs (1996) demonstrated disruption of
Like many crustaceans (Hartnoll, 1969), the blue crab pairing with male antennule ablation.
Callinectes sapidn.\ Rathbun practices a polygynous mating In this study, the occurrence and variability of courtship
systeminvolving acomplexcoordination offemale ecdysis, behaviors observed during blue crab pair formation were
maturation, and copulation. The mating process has been examined. These behaviors were then compared with those
well described (Hay, 1905; Churchill, 1921; Van Engel, generated by male and female pairs with vision, distance
1958; Gleeson, 1980). Immature females nearing their final chemoreception, both senses, or urine release impaired.
maturational molt, termed prepubertal females, are ap- This allowed a determination of the relative importance of
proached and courted by mature males. Pairing success visual andchemical sensory systems during blue crab court-
results in females being held beneath males in a "cradle ship and an examination of urine- and nonurine-based
carry" posture for a period ofprecopulatory guarding. They chemical signals for both males and females.
are released fortheirmolt, matedwhile still soft, andcarried
again for a period of postcopulatory guarding. This latter Materials and Methods
guarding protects the female while she is soft and prevents Adult male crabs (125 mm-170 mm carapace width)
subsequent inseminations by other males (Jivoff, 1997a). were collected from the Rhode River, an upper Chesapeake
Females are thought to receive only one copulation in their Bay subestuary, with baited commercial crab traps. Premolt
lifetime while males mate repeatedly (Van Engel, 1958), prepubertal females (96 mm-127 mm carapace width) were
although multiple inseminations are possible and occur oc- purchased from two local businesses which hold molting
casionally (Jivoff, 1997a). females for the soft crab industry. Females ranged in molt
emaactBhelupeahtatcrsraeactbaiocnpo,ruercptiassihreipsfiogrcnmaaanltiinbogen,sdyiasvntidedmepdawiorinutmloaditnshtreeeenemanpichmeap.soersI:-n swintaatfgeleroafttrainonkmgslcfaaotgreensDoimntootrhDee3tRh(haDnorad4ce8h.hRi1bv9ee3fr9o)r.oerApfnalritomiwac-litpshartwoieuorngehinhsetelhade-
tantto help insure mating success. The coupling ofmolt and
study.
reproductive condition requires individuals to ascertain the Behavioral interactions were observed in outdoorcircular
physiological state of prospective partners. Signals can pools (150 cm d. X 20 cm h.) with three centimeters of
function in the reduction ofagonistic behaviors (Tinbergen, washed river sand as substrate. Prior to a trial, pools were
1953; Bastock, 1967), and during mating female blue crabs filled with 15 cm of new river water filtered through a felt
must in some way guard against injury or death by aggres- bag with 10 /nm mesh. A trial began by randomly selecting
qsiuveen,cecasnnmiibgahlti,stitchermeafloerse., Rbeeprtiogdhutclytirveegubleahtaevdiobryscaonmdmuse-- aa rmaanledocmrlaybsaenldecptleadcipnrgephubiemrtianltofaempaoloel.wTaesnplmaicneudteisntloattehre,
nication signals, making appropriate responses more likely middle of the pool, inside an opaque plastic cylinder de-
and increasing the eventual mating success of the partici- signed to prevent interactions prior to the start of the trial.
pants (Ryan, 1990; Reynolds, 1993). After 10 min acclimation, the cylinderwas removed, allow-
Chemoreception and vision are the two best studied sen- ing the animals to freely interact. Three pools were started
sory modalities in blue crab courtship. Teytaud (1971) re- and watched simultaneously, and the ensuing behaviors
ported a role for visual signals in male recognition by were recorded by hand for45 min. Carapace width and molt
pre-pubertal females. However, Gleeson (1980) showedthat stage were recorded for each animal.
males did not respond to female visual stimuli alone, and Priortotrialseitheramaleorafemale fromeachpairwas
pairing could proceed in darkness. Chemical signals are subjected to an experimental treatment. They were as fol-
important tor both male (Gleeson, 1980) and female
lows:
(Teytaud, 1971; Gibbs, 1996) mate recognition. Some ma-
ture males respond with a courtship display to chemical 1. Nephropore Occlusion: Blue crabs possess bilateral
compounds in pre-pubertal female urine (Gleeson, 1980; nephropores, located anteriorly andjust ventral to the
Gleeson et al., 1984) and reception of these chemical sig- eye stalks. Each opening is found in a pit in the
nals occurs via the aesthetasc sensilla on the lateral filament carapace. A chitinous flap opens to allow urine toexit.
(outer flagellum) of the male antennules (Gleeson, 1982). A modification of a successful cannulation technique
This signaling theme appears common in crustaceans: urine was used to prevent urine release. Each pit was first
carries chemical courtship signals (Ryan, 1966; Bushmann dried by blotting and a drop of acetone, then filled
and Atema, 1997; Bamber and Naylor, 1997) and the an- with a viscous cyanoacrylate glue. The glue was im-
tennules appear to be the site of distance chemoreception mediately hardened with a catalytic accelerator. This
(Ache, 1975; Ameyaw-Akumfi and Hazlett, 1975; Devine sealed the nephropore flap shut. Animals were oc-
and Atema, 1982; Cowan, 1991). The presence of a male cluded 30 min prior to a trial. The blocks were
CONCURRENT SIGNALS IN BLUE CRABS 65
checked for a tight bond with the carapace immedi- Comparisons of the intact and sham-treated groups
ately before and after a trial, n = 12 males (M: showednodifferences in the frequency ofoccurrence ofany
URINE). 14 females (F:URINE). measured behavior or pairing outcome. These two groups
3. Antennule Ablation: the distal lateral filament (outer thus appeared to represent samples of the same population
flagellum), containing the aesthetasc sensilla, of both and their data were pooled to yield 22 intact control trials.
antennules was removed, n = 12 males (M: Behaviors of these pairs were examined to determine a
ANTENN), 12 females (FiANTENN). normal range of behavioral variability and sequence. Be-
4. Blindfolding: two strips ofblack plastic (50 X 10mm) haviors were scored once if they occurred in a given trial.
were fastened with cyanoacrylate glue to the dorsal The number of trials in which behaviors occurred for the
and ventral carapace so that each wrapped over and intact control group was then compared with those gener-
covered an eye stalk, n = 13 males (M:BLIND), 12 ated by the treatment groups. Overall differences between
females (F:BLIND). treatment and control groups were evaluated with a Chi-
5. Antennule ablation and blindfolding: animals received square test for multiple independent samples (Siegel and
both antennule ablation and blindfolding treatments. Castellan. 1988). Where significance was found, differences
n = 12 males (M:ANT-BLIND). 12 females (F:ANT- between specific treatment groups and the control were
BLIND). evaluated with a Fisher exact test (FAT) (Siegel and Cas-
6. Sham treatment: both animals in a pair were subjected tellan, 1988). The mean times between trial start and both
to sham operations. Antennules were held with for- the first behavioral interaction and Initiation ofPair For-
ceps without ablation, nephropores were treated with mation were also compared between the control and treat-
acetone and accelerator but not glued, and blindfolds ment groups. Overall differences were evaluated with anal-
were attached similarly, but lateral to the eye stalks so ysis of variance (Jaccard. 1983), while mean differences
that vision was not impaired, n = 10. between specific treatments and the control were evaluated
7. Intact: No treatments or sham operations were per- with a non-directional r-test (Jaccard, 1983).
=
formed on either animal, n 12.
Results
Blue crab reproductive and agonistic behaviors have been
well described over the years (Churchill. 1921; Van Engel, Male and female bluecrabs in intactcontrol pairs showed
1958; Teytaud, 1971; Jachowski. 1974; Gleeson. 1980). great variability in the occurrence oftheirbehaviors. During
This study analyzed one agonistic and five reproductive courtship, no behavior occurred with a high frequency (Ta-
behaviors. These behaviors were common, unmistakable, ble I). Male Strike, Male Display, Female Present and
and reliable indicators of the nature of the interaction oc- Female Rock occurred in only 41. 41, 56, and 36 percent of
curring. They were: intact control trials, respectively. Pairing was initiated at a
high rate, however (82% of trials), with 50% of trials
1. Male Strike: an agonistic behavior in which the male resulting in Stable Pair Formation. No single behavior
strikes or seizes any female body part with either more likely led to the initiation ofpairing or stable pairing,
2. cMhaelleaeDiwsiptlhaovu:tAsucbosuerqtusehniptbaethtaevmipotrs iantwchraidclhetchaerrmya.le cnoormedsid(TtahbeleexhI)i.bTihtieorneowfasannyobseihnaglveiosreqpureenccleudoeftbheehsaevioourts-
raises high on his walking legs, spreads his chelae
laterally, and raises and rotates his 5th walking legs
(periopods) laterally. Table I
3. Female Present: a courtship behavior in which the Fret/iiencvofcoiin.\lui> unclagonistic behaviors in intactblue crah
female faces away from the male and holds her body pairs. The numberoftrials in which each behavioroccurred is shown
in a cradle carry posture, with or without spread forall trials, those trials in which Initiation ofPair Formation occurred,
chelae. andthose trials in which a stablepairwasfanned
4. Female Rock: a courtship behavior in which the fe-
male rocks her body from side to side. Trials (%) with Trials ('',', ) with
Imitation of Stable Pair
5. Initiation ofPair Formation: the male seizes the fe- Occurrence in Pair Formation Formation
male and attempts to pull her into a cradle carry Behaviors 22 trials (%) (n = 181 (n = 111
position. Females often resist, males may make many
attempts, and pairing may or may not become estab- Male Strike
lished.
6. Stable PairFormation: this was scored at the end ofa
trial. Pairs were in stable cradle carry if both female
and male struggling had ceased, and the animals had
been paired for at least 10 min.
BUSHMANN
66 P. J.
(FAT, P = 0.009) (Fig. 2C). Thisbehaviorwasalsoreduced
by male antennule ablation (FAT, P = 0.001). Female Rock
(Fig. 2D) was reduced in incidence when females were
antennule ablated and blindfolded (FAT, P = 0.009): fe-
male antennule ablation alone did not significantly reduce
the occurrence of this behavior (P = 0.083). Female Rock
also occurred less frequently when males were antennule
ablated and blindfolded (FAT, P = 0.009). Male or female
nephropore occlusions or blindfolding had no significant
effect on either female courtship behavior.
Initiation ofPairFormation occurred frequently (80% of
trials) in the intact control group (Fig. 2E). There were
significant overall differences between groups in the occur-
rence of this behavior (x2 = 34.8, P < 0.05). It occurred
Figure 1. Flowchartshowingbehavioral pathwaysfromfirstencoun- significantly less often than the control group when males
ter, through courtship and/or male agonistic behavior, to stable pairing were antennule ablated (FAT. P = 0.007), while the reduc-
success or failure. The circled numbers represent the number of trials tion for antennule ablated and blindfolded males ap-
following that particular pathway. proached statistical significance (P = 0.062). Examination
ofstable pairing atthe trials' conclusions showed significant
that predominated, nor any single sequence that invariably overall differences between treatment groups (x2 = 31.36,
led to greater or lesser pairing success. Neither male or
fmeomlatlestacgoeur(tesahrilpy bperheamvoilotrsDwevrs.e lcaotrereplraetmeodltwiDth?)foermatlhee 18000 , MaleDisplay
relative sizes of males and females. 60 lUul
40
However, some general trends emerge from courtship 20 I-
sequences examined together with male agonistic behavior 100 MaleStrike
(cFoiugr.ts1h)i.pMboeshtavpiaoirrssp(r1i8orofto2p2a)irexfhoirbmiatteidonso(mx2e=se8q.u9e1n,cPe o=f 864000
0.003). The presence of male agonistic behavior signifi- 20 1 1 !..
cantly reduced the likelihood of stable pairing (FAT, P = |g 100 FemalePresent
0.040). Of the nine pairs in which males exhibited Male 8 80
60
Strike, only two (22%) formed stable pairs. Of the remain- 40 I.
ing 13 pairs in which males did notexhibitMaleStrike, nine X 20o
(69%) formed stable pairs (Fig. 1 >. z 1 FemaleRock
Examination of male agonistic and display behaviors Ig 8600
revealed overall differences between treatment and control 1 "0
groups (x2 = 20.45. P < 0.05; r = '7.62, P < 0.05). The 20
incidence of Male Strike was significantly diminished j2/i 100 InitiationofPairFormation
(FAT, P = 0.009) if females were antennule ablated (F: >- 6800
ANTENN) (Fig. 2A). Scores for females antennule ablated 40 h.lillll
20
and blindfolded (F:ANT-BLIND) closely approached sig-
nificance (FAT, P = 0.050). Male Display was significantly 100 StablePairFormation
80
reduced when males were antennule ablated (M:ANTENN) 60
(FAT, P = 0.009) or antennule ablated and blindfolded 40 Illllllll
(M:ANT-BLIND) (FAT, P = 0.049), but were unaffected 20
by female or male nephropore occlusion (F:URINE or M:
URINE) (Fig. 2B). Blindfolding alone (M:BLIND and
F:BLIND) had no effect on any measured behavior.
Treatments
When the behaviors Female Present and Female Rock
were examined, there were significant overall differences Figure 2. The percentage oftrials in which Male Strike. (2A). Male
0b.e0t5w;eexn2 tr=ea2t0m.e2n.t Pand<co0n.t0r5o)l. gTrhoeupsinc(ixd~en=ce45o.f78F,emPal<e cDFoionsrtpmrlaoaltyioa(n2nBd)(,2tEr)F,eeamtaamnlednetSPtragebrsloeeunptsP.a(i2rDCi)F,fofreFmreeamntacileoesnRb(oe2ctFk)we(oe2cnDc)u.irnrItenadicttifaoctroinotnthreoolfinPtaaanicdrt
Present was reduced when females were antennule ablated treatment groups were evaluated with a Fisher exact test. Stars indicate
(FAT. P = 0.035) or antennule ablated and blindfolded statistical significance at a = 0.05.
CONCURRENT SIGNALS IN BLUE CRABS 67
insect species have shown greater flexibility, with individ-
uals basing their behavioral responses upon current condi-
S 16
i ,. tions and context (Carlson and Copeland, 1978; Dejean,
1987).
Similarly, the behavior ofmany crustacean species is not
based upon stereotyped responses but instead shows great
plasticity and can be modified as context changes (Ra'anan
andCohen, 1984; Finerand Beninger, 1995; Hazlett, 1995).
O 20
The current study demonstrates such flexibility in Calli-
nectes sapidus courtship behavior. Courtship is variable in
o 12 that no single behavior must occur, nor does any behavior
invariably lead to successful pairing. No single behavior
occurred more than approximately half the time, yet the
odds ofsuccessful pairing remained high. This suggests that
courtship follows multiple behavioral pathways, all poten-
tially leading to successful pair formation. Such flexible
courtship would be useful for both males and females in a
species that mates in a fluctuating estuarine environment.
PaiFrigFuorrema3.tioMnea(3nB)lifmoertothfeirsitntoabcstecrovnetdroblehaanvdiortr(e3atAm)enatndgrInoiutpisa.tioBnarosf With intense male competition for females (Jivoff, 1997b)
represent mean standard error. Differences between intact control and and only one chance for females to receive sperm, it max-
treatmentgroupswereevaluatedwithanon-directionalt-test.Starsindicate imizes the chances of an encounter producing pair forma-
statistical significance at a = 0.05. tion, with eventual mating and reproductive success.
However, blue crab mating behavior is not without con-
Pwer<e0a.n05t)e.nnFuelewerablpaatiersd w(eFrAeT,staPble=(F0i.g.0126)F)oirf tahnetemnanluelse sdtirsapilntasyeadndsormegeulcaotuirotns.hIinptbheehainvtiaocrtscopnritorroltogrpoauirpfmoorsmtatpiaoinr,s
aswtbealrbaelteeodcpaacnilrduidbnegldinw(daFfsoAlTda,eldsPo(F=rAeTd0,u.c0Pe1d6=).w0hT.e0h0in2s).mwaaTlsheetniheencpoihdnrelonypcoesrieogsf- patmarnaiedlraeitmnmagae.lgnegtTrahtegrisoissanliisosd,tneiimclodlnuubssrettihrrnaaagtvteiseocsrotuhrretethdresouhliciepemdtphaotanrhtdte,aclnoitcmkoemeguleointfhhioecorcadotnwoitifrotonshltlasitbinlhgege-
nificant effect observed with any nephropore occlusion. nals often serve in this regard (Tinbergen, 1953). For blue
An examination of the mean time between a trial's start crabs, the most likely path to successful pairing, and there-
dpainfd=fetrh0ee.n0fc0ier9ss)t.boebTtshweeerevmneedtabrneehatatimvmeienotrtog(Frifogiur.spt3sAb()ehAsaNvhioOowVreAdwasFsig=nsiifg2in.ci7af3ni,t- dfourcTeehdesumcactleresesafatugmlgernetrsespirtoornid.aulcstiosnu,ggeisntvolvbeeshavcioourratlshipregaunldatiroen-
cOfafaovennlemdtdralealaydlenlstl(teedsnwi=snefurft2leeh.era9en7ana,ncbttelhPesaent=newcudoeln0rt.e(er0to2afl6=b)ol,gua2rntw.ode2hud8ep(,n(AtwPmNh=aeOl=nVe3sA.m06.aw90leF,3er2se)=P,wbel2=a.irn2ned9d0,f.bwo0lPl0hid1nee)d=n.d- tcmPsohaahurilororewtuesFgahdhoinrpdcmrheaemdatmauniilcdoceenadlpacaihnicnedrosmimtniSamgctn.uaacnblelisMecasaiolPtgfeanisiaoMrlnasFlwsoiepitrlghmanDayaitlsaispibolmlnaapa.nyot,dreFtdtoaIhnnraaitttntithbraeeootnlitmneohausnllfeeeio,s-nf
0.030) when the time between trial start and Initiation of loss ofdistance chemoreception affected behavioral expres-
PairFormation was evaluated (Fig. 3B). In this comparison sion and directly reduced courtship success. The relevant
coannlty rtehdeucfteimoanleinatnitmeenn(utle=-a3b.l9a0t,edPtr=ial0s.0s0h1)o.weTdimaesdiigfnfiefir-- curhienmei,chaolwienvfeorr,mabteicoanusdeidfneomtalseesewmittohroecscilduedseodlenleypihnrofepmoarlees
ences between the male blindfolded group a=nd the iPntac=t induced male behaviors at frequencies similar to intact
controls closely approached significance (t 2.01, controls. Although the results were less clear, females also
0a.b0l6a)t,edwhgirloeupthwoesreefnorotthseignmiafliecanbtli(ntd=fol1d.e4d6,aPnd=an0t.e1n7n0u)l.e waphpeenartehdeirtoanetxehinbniutlefsewweerreinasbtlaantceed,s wohficloeurptaisrhiinpgbienhiatviaitoirosn
or stability was unaffected. The physical act of pairing is
Discussion
initiated by the male, and evidently an antennule-ablated
Arthropod behavior has generally been considered ste- female is still attractive to males. However, an unreceptive
reotyped. Studies of some insects, such as many moth female can likely flee and decline pairing in the wild.
species, have demonstrated stereotypic courtship behavior: Blocking male urine release had no effect on female court-
specific chemical signals elicit specific and predictable re- ship behaviors, again suggesting that the relevant chemical
sponses (Kaissling, 1979; Charlton and Carde, 1990). Other compounds are not restricted to urine.
68 P. J. BUSHMANN
Itis now generally recognized that many chemical signals impaired. Male antennule ablations must alter male behav-
are mixtures or blends and thus can serve as multiple or iorsorcommunication signals in away that makes them less
redundant signals (van den Hurk and Lambert. 1983; Vetter attractive to females and less capable of inducing female
and Baker, 1983; Linn < t al. 1984). In blue crabs and other courtship behavior. This is consistent with field work
brachyurans, a chemical signal in female urine that induces (Gibbs, 1996) demonstrating that antennule-ablated males
male courtship behavior has been well described (Ryan. in crab traps are less able to attract prepubertal females.
1966; Gleeson. 1980; Seifert. 1982; Bamber and Naylor, There is evidence for an obligatory male urine-based
1997). The present study does not refute the existence of signal involved in pair maintenance during precopulatory
this signal, but rather suggests urine is only one source of guarding. When male nephropores were occluded, initiation
courtship signals and is not obligatory for the initiation of of pair formation was not affected yet there was reduced
male or female courtship behaviors. There appears to be incidence of stable pairing. This was the only evidence for
chemical information from non-urine sources capable of a urine-based signal in this study. However, female anten-
eliciting the same behaviors when nephropores are oc- nule ablation did not reduce the incidence of stable pair
cluded. It is only when all chemical signals are lost through formation. It is possible that the direct contact involved in a
antennule ablation that behavior is negatively affected. cradle carry produces other avenues for signal reception,
These statements appear at odds with Ryan's (1966) work such as contact chemoreceptors on the dactyls orelsewhere
showing no male responses to seawater that had contained on the exoskeleton (Fuzessery and Childress, 1975). Al-
nephropore-blocked premolt Portiimis sanguinolentus fe- though the observed reduction in stable pairing could have
males. It may be that the relevant female P. sanguinolentus resulted from some male trauma associated with the occlu-
signal is sent only in urine. In addition, the females in sion procedure, occluding females produces no such pattern
Ryan's study were isolated in 8-1 buckets during signal and blue crabs and lobsters appear capable of suspending
release, while females in the current study were placed in urine release for periods of several hours without ill effect
largertanks in the presence ofamale. This more naturalistic (Bushmann. unpub. data, Breithaupt and Atema, 1993).
behavioral context may have elicited female nonurine signal Visual signals seem to play no role in influencing court-
release and male responses not seen in the earlier study. ship behaviors oroutcomes. Blindfolded males and females
Lastly. Ryan used molten paraffin rather than glue as courted, received courtship, and paired with success rates
blocks; this may have affected the animals differently from equal to the intact controls. This is consistent with previous
the blocks used here. These apparent interspecific differ- observations for blue crabs and lobsters that visual signals
ences in behaviors and signals should be more closely are of secondary importance during social interactions
examined. (Gleeson, 1980; Snyder et al.. 1993: Kaplan et al.. 1993).
Blue crab courtship thus appears regulated by female and Thus, the primary function of the male courtship display is
male concurrent chemical signals emanating from multiple likely not transmission of a visual signal. However, it may
sources. It is unknown if the concurrent signals demon- be an excellent method for transmitting both chemical and
strated here are different compounds or ifthey are the same hydrodynamic signals to a potential partner. Rotation ofthe
compound released at different sites. This knowledge awaits periopods causes a strong and highly turbulent flow ofwater
the purification and structural description ofthese chemical directed forward of the animal (Gleeson, 1991; Bushmann,
courtship signals. The release sites of the non-urine chem- unpub. data). This flow would likely entrain any chemical
ical compounds are likewise unknown. In lobsters (Hoimi- signal emanating from the gills or nephropores. In addition,
nis (imericanus), the gill current has been implicated as a some crustaceans use hydrodynamic information during ag-
method for transporting chemical signals to a receiver onistic interactions and prey capture (Barron and Hazlett,
(Atema, 1985). Because blue crabs possess a similar cur- 1989; Breithaupt ct al., 1995). The highly turbulent, di-
rent, it is possible that the gills themselves or structures rected flow generated by male paddle waving could provide
within the gill cavity are sources ofchemical signals. Teg- directional or other information to females.
umental glands, found in blue crabs and other arthropods Many aspects of the male courtship display remain un-
(Johnson, 1980; Talbot and Demers, 1993) have been sug- clear. It must have some energetic cost and may draw
gested as chemical signal sources in several crustacean attention by predators, yet it need not occur for successful
species (Berry, 1970; Kamiguchi, 1972; Bushmann and pairing and occurred in less than halfthe observed encoun-
Atema, 1996) and also may play a role here. ters. In this study its occurrence was not correlated with
Loss of chemical signals in some instances had indirect female premolt stage, the relative sizes of males and fe-
effects on behavior. Males were less aggressive toward males, orpairing success during theencounter. The function
antennule-ablated females. Ablation evidently alters either ofthis rather spectacularbehaviorand the stimuli leading to
female behavior or her signaling patterns in a way that its initiation require further investigation.
affects male agonistic behavior. Similarly, female courtship Loss of female chemoreception appeared to accelerate
behaviors were reduced when male chemical reception was rather than retard pairing. When females were antennule-
CONCURRENT SIGNALS IN BLUE CRABS 69
ablated, males showed little agonistic behavior, females In summary, Callincctes sapidus courtship illustrates
exhibited fewercourtship behaviors, and pairs formed more both behavioral plasticity and the importance of behavioral
quickly than in the intact control group (Fig. 3B) and they regulation through a signaling system. The concurrent and
remained stable. This is at odds with Gibbs (1996), who seemingly redundant chemical signals discussed here may
found males to be more aggressive toward antennule- be different compounds or the same compound released
ablated females and the time required for pairing to be from different sites. Chemical rather than visual signals
unaffected. The present study suggests that females use from both male and female seem to play crucial roles in
chemical information and courtship behaviors to lengthen courtship and pairing. Although these signals influence the
courtship periods, perhaps as a way of better evaluating initiation of behaviors and pairing success, there appear to
potential partners. Loss of chemical information through be many different pathways leading to pairing success, and
female antennule ablation would then result in less female no single behavior and perhaps no single signal is necessary
evaluation and faster pairing. for pairing success. Courtship behaviors and chemical sig-
The significant reduction in time until first behavior seen naling may operate in a more complex and flexible manner
in the male blindfolded group was probably a general be- than previously demonstrated.
havioral rather than specific communication effect. Blind-
folded males, without visual stimuli, may have been less
wary and more likely to begin moving about the pool after Acknowledgments
trial start. This male movement would result in more rapid
encounters with females. The time until Initiation ofPair The author thanks Dr. Anson H. Mines forhis assistance,
Formation was not significantly shortened, however (Fig. support, and review of this manuscript. This work was
3B), and blindfolding had no effect on any measured be- funded through a Smithsonian Postdoctoral Fellowship to
havior. PB, and an NSF grant OCE-971 1843 to AHH.
Several studies have shownthat lateral antennule ablation
affects behavior by interfering with chemical reception
(Ache, 1975; Ameyaw-Akumfi and Hazlett, 1975; Gleeson,
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