Exploration in a T-Maze by the Crayfish Cherax destructor Suggests Bilateral Comparison of Antennal Tactile Information

2005·2.5 MB·English

by  Adrian Mcmahon

Reference: Bio/. Bull. 208: IS3-188. (June 2005)
2005 Marine Biological Laboratory
Exploration in a T-Maze by the Crayfish Cherax
destructor Suggests Bilateral Comparison of Antennal
Tactile Information
ADRIAN McMAHONt, BLAIR W. PATULLO, AND DAVID MACMILLAN*
L.
Department ofZoology, The University ofMelbourne, Parkvillc, Victoria 3010, Australia
Abstract. Many crayfish species inhabit murky waters or and orienting (Basil and Sandeman, 2000). The major ap-
have a crepuscular lifestyle, which forces them to rely on pendages for these sensory tasks are the antennules and
chemical and mechanical information rather than visual antennae. Although these appendages are both chemosen-
input. Information on how they use one form ofmechanical sory and mechanosensory. the antennules are the primary
information tactile cues to explore their local environ- olfactory chemosensory organs (Gate and Derby, 2002;
ment is limited. We observed the exploratory behavior of Grasso and Basil, 2002), while the antennae respond pri-
the crayfish Cherax destructor in a T-maze under red light. marily to mechanosensory stimuli (Bush and Laverack,
Animals moved forward along the long armofthe maze and 1982). Each antenna consists of five basal segments and a
then moved equally in one oftwo available directions. The long segmented flagellum. In some species, the antennae are
arm chosen by one crayfish did not affect that selected by a as long as the body and extremely flexible (Sandeman,
second crayfish tested immediately after in an unwashed 1985, 1989; Zeil et al, 1985). These attributes assist cray-
maze. PrevioWuseexperience in the maze also did not affect fish to locate the position of objects by using information
the choice. found, however, that crayfish with one from receptors on the flagellum (Zeil el al.. 1985; Sande-
antenna denervated or splinted back to the carapace turned man, 1989).
more often toward the unaltered side. Our data support the The physiological evidence that the antennae are impor-
hypothesis that crayfish bilaterally compare information tant in tactile responses is substantial (Bush and Laverack.
from their antennae.
1982). Proprioceptive organs at the base of the flagellum
monitor antennal movement and position (Bush and Laver-
Introduction ack. 1982; Mellon. 2000). Changes in tactile or hydrody-
Crayfish are found in a variety of habitats including namic stimulation of sensilla on the flagellum assist to
springs, ephemeral lakes, creeks, rivers, and alpine and determine the direction ofa stimulus (Masters etal., 1982).
subtropical streams (Merrick, 1991; Lawrence and Jones, Thisdetailedinformationallowstheanimal todetermine the
2002). Many species are crepuscular and make regular type of object and the distance to it (Zeil et al.. 1985;
excursions from their shelters in the first few hours after Sandeman and Varju, 1988). Mechanical, including tactile,
dark and before dawn (Page and Larimer, 1972; Reynolds, input from the antennae is therefore likely to be important
1980; Corotto and O'Brien, 2002). As a result, these ani- fornavigation andexploration ofterrain in the wild. In spite
mals rely heavily upon nonvisual stimuli such as chemical of this, behavioral evidence on the use of antennae during
and mechanical, including tactile, cues for moving about exploration of novel environments is limited (Basil and
Sandeman, 2000), and there is no information on how
crayfish explore or navigate in confined spaces. In streams,
Received 14 September 2004; accepted 25 March 2005. crayfish are often exposed to habitats that contain crevices
*Towhomcorrespondenceshouldbeaddressed: Dr. DavidMacmillan. and wooded debris. These and other features restrict or
DAuesptarraltimae.ntE-moafilZ:oodllomgayc,[email protected]. Parkville VIC 3010. impede movement and force animals to make decisions
tPresent address: School ofTropical Environment Studies and Geog- about moving over or around obstacles.
raphy, James Cook University, Townsville, Queensland 4811. Australia. This study investigates the exploratory behavior of the
183
184 A. McMAHON ET AL.
Cherax destructor (Clark 1936) in a restricted
crayfish
space. We used an experimental choice apparatus based on
atraditional Y-maze to mimic a simple exploratory decision
that crayfish might make in their natural habitat. In the
maze, we compared the effects of crayfish scent, memory,
and removal of sensory input from the antennae with the
normal exploratory behavior of control animals.
Materials and Methods
Animals
Crayfish, Cherax destructor, of 6-10 cm rostrum to tail-
fan, were obtained from a commercial supplier and main-
tained in fiberglass aquaria (120 X 50 X 20cm) at 18 C
1 C and an artificial 12 h/12 h light/dark cycle. Animals
were fed pellets ad libitum.
Apparatus
A T-maze was constructed from PVC pipe (diameter 10
cm). An entrance arm (120 cm) and two side arms (55 cm
each) were joined with a T-joint, and each arm was capped
to make the maze watertight (Fig. 1). A 3-cm-wide cut was
made along the top of each arm to allow us to view the
crayfish. After each trial, the maze was cleaned twice with
a high-pressure hose and refilled with tap water. Trials
commenced 30 min after the onset ofthe dark period ofthe
artificial light/dark cycle and continued for 3-6 h, a period
55cm
CRAYFISH EXPLORATION 185
TD control for any surgical effects, sham denervations to guide themselves (thigmotaxis). The tubular arms of the
were performed identically, except that the nerves were maze meant lhal animals walked roughly in the center wilh
neither hooked nor severed, and care was taken to avoid no apparenl deviation. At thejunction, they scanned left and
severe bleeding in case this could produce clotting and right with their antennae before lurning into one arm ofthe
damage the nerve. maze. Animals entered the side arms without preference for
a particular direction: 1 1 animals turned right and 9 turned
Splinting ofantennalflagellum left (n = 20. df = I. ,v~ = 0.25. P = 0.617).
The antennal flagellum was splinted to the top of the
crayfish's carapace. A small plastic tube (6-8 mm length) Influence ofconspecific scent
was attached with cyanoacrylate adhesive to the carapace Twenty crayfish were tested in the maze when it was not
centrally at the fusion between head and thorax. Crayfish washed between trials. These animals were selected ran-
were then given 24 h to adapt before experimentation. domly from a densely populated communal holding tank
Thirty minutes prior to a trial the crayfish was placed in a (=60 animals/nr) to minimize differences in social status
aplnatsetnicnacownatsaisnpelrin(t2e0d bXy2f0eedXing10itcmt)h,rouagnhd tihtse lpelfatstoircrtiugbhet Tbehtewereesnultinodfivaidturailals waansd troeceonrsduerdeassoamechgoriocuepbefatmwielieanritthy.e
on the carapace. The flagellum was held in place with a same or different arm chosen by the animal in the immedi-
small amount of adhesive at the distal end of the tube to ately preceding trial. A 'dummy" crayfish was run in the
secure it to the animal's back. The splint was checked after maze at the start of the experimenl bul excluded from the
the experiment to confirm that it was still in place. analysis. Ifacrayfish failed to walkthrough Ihejunclion and
relurned down the entrance arm. it was excluded and an-
Analysis other dummy crayfish was used before Ihe experimenl con-
General exploratory' behavior. Arm choice was scored as tinued. Once acrayfish hadentered a side arm. a mesh fence
either left or right and analyzed with a chi-square test. A was insertedby hand intothaiarm.belween Ihejunclion and
Yale's correction was applied because there were only two Ihe animal, to prevent the crayfish from turning back during
alternatives in the maze (Fowler et <//., 1998). capture. The crayfish was then removed wilh a nel. In Ihese
experiments. 9 crayfish went in the same direclion as the
Influence ofscent. A runs test for dichotomized data was previous animal and 1 1 went inlo Ihe opposite arm (runs
used to compare right and left choices for randomness test, P > 0.05). This resull suggesls lhal eitherno scent was
(Sokal and Rohlf, 1995). This test determines whether left by othercrayfish in the maze orthere was no preference
events occur in a random sequence or whether the proba- for animals to follow the preceding individual.
bility of a given event is a function of the outcome of a
previous event. Influence ofmemory
Influenceofmemory. To checkforany patterns in each trial, BeTtweenencraalylfiIsrhialws,erIeheemaaczhetewsatsedwiansh1e0dcaonndseacnuilmiavlesirwiealrse.
jatuibnmocevteitoaanknedwnetbroeelwoaalwnkatluhyepzemtdheedfieoanrnt.reaancchecarramyfaisnhd twiimteh sapernutnsinttehset rsreiegspnteieafdliecfdaonrttr2idai-lfs4fe(mrreiunnncseitnienstta,heramlpllcahPsotii>ccec0fo.on0rt5a;ainnsyeerec.rFaTiyhgfe.irsh2e).iwnSaiestsven1no0
Removal ofsensory input. Arm choice was compared with jcurnacytfiisohns(hrouwnsedtersat,ndPom>be0h.a0v5i)o,rwinhetriemaestatkherneetosrheoawcehdthae
artpirogYaohanllcleeedd'aesfnrocemrorrdvoreafentcteethrdeevdaamtncaeihzdmiae-alssnqa.dunadrsTethiiamtmemeestgtsrfapookeruneptensa,ictnohlotgwhgreatoljrukuapnncusotpffiooltrnehmfetewdeaernnted-o aNisniigsntniheigefnoiijfcfuaintncchtaetniptcaortpnatayet(frtrineusrnhonsvst(eherrsoutn,twshePediter>srt1a,00n.P0dt5ro)i<ma,lsba0en.(0hdr5au)ovn.nislotyresofton.rePldii<msep0ls.ap0ye5en)d.t
normalize data, and compared with a Studenl's Mest using
Systat 10.2.
Effect ofthe removal ofantennal sensory information
Results Removal ofsensory input from one ofthe antenna had a
General exploratory behavior pronounced effect on behavior and arm choice. Crayfish
with a denervated flagellum often trailed thai appendage
When placed in the T-maze. crayfish spread their anten- behind when Ihey walked. They walked down the center of
nae to touch the sides before starling lo walk. They then the maze with Ihe intact antenna touching the side, similar
walked up the middle of the lube with both anlennae held to the intact animals. These animals turned toward the side
out in front, touching the walls on either side of the maze. of Ihe intact antenna. The response was consistent whether
186 A. McMAHON ET AL
10
(0
0)
rWe
6 -
o>
*- ~L.
</>
0> (0
CRAYFISH EXPLORATION 187
from a straight wall. In those situations, animals compared a largeopen testarenaand moved more rapidly through it as
known tactile information from the wall with no informa- it became more familiar. If crayfish had remembered their
tion from the water on the other side, which supports the previous choice in the T-maze, one would predict that they
idea that crayfish prefer to explore identified environments. would make a choice more quickly in subsequent trials.
This is also supported in ourexperiments by the finding that However, our time data suggest that this is unlikely. Fur-
denervated animals make a decision in the junction of the thermore, we would expect arm choice to be the same. It
maze faster than intact animals. remains possible that crayfish remembered the maze, but
Our data suggest that crayfish compare tactile input from that the memory did not result in a response to move to a
the two antennae. The finding that both denervated and familiar environment. The result might be different when a
splinted crayfish turned toward their unaltered side suggests chosen direction is reinforced by some resource such as
that the response was not some artifact due to the artificial food or shelter. In such situations, animals would be ex-
removal of sensory information from the denervation pro- pected to turn in the direction that rewards a particular
cedure, but rather that they were comparing inputs from choice.
both antennae. When both antennae detected tactile cues in The extent that vision interacts with the tactile system is
the maze, animals explored randomly: however, when input unclear. Antennal movement appears to be different be-
wasremoved fromone appendage, turns werebiasedtoward tween sighted and blinded crayfish (Zeil et til., 1985). The
the side from which information was still arriving. combination of additional sensory input and tactile infor-
It has been proposed that crayfish and other decapod mation may influence exploration in spaces such as the
crustaceans use bilateral comparison between the antennae T-maze or in the wild, but our darkened conditions elimi-
or antennules to orientate toward chemical cues (lobsters: nated this factor. This situation has a parallel in haptic
Reederand Ache. 1980; Atema, 1996; Beglane el al. 1997; perception in humans. The haptic sense refers to the move-
crayfish: Kraus-Epley and Moore, 2002; review: Grassoand ment of limbs to gather information about their position in
Basil. 2002). When considered in conjunction with these space and about objects they encounter by touch. The cray-
studies, our results suggest subtle differences between the fish system presents a model that may help explain how
way chemical information and tactile information are used visually impaired people gain conscious knowledge of po-
forthis comparison. We observed that animals moved faster sition (Zeil et al., 1985).
in the junction when tactile input was reduced, whereas This study highlights the importance of the antennae to
there is evidence to suggest that selective absence ofchem- crayfish performing directional responses in restricted
ical input produces slower movement (Kraus-Epley and spaces. The role ofthe antennae may have implications for
Moore. 2002). crayfish living in a dynamic environment where all senses
Crayfish encounter a variety of scents in the wild. Some may not always be available. It remains to be determined
decapod crustaceans are sensitive to chemical cues at nano- whether the effect of denervation is temporary or persists
molar and picomolar concentrations (Derby and Atema, until the crayfish grows a new antenna.
1982). Crayfish release urine in bursts (Breithaupt and Eger.
2002), and thus animals may be able to detect other indi- Acknowledgments
avtitdruaacltsedintothtehmeaszcee.ntItoifs kfanmoiwlinarthcaotncsrpaeycfiifsihcsan(dWashrrdimetpaalr.e, We thank Robyn Crook, Garry Jolly-Rogers, Luke Fin-
2004; Crook et al, 2004). In our experiment, we adminis- ley, and Theresa Jones for their input in discussions and
tered scent in a way that crayfish may encounter it in the experimental design. This research was supported by fund-
wild: however, this was not sufficient to affect the direction ing from the Australian Research Council to D. L. Macmil-
lan.
explored by an individual. This mayhave been because they
could detect the residual scent of previous trials in both
Literature cited
arms, orbecause no scent trail was laid in the short time that
animals were in the maze. Given that crayfish were main- Atema, J. 1996. Eddy chemotaxis and odor landscapes: exploration of
tained in high-density communal tanks, individuals were nature with animal sensors. Bil. Hull. 191: 129-138.
likely to be familiar with each other in our experiments, or Basil, J., and D. Sandeman. 2000. Crayfish (Cheru.\ ilcitructur) use
at least to have recognized that they were from the same tmaecnttil.eEctuheoslotogyde1t0e6ct:a2n4d7-l2e5a9rn.topographical changes in theirenviron-
cohort. Testing with scents added in a more guaranteed Beall, S. P., D. J. Langley, and I). H. Edwards. 1990. Inhibition ol
manner, albeit also more artificial, may reveal a different escape tailrlip in crayfish during backward walking and the defense
result. posture. ./. E.\p. Biol. 152: 577-582.
When compared to other studies, our research suggests Beglane.P.F..F.W.Grasso,J.A.Basil,andJ.Atema. 1997. Farfield
chemo-orientation in the American lobster. Homarus americanus: ef-
that the learning mechanisms ofcrayfish may differdepend- fects ofunilateral ablation and lesioning ofthe lateral antennule. Biol.
ing on the topography ofthe environment. Basil and Sande- Bull. 193: 214-215.
,man (2000) found that crayfish learned the environment of Breithaupt, T., and P. Eger. 2002. Urine makes the difference: chem-
188 A. McMAHON ET AL.
icalcommunicationin fightingcrayfishmadevisible.J. Exp. Biol. 205: Masters,W.M.,B.Aicher,J.Tautz,andH.Markl. 1982. Anewtype
1221-1231. ofwater vibration receptoron the crayfish antenna. J. Comp. Physiol.
Bush,B.M.H.,andM.S.Laverack. 1982. Mechanoreceptors.Pp.369- A 149: 409-422.
468 in Biology ofCrustacea. Vol. 3. D. H. Bliss, H. L. Atwood, and Mellon, DeF.,Jr. 2000. Convergenceofmultimodal sensory inputonto
D. C. Sandeman. eds. Academic Press, New York. higher-level neurons of the crayfish olfactory pathway. J. Neitro-
Cate,H.S.,andC.D.Derby.2002. infrastructureandphysiologyofthe physiol. 84: 3043-3055.
hooded sensillum. a bimodal chemo-mechanosensillum of lobsters. Merrick, J. R. 1991. The Biology. Conservation and Management of
J. Comp. Neural. 442: 293-307. Australian FreshwaterCrayfishes.ABibliography. MacquarieUniver-
Corotto. F., and M. R. O'Brien. 2002. Chemosensory stimuli for the sity, NSW, Australia.
walking legs ofthe crayfish Procambams clarkii. J. Chein. Ecol. 28: Page, T.. and J. L. Larimer. 1972. Entrainment ofthe circadian loco-
1117-1130. motor activity rhythm in crayfish. The role of the eyes and caudal
Cronin, T. \V., and T. H. Goldsmith. 1982. Photosensitivity spectrum photoreceptor. J. Comp. Physiol. 78: 107-120.
ofcrayfish rhodopsin measured using fluorescence ofmetarhodopsin. Reeder, P. B. and B. W. Ache. 1980. Chemotaxis in the Florida spiny
J. Gen. Physiol. 79: 313-332. lobster, Panulirusargits. Anim. Behav. 28: 831-839.
Crook, R., B. W. Patullo, and D. L. Macmillan. 2004. Multimodal Reynolds,K.M. 1980. Aspectsofthebiologyofthefreshwatercrayfish,
individual recognition in thecrayfish Cheraxdestructor. Mar. Freshw. Cherax destructor in farm dams in far-western NSW. M.Sc. thesis.
Behav. Physiol. 37: 271-285. University ofNew South Wales, Australia.
Derby, C. D., and J. Atema. 1982. The function ofchemo- and mech- Sandeman, D. C. 1985. Crayfish antennae as tactical organs: their mo-
anoreceptors in lobster (Homarus americanus) feeding behaviour. J. bility and the responses of their proprioceptors to displacement.
Exp. Biol. 98: 317-327. J. Comp. Physiol. A 157: 363-373.
Fowler,J..L.Cohen,andP.Jarvis. 1998. PracticalStatisticsforField Sandeman,D.C. 1989. Physicalproperties,sensoryreceptorsandtactile
Bio/ogv. John Wiley, New York. reflexes of the antenna of the Australian freshwater crayfish Cherax
Grasso, F. W., and J. A. Basil. 2002. How lobsters, crayfishes, and destructor. J. Exp. Biol. 141: 197-217,
crabslocatesourcesofodor:currentperspectivesandfuturedirections. Sandeman, D. C., and D. Varju. 1988. A behavioural study oftactile
Curr. Opin. Neumbiol. 12: 721-727. localizationinthecrayfishChera.\destructor.J. Comp. Physiol.A 163:
Hartman, H. B., and W. D. Austin. 1972. Proprioceptor organs in 525-536.
antennaeofDecapodaCrustacea. 1.Physiologyofachordotonalorgan Sokal, R. R., and F. J. Rohlf. 1995. Biometry: The Principles and
spanning twojoints in spiny lobster Panulirus interruptus (Randall). Practice ofStatistics in Biological Research. 3rd ed. W. H. Freeman,
J. Comp. Physiol. 81: 187. New York.
Kraus-Epley, K. E., and P. A. Moore. 2002. Bilateral and unilateral Ward,J.,N.Saleh,D. W.Dunham,andN. Rahman.2004. Individual
antennal lesions alter orientation abilities of the crayfish. Orconectes discrimination in the big-clawed snapping shrimp,Alpheusheteroche-
rusticus. Chem. Senses 27: 49-55. lis. Mar. Freshw. Behav. Physiol. 37: 35-42.
Lawrence, C.,and C.Jones. 2002. Cherax. Pp. 635-670 in Biologyof Zeil,J.,R.Sandeman,andD.C.Sandeman. 1985. Tactilelocalization:
Freshwater Crayfish, D. L. Holdich, ed. Blackwell Science, Victoria, the function of active antennal movements in the crayfish Cherax
Australia. destructor. J. Comp. Physiol. A 157: 607- 617.