1 60

ReferencesBond, A . B . 1983 . Visual search and selection of natural

stimuli in the pigeon : the attention threshold hypothe-sis . J. exp . Psychol . : Anim . Behav. Proc ., 9, 292--306 .

Dawkins, M . 1971 . Perceptual changes in chicks: anotherlook at the 'search image' concept . Anim. Behav., 19,566-574 .

Friedman, M . B . 1975 . How birds use their eyes . In :Neural and Endocrine Aspects of Behavior in Birds (Ed .by P . Wright, P . G . Caryl & D . M. Vowles), pp . 181204 . New York: Elsevier.

Gendron R. P. 1986 . Searching for cryptic prey : evidencefor optimal search rates and the formation of searchimages in quail . Anim. Behav ., 34, 898-912 .

Guilford, T . & Dawkins, M . S . 1987 . Search image notproven : a reappraisal of recent evidence . Anim. Behav .,35,1838-1845 .

Lawrence, E . S . 1985a. Evidence for search image inblackbirds (Turdus merula L .) : short-term learning .Anim. Behav ., 33, 929-937 .

Lawrence, E . S . 1985b. Evidence for search image inblackbirds (Turdus merula L .) : long-term learning .Anim. Behav ., 33, 1301-1309 .

Lawrence, E . S . 1985c . Vigilance during 'easy' and'difficult' foraging tasks . Anim. Behav ., 33, 1373-1375 .

Lawrence, E . S . 1986 . Can great tits (Parus major) acquiresearch images? Oikos, 47, 3- 12 .

Martin, G. R . 1986 . The eye of a passeriform bird, theEuropean starling (Sturnus vulgaris) : eye movementamplitude, visual fields and schematic optics . J. comp .Physiol. A ., 159, 545-557 .

Pietrewicz, A . T . & Kamil, A. C . 1979 . Search imageformation in the blue jay Cvanocitta cristata. Science,N. Y., 204, 1332-1333 .

Wallman, J. & Pettigrew J. D. 1985 . Conjugate anddisjunctive saccades in two avian species with contrast-ing oculomotor strategies. J. Neurosci ., 5, 1418-1428 .

Zeigler, H . P ., Levitt P. W . & Levine R . R . 1980 . Eating inthe pigeon (Columba livia) . Movement patterns, stereo-typy and stimulus control . J. comp . physiol. Psychol.,94,783-794 .

(Received 10 November 1987; revised 11 January 1988 ;MS. number.• sc 410)

Search Image versus Search Rate:a Reply to Lawrence

In an attempt to distinguish the search image andsearch rate hypotheses (defined elsewhere : Guil-ford & Dawkins 1987), Lawrence (1988) has reana-lysed some of his blackbird, Turdus merula, forag-ing data with respect to what he calls 'scan times' .Lawrence is entirely correct that measurements ofthe time it takes to detect the presence or absence offood items are potentially the best way to decidebetween the two hypotheses . But his own scan timedata can only be used in this way if (1) we can besure that a single scan corresponds to a singledecision or view, and (2) causes of the reduction in

Animal Behaviour, 37, l

scan time with experience other than increaseddetection ability (e .g . preference changes, motorability changes) have been eliminated . We areunhappy with Lawrence's data on both accounts .

(1) What is a scan? To answer our (1987)criticism of his 'residual search time' (Lawrence1985b) being used to measure detection times,Lawrence (1988) has reanalysed his videotapesdirectly measuring 'scan times' . . .'the time (ms)that the bird's head remained stationary immedia-tely following swallowing an item until the com-mencement of the next prey-strike' . The crucialquestion is whether his measured scan times aremade up of just one (as he claims), or several, viewseach involving a decision about whether a crypticprey item is present . If a 'scan' is made up of severalsuch decisions, then our original objection (Guil-ford & Dawkins 1987), that long periods before aprey item is eaten could include several unsuccess-ful views, still holds .

The problem with Lawrence's scans is that theyare, by definition, always terminated either by preycapture (successful scans), or by a background-directed peck, look, or period of vigilance (unsuc-cessful scans) . This seems to imply that birds neverviewed more than a single piece of the backgroundbefore switching to one of these different beha-viours, and that it was always possible to judgeevery time a bird rejected a view as empty (wronglyor rightly) . We find this situation hard to accept,and we suspect, therefore, that scans do in factsometimes constitute multiple views . Lawrencedoes consider this point, but rejects it on thegrounds that his scan times are too short . Thisrejection is based on the comparability of themajority of the endogenous intervals between theeye movements (saccades) of laboratory restrainedbirds . However, in the study cited inter-saccadicintervals are measured under conditions 'far fromwhat the animals would experience in their naturalcircumstances' (Wallman & Pettigrew 1985, page1418), where there is little or no need for the bird tosearch at all . This study was done specifically inorder to investigate endogenous activity ratherthan that associated with the search for specifictargets, and it seems likely that saccades would bemuch more frequent (hence views much shorter) ina bird actively searching a complex environmentfor hidden prey. Actively foraging ring doves,Streptopelia risoria, have inter-saccadic intervalspeaking at about 200 ms . For house sparrows,Passer domesticus, the modal interval is evenshorter, about 100 ms (Friedman 1975) . AlthoughFriedman's experiments measured head move-ments, and cannot tell us about possible eyemovements within head-stationary periods, theyclearly illustrate that birds can and do make use of

very short viewing periods when searching for prey .Multiple views within the time range of Lawrence'sscans are certainly possible . We accept that it islikely that if the blackbird's head and eyes reallywere stationary during every scan, then scanswould constitute single views, and Lawrence'spredictions of the search image hypothesis wouldthen follow . But unfortunately the data really arenot good enough to tell . And if scans are multipleviews then Lawrence's major prediction, that suc-cessful scan times should decrease with experienceof cryptic prey, is also predicted by the search ratehypothesis because each successful view will bepreceded by fewer unsuccessful views even thoughthe length of each view may have increased (seeGuilford & Dawkins 1987) .

Lawrence cites `Two additional lines of evidencethat support a search image interpretation' . In oneexperiment two juvenile blackbirds failed to eat anycryptic prey, and they had longer scan times thansuccessful birds . However, as with the 'unsuccess-ful' scans of generally successful birds, this resulthas a search rate interpretation too: if scans aremultiple views, then prey detection will tend to cutshort scans . Unsuccessful scans should be longerthan successful scans . The second line of evidence isthat `blackbirds learnt to speed up their assessmentof empty patches' . Although it is indeed a predic-tion of the search rate hypothesis that a bird that islearning to see cryptic prey should slow down itssearch rate (increase its viewing time) both beforedetecting prey, and before deciding to reject a viewas empty, Lawrence's result is concerned with aquite different phenomenon altogether. In hisexperiment empty patches are not empty views, butentire tests in which a background board containedno prey at all. Blackbirds were learning to dis-tinguish quickly between potential feeding sitesthat either did or did not contain food . Thisevidence is wholly inappropriate to the question ofsearch image versus search rate .

(2) Why do scan times decrease? Lawrence'smain result is that for birds hunting cryptic preyscan times decrease with experience, and heassumes that the only reason for such decreases isan increase in the ability of a predator to detectprey (which he interprets as building up a searchimage, although we have shown that, if scans aremultiple views, it is equally explainable by thesearch rate hypothesis). But many other processesmay occur during the course of tests such as thosedescribed by Lawrence (Dawkins 1971) . Evenpretrained predators may increase their preferencefor certain foods, for example, so that a decreasingdelay before striking prey may occur during orbetween tests simply because the predator finds thefood more acceptable . Thus the predator would

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show a decrease in what could be called 'scan time'but could equally be called `acceptance time' or`preparation to strike time' . At the end of a test apredator would, on this explanation, be no better atdetecting prey than it was at the beginning, but itwould have learnt to like, or to target, what it seesand so strike sooner .

One way of partially overcoming such problemsis to compare the behaviour of predators in testswhere the same food is either cryptic or conspi-cuous (Dawkins 1971 ; Lawrence 1985a). Lawrencedoes not present proper data for making therequisite within-trial comparisons of scan times forconspicuous prey, although it seems to be statedimplicitly in the figure (Lawrence 1988) that theyremain constant at 260 ms . There is considerablevariation between Lawrence's experiments (1985a .b, c), but in some it is clear that birds do changetheir behaviour (e .g . foraging rate ; handling time)towards conspicuous as well as cryptic prey withexperience. In one experiment with juvenile birds(Lawrence 1985b ; experiment 3) even residualsearch times decrease between conspicuous tests .which Lawrence himself attributes to the birdsbecoming accustomed to green baits .

Lawrence's data suggest that such changes mayplay an important role in his results . The essence ofthe search image hypothesis is that it involvesshort-term perceptual changes in the ability todetect cryptic prey (Lawrence & Allen 1983) .perhaps through selective attention (Bond 1983 :Guilford & Dawkins 1987) . It is this short-termflexibility that makes it an adaptive response forhunting variably cryptic prey . But many of theeffects that occur within trials in Lawrence's experi-ments appear also to be consolidated between testsperformed hours, even sometimes days, apart . Weconclude, therefore, that whilst Lawrence's experi-ments provide much detailed evidence of howpredator performance improves with foraging ex-perience, they probably cannot allow us to decidecategorically between the various potential mecha-nisms, particularly search image formation andsearch rate adjustment, responsible for such im-provements .

We thank Simon Lawrence for his helpful corre-spondence, and St John's and Somerville Colleges,Oxford, for financial support .

TIM GUILFORDMARIAN STAMP DAWKINS

Animal Behaviour Research Group,Department of Zoology,South Parks Road,Oxford OXI 3PS, U.K.

ReferencesBond, A . B . 1983 . Visual search and selection of natu al

1 6 2

stimuli in the pigeon : the attention threshold hypothe-sis . J. Exp . Psvchol . : Anim . Behar . Proc . . 9, 292- 306 .

Dawkins, M . 1971. Perceptual changes in chicks : anotherlook at the 'search image' concept . Anim. Behav ., 19,566-574 .

Friedman, M . B . 1975 . How birds use their eyes . In :Neural and Endocrine Aspects of Behaviour in Birds (Ed .by P. Wright, P . G . Caryl & D . M . Vowles), pp . 181-204 . Amsterdam: Elsevier .

Guilford, T . & Dawkins, M . S . 1987 . Search images notproven : a reappraisal of recent evidence . Anim . Behar .,35,1838-1845 .

Lawrence, E. S . 1985a. Evidence for search image inblackbirds (Turdus merula L .) : short-term learning.Anim . Behav ., 33, 929-937 .

Lawrence, E . S . 1985b. Evidence for search image inblackbirds (Turdus merula L .) : long-term learning .Anim. Behav ., 33, 1301-1309 .

Lawrence, E. S . 1985c. Vigilance during 'easy' and'difficult' foraging tasks . Anim . Behav ., 33, 1373-1375 .

Lawrence, E . S . 1988 . Why blackbirds overlook crypticprey : search rate or search image? Anim. Behav ., 36,157-160 .

Lawrence, E . S . & Allen, J . A . 1983 . On the term 'searchimage' . Oikos, 40, 313-314 .

Wallman, J . & Pettigrew, J . D . 1985 . Conjugate anddisjunctive saccades in two avian species with contrast-ing oculomotor strategies . J. Neuro .sci. 5, 1418-1428 .

(Received 22 April 1988; MS. number; s(44 1)

In Search of a Hypothetical Construct:A Reply to Guilford & Dawkins

Predators hunting for cryptic prey exhibit anenhanced ability to detect those items as a result oftheir experience with them . This type of learning iscalled search image formation, a term that has beenused to connote a perceptual change in the preda-tor that not only enhances detection for one preytype but interferes with detection for other preytypes . Despite its theoretical connotations, closerscrutiny of this search image hypothesis, togetherwith Guilford & Dawkins' (1987) careful analysisof it, reveals that 'search image' is little more than adescriptive term, and one that, for many years now,has been in need of an explanatory mechanism .That is, although the language used to describesearch image formation ('perceptual filter' and'perceptual specialization') for example, might givethe impression that legitimate hypothetical con-structs are being invoked, this perceptual languageis glib if not entirely vacuous .

The authors might charge that this is an overin-terpretation of their paper . But, by revealing theproblematic nature of previous perceptual inter-pretations of the search image hypothesis, and by

Animal Behaviour, 37, 1

suggesting what they consider to be an alternativeexplanation, Guilford & Dawkins inevitably opena can of worms (coloured baits?) . Specifically, I willargue that (1) perhaps contrary to Guilford &Dawkins' view, some 'perceptual change' is, ofnecessity, involved in predators' enhanced rate ofprey capture, and (2) Guilford & Dawkins' searchrate hypothesis, even if accepted as true, can never,strictly speaking, be considered an alternative tothe search image hypothesis as the authors imply .(To avoid confusing description with theory,henceforth I shall use 'enhanced prey capture' torefer to the empirical phenomenon under discus-sion .)

(1) My insistence that a 'perceptual change' mustunderlie enhanced prey capture is merely recogni-tion of the fact that the central nervous system(CNS) is necessarily involved in vertebrate learn-ing. The logic of this statement, accepted asaxiomatic by students of learning, is as follows . If,in an enhanced prey capture (or any other learning)experiment, animals are not simply making periph-eral adjustments, say in orientation, that wouldalter the afferent stimulus input, and if we observe arelatively permanent change in motor behaviour(i .e . efferent output), then we must ask, 'Whatinstructs those motor neurons?' The answer is thata change must have occurred in the CNS portion ofthis sensory motor arc . Some scientists have calledthis 'a perceptual change', others 'a cognitivechange', and still others, simply 'learning' . What-ever one wishes to call it, and elusive though suchprocesses may be, that CNS change nonethelessmust occur a priori to any observable changes inmotor behaviour (such as a change in search rate) .

(2) 'Perceptual change' and search rate changeare not mutually exclusive . Enhanced prey captureis thought to involve interference with other preytypes. This conflation of enhanced prey captureand interference effects is unfortunate becauseinterference need not of necessity be part of the yet-to-be-identified perceptual/cognitive mechanism .Failing to recognize this fact has led Guilford &Dawkins to confuse different levels of proximateanalysis, namely perceptual/cognitive versusmotor/efferent. That is, the thrust of their paperseems to be to pit a 'perceptual change' hypothesis(the search image hypothesis) against a motor/efferent hypothesis (search rate hypothesis) when,in fact, they are not mutually exclusive . Certainly,any perceptual hypothesis that postulates interfer-ence with an animal's ability to see other crypticprey might not seem compatible with a motorhypothesis that involves a reduction in visualsearch rate but, strictly speaking, these are notalternative explanations and it is important to