Individual three-spined sticklebacks (Gasterosteus aculeatus) moved closer to a predatory trout when a ‘cooperator' stickleback, which the test fish could see through a one-way mirror, swam up to the predator than when a ‘defector' stickleback appeared to swim only half as close to the predator. After four training runs with both types of partners, the former cooperator also defected. The test fish continued to move closer to the predator in the presence of the former cooperator even though both the former cooperator and the defector now appeared to stop in their approach to the predator at the same distance. This shows that probable partners build up trus

Kettler, Rolf

K¨lling, David

Milinski, Manfred

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Tit for Tat: sticklebacks{Gasterosteus aculeatus) "trusting"a cooperating partnerIndividual three-spined sticklebacks {Gasterosteus aculeatus) moved closer to a predatory troutwhen a "cooperator" stickleback, which the test fish could see through a one-way mirror,swam up to the predator than when a "defector" stickleback appeared to swim only half asclose to the predator. After four training runs with both types of partners, the formercooperator. also defected. The test fish continued to move closer to the predator in thepresence of the former cooperator even though both the former cooperator and the defectornow appeared to stop in their approach to the predator at the same distance. This showsthat probable partners build up trust. [Behav Ecol 1990; 1:7-11]When a pike (Esox Indus) is stalking ashoal of minnows (Phoxinus phoxi-nus), individual minnows leave the shoal andapproach to within four to six body lengthsfrom the predator, wait there for a few sec-onds, and then slowly turn and go back tothe shoal (Magurran et al., 1985; Magurran,Pitcher, 1937; Pitcher et al., 1986). It hasbeen shown that the fish gather informationabout the predator's identity, precise loca-tion, and current motivational state duringsuch inspection visits (Licht, 1989; Magur-ran, Girling, 1986; Magurran, Higham,1988). Two minnows, or sticklebacks (Gas-terosteus aculeatus), will approach a predatormore closely than will single fish (Milinski,1985; Pitcher et al., 1986). Two inspectorsgain similar information but have only halfthe risk of being eaten per individual com-pared to singletons. Although the two fishprovide each other with the shoal advantage(Hamilton, 1971), the fish that initiates thenext step forward has to rely on the otherone following. The two fish are probably ina "prisoner's dilemma," a "game" in whichdefection rather than cooperation is the evo-lutionarily stable strategy (Milinski, 1987,1990). This only applies if the game is playedeither once or a predictable number of times.Insuch a scenario, mutual cooperation wouldyield the highest benefit for both individuals(Axelrod, Hamilton, 1981; May, 1981; May-nard Smith, 1982; Trivers, 1971).A solution to the problem posed by theprisoner's dilemma is provided by the co-operation strategy of Tit for Tat; that is,cooperating in the first game and thereafterdoing what your partner did in the preced-ing game. This strategy has been shown tobe very successful if the players have a cer-tain minimum probability of meeting againin the same situation (Axelrod, 1984; Ax-elrod, Dion, 1988; Axelrod, Hamilton, 1981;Boyd, 1989; Feldman, Thomas, 1987; No-wak, Sigmund, 1989; Peck, Feldman, 1986).Although reciprocity has been demonstrat-ed in a number of species (Dugatkin, 1988;Fischer, 1980; Ligon, Ligon, 1978; Lom-bardo, 1985; Milinski, 1987; Packer, 1977;Seyfarth, Cheney, 1984; Whitehead, 1987;Wilkinson, 1984), only a few investigationshave demonstrated experimentally that anumber of the conditions and predictions ofTit for Tat are fulfilled (Dugatkin, 1988;Lombardo, 1985; Milinski, 1987, 1990;Whitehead, 1987; Wilkinson, 1984).Milinski (1987) used a system of mirrorsso that single sticklebacks approaching a livepredator were provided with either a sim-ulated cooperating companion or a simulat-ed defecting one. In both cases the test fishbehaved according to Tit for Tat. By re-peating the mirror experiments with gup-pies (Poecilia rcticulata), Dugatkin (1988)found almost the same results. Individualsticklebacks in a group of four have theirpreferred partner with whom they repeat-edly perform inspection visits (Milinski etal., in press). May (1987) has suggested thatearly encounters could be used to build uptrust between partners, so that eventuallythey may undertake an enterprise with alarge reward. In the present study we in-vestigate whether single sticklebacks preferto join the more cooperative of two possiblepartners and whether they are willing to "payManfred MilinskiDavid KullingRolf KettlerAbteilungVerhaltensokologie,Zoologisches Institut,Universitat Bern,Wohlenstrasse 50 a,CH-3032 Hinterkappelen,SwitzerlandAddress reprint requests toM. MilinskiReceived 29 September 1989Accepted 9 January 19901045-2249/90/$2.00© 1990 International Societyfor Behavioral EcologyMilinski et al. • Cooperating sticklebacksFigure 1Experimental set-up asviewed from above. Outercompartments containconditioned sticklebacks;experimental compartmentsin middle contains test fishand plants; predatorcompartment at rightcontains a rainbow trout.Sliding Door Net[1 ^ 1]1 —Mill. One-Way MirrorPartition(Partition in Test)One-Way Mirror^ -[ILamp Sliding Door Net1]Lampin advance"—that is, approach the predatormore closely—when the more cooperativepartner is following.Materials and methodsWe divided the experimental tank (80 x 35cm) into four compartments: an experimen-tal compartment (33 x 14.5 cm) containingtwo plants (Vallbneria sp.) at one end; a pred-ator compartment (33 x 14.5 cm) contain-ing a rainbow trout {Oncorhynchus mykiss,about 28 cm long); and two outer compart-ments (80 x 9 cm), one on either side of theexperimental and predator compartments(Figure 1). Each of the outer compartmentshad a start section at one end from which aconditioned stickleback, could be made toswim toward the other end by opening asliding door and switching on a weak greenlight positioned at the far end, outside thebackwall. When a conditioned sticklebackcame within 5 cm of a net positioned at thesame distance as the glass partition betweenthe experimental and predator compart-ments, we switched off the green light andswitched on another green light positionedat the starting end. This made the condi-tioned fish swim back to the start section,where it was then trapped behind the slidingdoor. We used two different female stick-lebacks that we had individually conditionedto swim toward gTeen lights by rewardingthis behavior after a variable ratio schedulewith Tubifex worms under closed-economyconditions for several weeks. We had fed thetrout sticklebacks.Both long walls of the experimental com-partment consisted of one-way mirrors. Weilluminated each of the two outer compart-ments from above using two white lamps(Osram Concentra PAR-EC flood, 80 W)suspended 78 cm above the water level (18cm). The experimental and predator com-partments were illuminated only by the lightpassing through the mirrors. Thus, a con-ditioned fish could be seen from the exper-imental compartment, into which the con-ditioned fish, however, could not see. Weset up a video camera above the experimen-tal tank to film the experimental and pred-ator compartments.Before the start of each trial, we kept thetwo conditioned sticklebacks in their indi-vidual start sections and released a test stick-leback above the plants in the experimentalcompartment. We positioned an opaquepartition in front of the predator compart-ment and another in front of a one-way mir-ror covering the half (16.5 cm) of the ex-perimental compartment closest to thepredator. The test fish was given 30 min tobecome accustomed to the tank. At the startof each trial, we placed the trout in the pred-ator compartment and raised the opaquepartition in front of it. Then we sent one ofthe two conditioned sticklebacks forward andback again in the outer compartment beforetrapping it in its start section. Then the sec-ond conditioned fish was made to swim inthe same way. We sent the two conditionedfish alternately forward and back four timeseach (this was the training of the test fish).We alternated the sequence of the condi-tioned fish and the position of the opaquepartition from side to side between differenttest fish so that each possible combinationwas met almost equally often. After eighttraining runs, we placed a second partitionin the equivalent position to the first, thatis, in front of the opposite one-way mirrorin the half closest to the predator (Figure1). As before, we sent each conditioned fishalternately forward and back four times (this8 Behavioral Ecology 1990:1(1)constituted the testing phase). We used eachof 48 test fish only once.As well as video recording the behaviorof both the test fish and the predator, weobserved the course of each conditioned fishdirectly from behind a blind. We divided thepart of the outer compartments betweensliding door and net into six sequentiallynumbered sections of equal length. We usedthese numbered sections to record the po-sition of the conditioned fish. The shortestdistance between the test fish and the glasspartition next to the predator was measuredduring each run of a conditioned fish bothwhen the conditioned fish was in the half ofthe outer compartment closer to the pred-ator and when it was in the other half on itsway back to the start section.ResultsIn the majority of the eight training runs,the test fish approached the predator in syn-chrony with a conditioned fish. Because ofthe opaque partition that was positioned onone side of the experimental compartment,the test fish was able to see one of the con-ditioned fish (the "defector") swimmingabout half the available distance toward thepredator and the other fish (the "coopera-tor") swimming until it was close to the trout.The trout tried to attack each test fish sev-eral times between the start of a trial andthe last test run, especially when the test fishwas close to the trout.During each of the training runs, the testfish came closer to the predator with thecooperator than with the defector (Figure2). The difference between the means of allfour training runs combined with eithercompanion was significant (p < .02, one-tailed Wilcoxon matched-pairs signed-rankstest). In all eight test runs both of the con-ditioned fish were seen to approach onlyhalfway to the predator. In the second andthird test runs, the test fish tended to movecloser to the predator with the conditionedfish that had cooperated during the trainingruns (Figure 2). When the second partitionwas placed in front of the cooperator's sideimmediately before the first test run, the testfish appeared frightened by this distur-bance. This is supported by the fact that 25test fish which started with the cooperatorin the first test run tended to approach thepredator more closely with the former de-fector whereas the 23 test fish that startedwith the defector tended to swim moreclosely to the predator with the former co-operator (p < .05, one-tailed f/test). There-fore, the disturbance had a conservative ef-fect with respect to the hypothesis and wasi 1 2 -11 I1I 11 2 3 4Training11JU1 2 3 *Testmost pronounced in the test run that im-mediately followed the disturbance.When the conditioned fish was in the halfof its compartment close to its start sectionon its way back, the test fish also returnedfrom its inspection visit. This is depicted bythe test fish's greater distance to the pred-ator (Figure 3) as compared to when theconditioned fish was close to the predator(Figure 2). However, the test fish returnedmore slowly when it had started the inspec-tion visit with the cooperator than with thedefector. During each of the training runs,the test fish was significantly closer to thepredator with the cooperator than with thedefector (Figure 3). This was also the casein each of the first two test runs. Thereafter,the test fish reacted to the cooperator andto the defector in the same way.DiscussionAlthough we are using words such as "trust,"we do not assume that our fish were con-sciously trusting. What looked like trust mayhave been simply the result of applying arule that generates behavior which has beendescribed as "nice, retaliating and forgiv-ing" (Axelrod, 1984).In the four training runs with either thecooperator or the defector, the test stickle-backs moved closer to the predator whenthey were accompanied by the cooperatingpartner. Because neither the cooperator norO 16-O 12.8JLJL JLiJLJL1 2 3TrainingJL JL»7 «B 47 47 44. I1 2 3 4TestFigure 2Average (±SE) minimumdistance (cm) between thetest fish and the predatorwhen the conditioned fishwas in the half of itscompartment closer to thepredator during trainingruns and test runs. Shadedcolumns show runs with thecooperator, unshadedcolumns show runs with thedefector; n — number oftrials with different test fish,n with missing values shownin columns; p — significant(<.O5) differences betweenruns with cooperator anddefector after one-tailedWilcoxon matched-pairssigned-ranks test.Figure 3Average (±SE) minimumdistance (cm) between thetest fish and the predatorwhen the conditioned fishwas in the half of itscompartment close to itsstart section on its returnduring training runs and testruns. Other explanations asin Figure 2.Milinski et aJ. • Cooperating sticklebacks 9the defector could see the test fish, it musthave been the test fish's decision to movecloser to the predator with the cooperator.In both cases the test fish simply could havefollowed the other fish. No cooperationneeds to be involved here, in contrast toprevious mirror experiments (Milinski, 1987)in which the cooperating mirror image pro-ceeded only when the test fish moved for-ward. In the test runs, however, the test fishsaw both the former cooperator and the de-fector approaching the predator up to thedefector's distance. The test fish moved clos-er to the predator after the former coop-erator had disappeared behind a partition(i.e., defected), as had the defector. As boththe cooperator and the defector defected inthe test runs at exactly the same distancefrom the predator, the test fish's closer ap-proach to the predator can be interpretedas "paying for trust." When a partner ap-peared that had previously cooperated, thetest stickleback was willing to take the nextstep toward the predator, which is equiva-lent to "cooperate for cooperate" in the Titfor Tat strategy.Because the roles of defector and coop-erator were alternated between the two con-ditioned fish from test fish to test fish, theexperimental results were caused neither byindividual differences between the two con-ditioned fish nor by a hidden asymmetry ofthe tank. Although we cannot rule out thateach test fish learned on which side it couldexpect its cooperator to appear, we have evi-dence for individual recognition of the co-operating partner from another study (Mi-linski et al., in press).The finding that the test fish continuedto cooperate with the former cooperator un-til after this fish had defected twice suggeststhat the sticklebacks were playing Tit forTwo Tats, a strategy that has been shownto be more successful sometimes than Titfor Tat (Axelrod, 1984; Boyd, Lorberbaum,1987). However, it is possible that the num-ber of defections, which are accepted beforea defection* is the answer, is a function ofthe amount of "trust" that has been builtup. Possibly we would have found somethingsuch as Tit for Four Tats after 10 trainingruns with the cooperator. Furthermore, itis possible that the fish use strategies withsome realistic stochasticity in them (May,1987), such as cooperation with a probabil-ity of 90% after the partner has defectedonce, with a probability of 80% after its sec-ond defection, and so on.In a companion study (Milinski et al., inpress), it has been shown that sticklebacksin gToups of four have preferred partnerswith whom they cooperate repeatedly. Thepresent study suggests the mechanism bywhich such reciprocal pairs may build uptrust. This is to make the next cooperativestep when the partners that follow are thosethat had been seen to "pay in advance"themselves. This study and previous ones(Milinski, 1987, 1990; Milinski et al., inpress) have shown that the sticklebacks' be-havior is compatible with a cooperationstrategy modeled on Tit for Tat. This doesnot mean that a different cooperation strat-egy could not explain the results better.There is clearly a need for alternative strat-egies against which Tit for Tat can be tested.We thank Theo Bakker, Alex Kacelnik, and Anne Ma-gurran for comments, and Olivia Lassiere for improv-ing our English.ReferencesAxelrod R, 1984. The evolution of cooperation. NewYork: Basic Books.Axelrod R, Dion D, 1988. The further evolution ofcooperation. Science 242:1385-1390.Axelrod R, Hamilton WD, 1981. The evolution of co-operation. Science 211:1390-1396.Boyd R, 1989. Mistakes allow evolutionary stability inthe repeated prisoner's dilemma game. J Theor Biol136:47-56.Boyd R, Lorberbaum JP, 1987. No pure strategy isevolutionarily stable in the repeated prisoner's dilem-ma game. Nature 327:58-59.Dugatkin LA, 1988. Do guppies play Tit for Tat duringpredator inspection visits? Behav Ecol Sociobiol 23:395-399.Feldman MW, Thomas EAC, 1987. 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Tit for Tat: sticklebacks (Gasterosteus aculeatus) ‘trusting' a cooperating partner

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