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CROC JAWS MORE SENSITIVETHAN HUMAN FINGERTIPS

Armoured in elaborate scales, the skins ofcrocodiles and alligators are much prized

by the fashion industry. But sadly, not allskins are from farmed animals. Some arefrom endangered species and according toKen Catania from Vanderbilt University,USA, sometimes the only way todistinguish legitimate hides from poachedskins is to look at the distribution ofthousands of microscopic pigmented bumpsthat pepper crocodiles bodies. Adding thatthe minute dome organs are restricted to thefaces of alligators, Catania puzzled, Whatare the organs for? Explaining that theyhave been proposed to detect subtle shiftsin water salinity and shown to sense ripplesin water, Catania says, We suspected thatthere might be more to the story, so he andDuncan Leitch teamed up to take a closerlook at the small structures (p. 4217).

Observing the skin of American alligatorsand Nile crocodiles with scanning electronmicroscopy, Leitch could see that eachdome was surrounded by a hingedepression. And when he sliced through a

series of domes to identify the sensoryreceptor structures beneath, he foundsensitive free nerve endings near the domesurface, and laminated corpuscle structures

which are vibration sensitive anddermal Merkel complexes which respondto sustained pressure in the lowest skinlayer.

Next, Leitch stained the nerve structuresleading from the skin through the reptiles

jaw and painstakingly traced the sensitivetrigeminal nerve as it branched to thedomes. The innervation of these jaws wasincredible! exclaims Catania. The entire

jaw was infiltrated with a delicate networkof nerves. There was a tremendous numberof nerve endings and each of the nerveendings comes out of a hole in the skull,Leitch adds. Referring to the animalscombative lifestyle, he suggests that thisarrangement protects the delicate trigeminalnerve fibres carried inside the skull from damage during attacks whilemaximising the nerve endings sensitivity atthe surface.

But none of these discoveries answered thequestion of which system the domes relay

sensory information to. Recalling that thedomes had been proposed to detect salinitychanges and even electric fields, Leitchgently bathed the limbs of Nile crocodilesin brackish water while carefully recordingthe electrical activity in the spinal nerve,

but couldnt detect a signal. And when he

repeated the experiments while applying aweak electric field to the water, there wasno response again. However, when Leitchgently touched one of the sensory domeswith a minute hair designed to test humantouch sensitivity, he discovered that thedomes around the animals teeth and jawswere even more touch sensitive than humanfinger-tips. And when he filmed crocodilesand alligators going about their business inthe aquarium at night, he was impressed athow fast the animals 50100 ms responsetimes were. As soon as they feelsomething touch, they snap at it, recallsCatania.

So, why do such well-armoured animalsrequire such an exquisite sense of touch?Leitch suggests that this sensitivity allowsthe animals to distinguish rapidly betweenunpalatable pieces of debris and tasty preywhile also allowing mother crocodiles todextrously aid their hatching young byextracting them from the egg with their

jaws. The pair is keen to understand howthese sensory areas map onto the forebrain.Explaining that massive regions of thehuman brain are dedicated to processingtouch sensory information, Catania says,Crocodilians are not an ancestor tohumans, but they are an important branch

that allows us to fill in key parts of theevolutionary puzzle for how sensory mapsin the forebrain have evolved.

10.1242/jeb.081950

Leitch, D. B. and Catania, K. C. (2012). Structure,innervation and response properties of integumentarysensory organs in crocodilians. J. Exp. Biol. 215,4217-4230.

Kathryn Knight

CUTTLEFISH EMBRYOS LEARNBEFORE HATCHINGCuttlefish hatchlings are on their own right

from the start. Emerging unprotected fromthe egg, the youngsters have to be able tofend for themselves, capturing food,evading predators and merging with the

background if they are to survive. Thequestion is, how are they able to perform somany complex behaviours? says LudovicDickel from the Universit de Caen Basse-

Normandie, France, adding, Is thisrepertoire under genetic control or is theanimal able to learn before hatching?According to Dickel, there is someevidence that the youngsters, which usually

prefer to dine on shrimp, can learn to feast

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on crab during the first week of life, buthow far back does the ability to learn go?Can tiny cuttlefish embryos that are stilldeveloping in the egg learn too? Intrigued,Dickel and his colleagues SbastienRomagny, Anne-Sophie Darmaillacq,Mathieu Guib and Ccile Bellangerdecided to investigate when the developingembryos sensory systems begin to functionand whether they were capable of learninga simple task (p. 4125).

Collecting eggs on cuttlefish traps, the teamwaited until the embryos had developed theability to flex their mantles (stage 23 ofdevelopment) before testing which of theirsenses had begun to function. Knowing thatcuttlefish hatchlings need to evadeEuropean sea bass they are one of thefishs favourite delicacies the team testedthe embryos sense of smell by exposingthem to the predators odour, and observedthe tiny animals movements after

painstakingly removing the eggs dark outercase. Explaining that the minute cuttlefish

pulse their mantles when startled, the team

was pleased to see that the developingyoungsters flexed their mantles in responseto the predators odour. And when theytested the embryos sense of touch bygently prodding their mantles with a bluntneedle, the tiny cuttlefish also reacted. Evenat this early stage of development, theembryos had developed the senses of smelland touch.

Yet, when Dickel and his colleagues testedthe embryos reaction to light, the animals

barely stirred: their visual sense had notdeveloped sufficiently. However, when theteam repeated the test 1 to 2 weeks later

when the visual pigments had developed(stage 25 of development), the cuttlefishpulsed their mantles: the visual system wasfinally functioning. The visual system isalso the last system to mature in vertebrateembryos, so this is an impressive homology

between vertebrates and cephalopods asthey diverged very early during evolution,says Dickel.

Having pinpointed when the tiny cuttlefishbegin to perceive light, the team testedwhether the animals could learn to becomedesensitised to light. As soon as the

embryos visual system was functional, theteam showed the youngsters 150 s longflashes of light interspersed by 30 minintervals of darkness: the youngstersenthusiastically pulsed their mantleswhenever the light came on; they wereunable to learn to ignore it. However, by

stage 30, the embryos picked the idea upquickly. They soon began to lose interestin the light and when the team checkedthat the older embryos simply werenttiring of the task by throwing in a gentletap from the needle between the bursts oflight the animals regained some of theirinterest in the light and began pulsingmore energetically again. The cuttlefishembryos were not tiring, they werelearning. So, cuttlefish embryos are able tocollect information while in the egg, andDickel is keen to find out how muchsensory detail the tiny embryos can

process before they embark on life in theopen.

10.1242/jeb.081943

Romagny, S., Darmaillacq, A.-S., Guib, M.,Bellanger, C. and Dickel, L. (2012). Feel, smell andsee in an egg: emergence of perception and learningin an immature invertebrate, the cuttlefish embryo. J.Exp. Biol. 215, 4125-4130.

Kathryn Knight

CRABS SMELL FEAR THROUGHANTENNULESEven if youre armed with a fierce pair of

pincers, life can be risky. Theres alwaysgoing to be a larger crab that might decide

to dine on you. So, crabs tend to give theodour produced by injured crabs a wide

berth, treating it as a warning that a largerpredator may be lurking nearby. Theenvironment is filled with threats, saysMarc Weissburg from the Georgia Instituteof Technology, USA, although it is alsofull of the scents of enticing tasty treats.Unless you are immune to eating, thenyou are always going to have to confrontthe conflict between aversive andattractive odours, Weissburg says.Intrigued by how crabs successfullynegotiate this conflict, Weissburg and ateam of undergraduate student researchers

set out to discover which course blue crabs(Callinectes sapidus) steer when presentedwith a whiff of lunch spiced with danger(p. 4175).

Collecting crabs from the ocean offSavannah, Georgia, Weissburg returnedwith them to the lab where he andKimberly Berkenkamp started to test theirreactions to plumes of different odours in aflow tank. Sure enough, when the animalswere downstream of luscious shrimp aromathey practically galloped toward the origin.However, when the water smelled of

injured crab, the animals became evasiveand some even buried themselves to avoidthe stench.

But, how would they react when the twoodours were flowing in parallel in close

proximity? This time, the crabs were much

more cautious. Although they continued topursue the attractive scent, the crabsactively avoided the side of the tunnel thatsmelled of injured crab. Discriminating

between the plumes and following theattractive odour to its source, the crabswere able to successfully home in on thefood despite the close proximity of thewarning signal.

However, when the duo disrupted the flowby introducing a cylinder into the water, togenerate turbulence and mix the plumes,Weissburg says, The animals were nolonger willing to track to the attractivesource and they reacted as if there was only

an aversive source. Thoroughly mixing thetwo odours had altered the crabs

perception of the tasty prawn aromasufficiently for it to no longer appearattractive. Weissburg decided to find outwhich of their many olfactory organs thecrabs use to distinguish between theattractive and aversive odours.

In blue crabs, the control over orientationtoward an attractive substance is split

between the antennules, which are the smallstructures between the eyes on the head,and chemosensors on the tips of thewalking legs, explains Weissburg. So,

together with Lauren Atkins and DanielleMankin, he tested the animals reactions tothe merged plume when one or other of thenostrils were effectively plugged.

Desensitizing the scent receptors on acrabs legs by immersing them in freshwater, Weissburg then released the animalinto the blended plume: the animal tried totake cover. However, after gently removingthe scent receptors from another crabsantennules and positioning it in the plumemixture, the animal bounded toward thesource of the attractive aroma of food as ifit was uncontaminated. The crab was no

longer repelled by the aversive odour. Wehad knocked out the input [from theantennules] that suppresses navigation. The

behaviour of the animals to track theattractive cue in the presence of theaversive cue was rescued, explainsWeissburg.

10.1242/jeb.081968

Weissburg, M., Atkins, L., Berkenkamp, K. andMankin, D. (2012). Dine or dash? Turbulence inhibitsblue crab navigation in attractiveaversive odorplumes by altering signal structure encoded by theolfactory pathway. J. Exp. Biol. 215, 4175-4182.

Kathryn Knight

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GREGARIOUS ELECTRIC FISH ADJUST TO MAINTAIN SOCIAL ENVELOPE

Bathed in their own gently oscillatingweak electric field, glass knifefish(Eigenmannia virescens) interpret

distortions of the field to learn about theirsurroundings, although the fish rarelyenjoy the opportunity to analyse

perturbations in their isolated fields.According to Sarah Stamper and ManuMadhav from Johns Hopkins University,USA, these fish spend most of their timein groups and in order to avoid jammingeach others electric fields with their ownoscillations, the fish adjust the frequenciesof their fields to prevent a clash. Inaddition, the team explains that thecomplex oscillating field that results whenthe fish congregate is enfolded by anenvelope known as the social envelope

which also has a characteristic lowfrequency ripple. Curious to find outwhether glass knifefish are able to identify

the social envelope produced by a smallcrowd and modulate their own electricalfields in response, Stamper, Madhav, Noah

Cowan and Eric Fortune simulated theelectric fields produced by two glassknifefish and measured the response of athird fish as they systematically varied thefields social envelope (p. 4196).

Presenting a fish with a simulatedcomposite field with a low frequency(2 Hz) social envelope, the team found thatthe fish altered the frequency of its ownoscillating electric field significantly,although fish located in a field with ahigher frequency social envelope (48 Hz)responded more weakly. Thus, the fish wereable to detect low frequency social

envelopes. And when the team analysed theimpact of the third fish on the structure ofthe social envelope, they realised that the

additional fish raised the frequency of thesocial envelope to 515 Hz. However, thefish were not simply increasing the

frequency of the oscillating field to avoidjamming the signals of the other nearbyfish. The team suspects instead that the fishincrease the social envelope frequency toimprove their electrical perception, as verylow frequency electric field envelopes(~2 Hz) may impair their ability to perceivetheir surroundings and objects moving inthe vicinity.

10.1242/jeb.081976

Stamper, S. A., Madhav, M. S., Cowan, N. J. andFortune, E. S. (2012). Beyond the jamming avoidanceresponse: weakly electric fish respond to the envelopeof social electrosensory signals. J. Exp. Biol. 215,4196-4207.

Kathryn Knightkathryn@biologists.com

2012. Published by The Company of Biologists Ltd