Report Nociceptive Sensitization Reduces Predation Risk

By R. Crook, Katharine Dickson, R. Hanlon, E. Walters. 2014

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Program in Sensory Physiology and Behavior, MarineBiological Laboratory, Woods Hole, MA 02543, USASummarySublethal injury triggers long-lasting sensitization of defen-sive responses in most species examined, suggesting theinvolvement of powerful evolutionary selection pressures[1]. In humans, this persistent nociceptive sensitization isoften accompanied by heightened sensations of pain andanxiety [2]. While experimental [3] and clinical [4] evidencesupport the adaptive value of immediate nociception duringinjury, no direct evidence exists for adaptive benefits oflong-lasting sensitization after injury. Recently, we showedthatminorinjury produceslong-term sensitizationofbehav-ioral and neuronal responses in squid, Doryteuthis pealei[5, 6]. Here we tested the adaptive value of this sensitizationduring encounters between squid and a natural fish pred-ator.Locomotionandotherspontaneousbehaviorsofsquidthat received distal injury to a single arm (with or withouttransient anesthesia) showed no measurable impairment6 hr after the injury. However, black sea bass given accessto freely swimming squid oriented toward and pursuedinjured squid at greater distances than uninjured squid,regardless of previous anesthetic treatment. Once targeted,injured squid began defensive behavioral sequences [7, 8]earlierthanuninjuredsquid.Thiseffectwasblockedbybriefanesthetic treatment that prevented development of noci-ceptive sensitization [6, 9]. Importantly, the early anesthetictreatment also reduced the subsequent escape and survivalofinjured, but not uninjured, squid. Thus,while minor injuryincreasestheriskofpredatoryattack,italsotriggersasensi-tized state that promotes enhanced responsiveness tothreats,increasingthesurvival(Darwinianfitness)ofinjuredanimals during subsequent predatory encounters.ResultsBecause minor injury in the squid, Doryteuthis (Loligo) pealeii,induces hypersensitivity to visual and cutaneous stimuliwithout affecting general activity levels or foraging behavior[5],wehypothesizedthatnociceptivesensitizationinthesean-imalsfunctionsprimarilytooffsetincreasedrisksofpredation.To test this hypothesis, we staged a series of controlledinteractions with a fish predator, black sea bass (Centropristisstriata),askingwhetherpreventionofnociceptivesensitizationby transient anesthetization during surgery influenced thecourse and outcome of the predatory interaction. Black seabass are benthic, visual hunters [10] that prey on D. pealei astheymigrateintoshallow,inshoreareas[11].Ourobservationsconfirmed that these predatory interactions follow a distinctseries of stages that are diagrammed in Figure 1 [5, 7, 8, 12],beginning with a primary defense of crypsis (avoiding detec-tion) and progressing swiftly to secondary defenses againstpursuit by the predator that begin with deimatic behavior ofrapid body patterning appearance and/or avoidance swim-ming, followed by escape jetting and protean defense (inkrelease and erratic, unpredictable jetting directions). When afish targets a squid, its chase sequence progresses in stagesfrom orientation to pursuit, attack, and capture [8, 13, 14],with many encounters abandoned prior to completion.Fish Predators Target Squid with InjuriesMinor injury to a single arm 6 hr earlier produced no effectson spontaneous swimming or other behaviors detectable byhumanobservers duringvideo analysis, regardlessof whetherthe animal had been anesthetized during the injury (see also[5]). Nevertheless, black sea bass selectively targeted squidinbothinjuredgroups(injured[I]andinjuredtreatedwithanes-thetic [IA]) compared to the uninjured groups (uninjured [U]and uninjured treated with anesthetic [UA]) (for anestheticdetails see legend of Figure 2 and Supplemental ExperimentalProcedures available online). In mixed-treatment trials (n = 4trials, containing 2 each injured and uninjured squid), squidin the I group were more likely to be captured than squid inthe U group present at the same time (five of eight I versusone of eight U squid, odds ratio = 11.7, z = 1.89, p = 0.05). Intrials involving single-treatment groups of squid (e.g., all fourwere uninjured or all four were injured), fish both oriented toandpursuedsquidintheIandIAgroupsfromlongerdistancescompared to squid in the U and UA groups (post hoc t tests,p=0.02and0.001,respectively;Figures2Aand2B),indicatingthat even minor injuries make squid either more conspicuousor more attractive targets to a natural predator [15].Sensitized Squid Are More Responsive to PredationThreatsSquid in the I group (n = 20) had longer alert distances [16, 17]than squid in the IA, U, or UA groups (n = 16, 20, and 16,respectively), indicating earlier initiation of secondary de-fense (I versus U, p = 0.03; Figure 2C). Similarly, I group squidshowedalertbehaviorsatearlierstagesofencountersthanIA,U, or UA squid (p = 0.004; Figure 2D), despite fish orientationandpursuit usuallyoccurringat greaterdistances frominjuredthan uninjured squid (Figures 2A and 2B). I group squid alsohad longer flight initiation distances (versus U, p = 0.008; Fig-ure 2E) compared with squid in the other three groups.Nociceptive Sensitization in Prey Affects the Likelihoodthat a Predatory Encounter Will EscalateSquid in the I group were less likely to be pursued after orien-tation by fish than U group squid (p = 0.046; Figure 2F),compared with squid in the IAgroup (p = 0.017). In encountersthatescalated topursuit, squidin boththeIandIAgroupshadhigher probabilities of being attacked (I versus U, p = 0.042;IA versus U, p = 0.023; Figure 2G). However, only attacks

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