Time in Residence Affects Escape and Agonistic Behavior in Adult Male American Lobsters

8 Pages·1999·3.9 MB·English

by  S I Cromarty

Reference: Biol. Bull. 196: 105-112. (February. 1999)
Time in Residence Affects Escape and Agonistic
Behavior in Adult Male American Lobsters
S. I. CROMARTY*, J. MELLO, AND G. KASS-SIMONf
Biological Sciences Department, University ofRhode Island, 100 Flagg Road,
Kingston, Rhode Island 02881-0816
Abstract. Acquisition and retention ofa shelter by a lob- cally ranked from least aggressive (0) to most aggressive
ster are two of the variables that play a role in lobster (6), animalsresiding in the tankfor 1 h hadan average index
agonistic interactions. Since shelter procurement and reten- value of 0.1 compared to a value of 5.0 for animals in
tion are important for lobster survival, behaviors related to residence for 48 h.
this activity frequently outrank other daily behaviors (e.g., These findings are consonant with the suggestion that
searching forfood). Here, we examine the effects oftime in lobsters that have occupied a given space for an extended
residence on the parameters of the escape response of the period of time take possession of the site and defend it
American lobster, Homarus americanus. instead of fleeing when threatened with a threat-inducing
Adult male intermolt lobsters (Stage C4) were placed in stimulus; it supports the idea that shelter retention increases
an experimental tank for three different time periods (one aggressiveness and diminishes avoidance behaviors.
hour, 24hours, and48 hours). Theprobabilityofeliciting an
escape response was inversely related to the time spent in Introduction
the tank. Eighty percent ofthe animals in residence for 1 h
tailflipped in response to a threat, whereas only 14% ofthe Shelter selection by American lobsters, as they make the
animals in residence for 48 h tailflipped. transition from their pelagic phase to a benthic existence,
There were also significant changes in some of the pa- has been studied in detail (Cobb and Wahle, 1994; a re-
rameters ofthe escape response among animals in residence view). Postlarval and early juvenile lobsters actively seek
out cobble and boulder habitats for shelter a habitat that
for24 h compared tothose in residence for 1 h. The number offers the most protection from predators and conspecifics
fofretqauilefnlciyps,avnedlotchietyd,isatcacnecleertartaivoenl,edfowrecre,e raendducweod,rkalftahcotuogrhs (asHuwdeolln,as1p9r8o7t;ecAtiboen aegtaiain,st1s9t8o8r;m sIunrcgzeesaannddWraaphilde,cur1r9e9n1t;s
were not significantly different. Wahle and Steneck, 1991, 1992). Such shelters may be
Furthermore, with increased time in residence, lobsters limited in number since cobble and boulder habitats com-
switched from an avoidance orescape-prone behaviorto an prise only 10% ofthe sea-floor (Kelley, 1987) the habitat
aggressive-prone behavior. Most ofthe animals in residence that is most favored by lobsters. In addition, as lobsters
for 48 h approached and attacked a threat-stimulus rather grow (up to five orders of magnitude increase in body
than fleeing from it. On an empirically defined "index of mass), their aggressiveness increases and their behavior
aggressiveness," in which various behaviors were numeri- becomes less cryptic, so crowding may become more of a
problem (Cobb and Wahle, 1994).
Received 22 July 1998; accepted 14 October 1998. Shelter procurement and retention may therefore be an
*Present address: Department of Neurobiology, Harvard Medi- important determinant of overall behavior in lobsters, with
cal School, 220 Longwood Avenue, Boston, MA 02115. E-mail: dominant individuals procuring and retaining the most fa-
[email protected] be addressed. E-mail: avflOl vorable shelters, which in turn may be important for an
individual's survival (Cobb, 1971; Stewart, 1972). Re-
@uriacc.uri.edu
Abbreviations: FEP. Fisher exact probability test; SSI, subsequent cently, Spanier and others (1998) assessed the behavior of
swims offirst half; SS2, subsequent swims ofsecond half. juvenile American lobsters under predation risk in labora-
105
106 S. I. CROMARTY ET AL.
lory settings. In the presence of a predator fish, the tautog, supplied with its own air supply, and water was obtained
Tautoga onitis, the dominant lobster appeared to guard the from the same source used to supply the tanks at the URI
available shelters; subdominant lobsters, which did not Bay Campus.
guard shelters, had a mortality rate seven times higher than
that of dominant lobsters. Moreover, field observations by
Experiments
O'Neill and Cobb (1979) showed that intruders were less
able to procure a shelter ifthe current resident had occupied Experiments were conducted from May to October, to
it for a certain period of time. avoid possible seasonal differences in behavior. Lnenicka
In laboratory settings, factors that establish the domi- and Zhao (1991) documented seasonal differences in the
nance of an individual over other conspecifics and allow physiology and morphology of crayfish neuromuscular
dominant individuals to have an advantage in procuring, terminals which suggested that lobster escape parameters
capturing, and more importantly holding on to a suit- might differ seasonally.
able shelter include a greater carapace length and claw size Experiments were carried out between 1200 and 1700 h
(Scrivener, 1971), the sex ofthe individual (male), and molt in an aquarium filled with filtered recirculated seawater
stage (O'Neill and Cobb, 1979). from Narragansett Bay. Salinity was measured before each
O'Neill and Cobb (1979) found that shelter familiarity experiment, and ranged between 29%c and 33%o. Waterwas
did not affect shelter procurement or retention in the labo- replaced or added as necessary to maintain salinity within
ratory, but that in the field, lobsters already in ashelterwere this range. The experimental tank was kept between 18C
more likely to retain that shelter. On the other hand, Amer- and 20C by a Frigid Units AE-234 AG-602 chiller. The
ican lobsters have been observed to display increased ag- chillerwasturnedoffbefore the startofthe experiment. The
m
gressiveness after being isolated in individual tanks (E. experimentalWarea consisted of an open-ended tank (1.0
wKreavoibtsz,erpveersd.tchaotmmit.watosSh.Ca.r)d,erantdodiunrdiuncgeoaunrimeaarllsietrosttauidlifelsi,p (L2.X2 0m.3LmX 0X.750.3mmWH)Xim0m.e9r1semd iHn).a lTahregerlamyaoiunt twaansk
after they had been kept for some time in isolated tanks. designed so that a threatening stimulus could be introduced
Therefore, the question arises as tothe extent towhich an at the open end of the experimental tank. A weighted
animal's time in residence is a significant determinant ofits wooden partition with a pulley acted as a blind and a
aggressive and avoidance behavior. To explore this ques- separation from the main tank at the open end. To ensure
tion, we placed animals in an isolated experimental tank for that lobsters were initially at the closed, non-stimulus end, a
periods of 1, 24, or 48 h and videotaped their responses to light was placed at theopenend, causing the lobstertomove
a nontactile threatening stimulus introduced into the tank. towards the darkened closed end. The partition was raised
We now present evidence that with increased time in once the lobster had reached the closed end, while the light
residence, lobsters not only are less likely to flee from a was moved to the closed non-stimulus end. This served to
threat, but also will confront it with increasing aggressive- "push" the animal back towards the open (stimulus), now
ness. darkened, end. A piece of PVC tubing (0.15 m L X 0.10 m
W) weighted to 1.45 kg with pebbles served as the threat-
Materials and Methods ening visual stimulus. The stimulus was raised above the
openendand was released intothe waterat apresetdistance
Procedures and experimental protocols are essentially the of 10 cm (measured from the open edge of the tank to the
same as those described in Cromarty etal., 1991, 1998), but lobster) whenever a lobster approached the open end after
are summarized here with relevant differences included.
the designated residency period. One hour before the ex-
Animals periment, the physical condition of each animal was
checked. Animals were used only ifthey moved around the
Adult American lobsters (carapace length 78 to 84 mm) tank or exhibited antennule flicking.
were obtained directly from an offshore lobster vessel fish- Cameras were placed in two positions (a Sony camcorder
ing in Narragansett Bay, Rhode Island. Animals were above the tank and a Panasonic WV-CD20 camera to the
housed atthe Narragansett Bay Campus ofthe Universityof side), and experiments were recorded (Panasonic AG-6010
Rhode Island in separate, but connecting, tanks in a free- and Panasonic NV-8950) simultaneously from the vertical
flow seawater system at ambient temperatures ranging from and horizontal perspectives. Video recordings of each lob-
16 to22C undera 14-h-light/10-h-dark illuminationcycle. ster were analyzed frame-by-frame. For measurements of
The animals were fed three times per week on a mixed diet distance traveled, a metric grid divided into 0.5-cm units
ofsquid, crab, and fish, but were not fed for48 h priorto an was painted onto the side of the experimental tank. Trans-
experiment. Six hours before an experiment, an animal was parent overlays on the video monitor were later used to
moved to the Kingston campus of the university, where it record the escape swimming distance of each animal. Dis-
was placed in a holding tank (30 cm3). The tank was tance traveled along the length ofthe tank was measured by
DURATION OF SITE RESIDENCY INFLUENCES LOBSTER BEHAVIOR 107
using the position of the tip of the lobster's rostrum as a fered and because each distance was divided equally in half
guide, and the number of tailflips was counted; time was for each escape sequence for each animal, no data are
automatically recorded on the videotape. An independent available to compare distance traveled between the two
observer inspected all recordings and rejected runs in which halves of the subsequent swims for each residency group.
the experimental parameters were not strictly adhered to To quantify the degree of "aggression" in the post-stim-
(e.g., cases in which the stimulus was released closer than ulus behavior ofeach animal, we ranked this behavior on a
10 cm to the experimental animal). scale of to 6 and subjectively ordered behavior towards
After each experiment, the animal's molt stage was de- the stimulus as follows:
termined by examining cuticular changes and setal devel- =
o(ipnmteernmtolitn)tahenipmlaelospowdesre(Auiskeedn,, s1i9n7c3e,p1r9o8b0a)b.ilOintylyofsteasgceaCpe4 1 == abpapcrkoaacwhayb,utnreevmearinapmporroaecthhan one bodylength away
2 approach within one bodylength
depends on the molt stage ofeach lobster (Cromarty et al, =
wl1ee9nr9g1et,hr,el1co9ob9rs5dt)ee.drwaMeteiatghsheutreaennmddeonvftosleuamcoehf,etcxeapmreparepiramacetenutraell,entagrtnihadl,.sacluitntiteyr 453 === aaapppppprrroooaaaccchhh,,, tttooouuuccchhh,, ggrraasspp, and tug/pull
Analysis of the escape response follows our previous 6 approach, touch and grasp, tug/pull, and an offensive
protocol (Cromarty et al, 1991, 1998). To analyze the tailflip
escape parameters, the response was broken into two ele-
Statistical analysis
ments the initial tailflip, henceforth called the "power
swim," followed by the numerous subsequent tailflips, Differences in weight, carapace length, and cutter size
called "subsequent swims." (The number of subsequent among the three residency periods were determined by
swims in this study ranged from one to six.) A tailflip, or parametric analysisofvariance (ANOVA). TheFisherexact
swim, is defined as beginning immediately after the start of probability test (FEP) was used to determine differences in
abdominal flexion and ending at abdominal extension. the probabilities ofescape among the three resident periods.
The following characteristics ofthe escape response were Due to a non-normal distribution ofdata, Kruskal-Wallis
analyzed for each lobster: distance traveled (centimeters), (KW) tests wererun forall the escape parameters except the
numberoftailflips, duration (seconds), frequency oftailflips subsequent swims andthe "aggression intensity index."The
(tailflips per second), velocity (meters per second), acceler- first and second halves ofthe subsequent swims were com-
ation (meters per second squared), force (mass X acceler- pared with a multiple analysis ofvariance (MANOVA) and
ation), work (force X distance), distance swum per weight a repeated measures follow-up test. A trend was considered
l(emnegttehr.sTpheerlkaisltotgwraomp)a,raanmedtdeirsstawnecreesmweuasmurpeedr tloobdsettererbmoidnye t0o.05exi<stPif<t0h.e1.PVavlauleusewfeorreacopnasriadmeerteedrsirganinfgiecdantbeattwPee<n
whether individual lobster variability in weight and size 0.05 forall the statistical tests. Both ANOVAs and MANO-
could alter the significance of a parameter, even though VAs were run on SPSS software ver. 6.6.1 (SPSS Inc.,
weight and size were not significantly different (using an Chicago).
ANOVA) among the animals in the three resident periods.
As in previous analyses, in evaluating acceleration, the Results
added-mass forces (Batchelor, 1967) thatacton accelerating Weight (in grams)/carapace length (in millimeters)/cutter
bodies in fluids were ignored since these are a multiple of length (in millimeters)
mass and would act equally on all animals of the same
eilwonsebvciseagtsphetetrigera(setscseeapedpoebnCsyrbeoeomhtiaashrvedtireoysrreiesagtennaedarldc.n,hotetor1st9rh9e(e1fBl)kae.ctitcnTherhemelealotartia,icnvae1rl9eyc6lsh7ait;asinoDgonaefsnshiitephilsen 0a(.nm3deT5ha,4en8rP-eh=(wS4e0E2r.7M7e1)f.noo3rN1a)olslir)gesnisoigiffndiie1cfn-aithnctal(no4tbd1si5dtfiefrfesfree2(rn9eAc)ne,NcseO2s4Vi-nAwhe,tr(he4Fe(124f,woeu2in7gd)3h2t)i=s,n
eanntdEiraMeceheyshocofafpetehre,ree1ss9pc8oa9np;seeN;paa(ur2ea)mnethtaeenrdisniStwhiaaalsdwpaioncwakel,ryz1es9dw9i3f)mo.;r ((31)) tthhee 4tPh8e-=hca0(.r78a94p)a;ces3i)lmierlneagsrtilhdysentothfelro1eb-shwtee(rr7es8(noAN4s.iO9g)Vn,iAf2,i4ca-Fnh(t2(,d7i92f7f)ere=2n)c,0e.sa1n7id,n
subsequent swims over the entire subsequent swimming the cutter lengths of 1-h (107 3), 24-h (109 =3), and
distance; and (4) the subsequent swims in each half of that 4P8-=h (108 2)resident lobsters (ANOVA, F(2, 27) 0.69,
distance, since earlier experiments showed that there were 0.61).
differences in the total subsequent swimming distance trav-
We Effects ofresidence time on the probability ofescape
eled by lobsters. therefore divided the distance traveled
in the subsequent swims by half and analyzed each half Probability ofescape. The probability of escape for ani-
(Cromarty et al., 1991, 1998). Because the distances dif- mals in the three residence time periods is summarized in
108 S. I. CROMARTY ET AL.
Table I
Escapeandpost-threatbehaviorofanimals in each residencyperiod:
some lobsters initially tailftippedandthen re-approachedthestimulus or
re-approachedandattackedit
Immediate
response
DURATION OF SITE RESIDENCY INFLUENCES LOBSTER BEHAVIOR 109
10 S. I. CROMARTY ET AL.
SSTIMR.l
SSTIME2
O
so
o
0.0 0.2 0.5 0.8 1.0 1.2
TIME
(s)
C3 SSTFl
D
SSTF2
X
O
93
O
NUMBER OF TAILFLIPS
Figure 4. Parameters of subsequent swims of the escape response
exhibited by lobsters in residence for 1 h (;i = 5) and 24 h (11 = 8). An
asterisk(*)indicatesresultsthataresignificantlydifferentatPs0.05. (A)
Mean duration in seconds (s) for the first (SSTIME1) and second (SS-
TIME2)halvesofthesubsequentswimmingdistance. (B)Meannumberof
subsequent swims in the first (SSTFl) and second (SSTF2) halves ofthe
subsequent swimming distance.
B
L.
DURATION OF SITE RESIDENCY INFLUENCES LOBSTKR BEHAVIOR
produce significant differences in the level of arousal in fested as afunction ofhow the animal assesses itsown place
24-h and 48-h residents. in its immediate environment. This assessment then be-
Nonetheless, ifpriorhandlingcontributed tothe observed comes a determinant of how an animal responds to other
time-dependent reluctance to escape and increase in aggres- conspecifics and might be considered operationally as a
siveness, then our findings suggest that an animal becomes "motivational state." A change in "motivational state" has
more aggressive the longer it is left undisturbed in a site. recently been tested in the European hermit crab Pagurus
Many other factors appear to affect an animal's ability to bernhardus during agonistic encounters (Elwood et al..
procure and retain a shelter (O'Neill and Cobb, 1979). 1998). This study showed that the duration and severity of
These include differences in dominance due to body length, the startle/threat response are inversely related to the "mo-
weight, and claw size (Scrivener. 1971). Reproductive sta- tivational state" of the animal to continue the previous
tus is also important. In a related decapod, maternal female activity, namely of fighting for a more suitable shelter
crayfish residents won 92% of their encounters with male inhabited by a conspecific.
intruders (Figler el ul.. 1995). Gravid lobsters exhibit a In summary, our experiments indicate that time in resi-
distinct reduction in escape behavior and are more likely dence and isolation are important physiological determi-
than males to attack an approaching stimulus (Cromarty et nants ofa lobster's behaviorandcan cause it to switch from
al.. 1998). Odor cues for discrimination of familiar and an avoidance-prone to an aggression-prone state.
dominant lobsters (Karavanich and Atema, 1991. 1993,
1998a, b) and sex-identifying urine and molt signals in
Acknowledgments
lobsters (Atema and Cowan, 1986), plus visual cues (Bruski
and Dunham, 1987), are most likely important sensory cues We thank Bill Mac Elroy for allowing us to collect
for procuring and residing in a shelter. Crayfish rapidly nongravid and male animals while he was fishing offshore
learn to discriminate between changing spatial configura- and Tom Angell of the Rhode Island Department of Envi-
tions (Sandeman and Varju, 1988; Varju and Sandeman, ronmental Management for collecting gravid animals off-
1989; Basil and Sandeman, 1997) and. as shown by direct shore. (All lobsters were returned to the Bay after experi-
measurements of electrical heart activity (Shuranova and mentation was completed.) Thanks to Dr. Mike Clancy and
Burmistrov, 1995), are constantly sampling their surround- Ms. Kathy Castro for help in lobster collection and main-
ings (i.e., predators or conspecific intruders, currents, shad- tenance. Drs. Stanley Cobb and Frank Heppner kindly pro-
owsA,nfoiomdpoarvtaainltabidleittye,rmeitcn.a)n.t in shelter retention may be vMiadleida lSacbhowraartotrzyfsorpaccreitainqudinegquainpmeearnlti.erWderafatlsoof tthheanmkanMus-.
ssohcoiwaledcotnhtatacltobwstietrhs wcohnospewceirfeicisn.viHsoufaflmcaonntaecttawli.th(1o9t7h5e)r script. This research was supported by a Whitehall Founda-
tion grant to G.K-S and Grant-in Aid of Research from
animals or were communally housed were less aggressive. Sigma Xi and Lerner Gray Grants for Marine Research to
In this regard, Yeh et ul. (1996, 1997) found that crayfish
S.I.C.
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