Why blackbirds overlook cryptic prey: Search rate or search image?

Why blackbirds overlook cryptic prey: Search rate or search image?

Short Communications subjected to restricted diets during gestation . Meikle et al . (1984) observed that low-ranking female rhesus monkeys, Macaca ...

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Short Communications

subjected to restricted diets during gestation . Meikle et al . (1984) observed that low-ranking female rhesus monkeys, Macaca mulatta, produced fewer offspring and fewer sons than high-ranking monkeys . Also, hamsters of advancing age and/or increasing parity produce smaller, more femalebiased litters (Huck et al ., 1988) . Therefore, it appears that the differential vulnerability of males in utero is exaggerated by various forms of maternal stress . The physiological mechanism by which this occurs is unknown at this time . Sex ratio modification by means of sex-differential prenatal mortality can be considered adaptive if the alternative is to invest heavily in offspring which have a low probability of ever reproducing . Stressed females producing smaller, female-biased litters could still invest as much in each surviving male offspring as non-stressed females with larger litters . Huck et al . (1986) showed that females who were food restricted early in life produced reduced sex ratios but normal litter sizes when bred as adults . This suggests that early nutritional stress may influence lifetime reproductive potential via some other mechanism which allows facultative sex ratio modification without differential mortality in this species . It seems, however, that subordination stress during pregnancy has a more immediate effect on that particular litter, and that this effect involves the inflation of a pre-existing differential male mortality in this species . NANCY C . PRATT U . WILLIAM HUCK * ROBERT D . LISK

Department of Biology, Princeton University, Princeton, NJ 08544, U .S .A .

* Present Address : Biology Program, Sangamon State University, Springfield, IL 62708, U .S .A .

References Clutton-Brock, T . H . & Albon, S . E . 1982 . Parental investment in male and female offspring in mammals . In : Current Problems in Sociobiology (Ed . by Kings College Sociobiology Group), pp. 223-247 . Cambridge : Cambridge University Press . Clutton-Brock, T . H . & Jason, G . R. 1986 . Sex ratio in mammals. Q . Rev . Biol., 61, 339-374. Huck . U . W ., Labov, J . B . & Lisk, R . D . 1986 . Food restricting young hamsters (Mesocricetus aural us) affects sex ratio and growth of subsequent offspring . Biol. Reprod., 35, 592-598 .

Huck, U . W ., Pratt, N . C . & Lisk, R . D . 1988 . Effects of age and parity of litter size and offspring sex ratio in golden hamsters (Mesocricetus auratus) . J . Reprod. Fert ., 83, 209-214 .

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Labov, J . B ., Huck, U . W ., Vaswani, P . & Lisk, R . D . 1986 . Sex ratio manipulation and decreased growth of male offspring of undernourished golden hamsters (Mesocricetus auratus), Behav . Ecol . Sociohiol. . 18, 241-249 .

McGinley, M . A . 1984. The adaptive value of male-biased sex ratios among stressed animals . Am . Nat ., 124, 597 599 .

McMillen, M . M . 1979 . Differential mortality by sex in fetal and neonatal deaths . Science, N.Y., 204, 89-91 . Meikle, D. B ., Tilford, B . L . & Vessey, S . H . 1984 . Dominance rank, secondary sex ratio, and reproduction of offspring in polygynous primates . Am . Nat . 124,597-599 .

Rivers, J . P. W . & Crawford, M . A . 1974 . Maternal nutrition and sex ratio at birth . Nature . Lond, 252, 297-298 .

Sundell, G . 1962 . The sex ratio before uterine implantation in the golden hamster . J. Emhrvol. exp . Morph-, 10,58 -63 .

Trivers, R . L . 1985 . Social Evolution . Menlo Park : Benjamin Cummings . Trivers, R . L . & Willard, D . E . 1973 . Natural selection of parental ability to vary the sex ratio of offspring . Science, N . Y., 179, 90-92 . (Received 21 March 1988, revised 13 Mat , 198X . MS. number . 4s-533)

Why Blackbirds Overlook Cryptic Prey : Search Rate or Search Image? Guilford & Dawkins (1987) have re-examined the search rate/search image hypotheses of animals searching for cryptic prey and highlighted two critical predictions which should distinguish between the two . The search rate hypothesis implies a general increase in detection accuracy and a predator is thought to learn to see cryptic prey by reducing its search rate . A predator that adopts a search image is thought to increase its detection accuracy by concentrating on a specific configuration of stimuli of a single prey type . The search rate hypothesis predicts (1) that learning to see one cryptic prey type will enhance the ability to detect other equally cryptic types (the search image hypothesis predicts that this will interfere with the ability to detect other equally cryptic types) ; and (2) that learning to see cryptic prey will be achieved by learning to spend longer looking at each patch of the environment . In my previous papers (Lawrence 1985a, b) I tested the search image hypothesis by calculating an indirect measure of how much time wild and captive European blackbirds, Turdus merula, spent looking at the background (termed the residual search time) . Guilford & Dawkins (1987) point out that a reduction in the average residual search time fails to exclude the search rate

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Figure 1 . (a) Mean (± SE) successful scan time of five blackbirds (measured in 20 ms frame intervals from videotape) . *P<0 . 05, F=i,,6=7 .7 ; **P<0 . 01, F1,12=10 . 3 . (b) Mean unsuccessful scan times (shaded bars) compared with successful scan times (open bars) . *P<0 . 05, F1,,6=7 . 3 ; **P<0 . 01, F,,12=14 . 4 . hypothesis because it includes both successful and unsuccessful views of the background . I have reanalysed my videotapes to obtain a direct measure of the individual views (the `scan time') preceding both successful and unsuccessful prey detection . If the birds adopt a search image they should search more quickly as they get better at detecting cryptic prey and the data should support the following three predictions :(l) the average scan time should decline from the start to the end of a feeding bout, (2) this pattern should be repeated over a longer time scale (i .e . repeated feeding bouts over a period of weeks) and (3) unsuccessful views of the background should consist of long scan periods (inexperienced birds should fail to see cryptic prey at first, despite spending longer looking at them) . My study took place at Southampton University, Hampshire, U .K . during 1981 and 1982 . The basic method was to video record the behaviour of individually colour-ringed adult blackbirds feeding on 200 small (4 . 5 x 4 . 5 mm) cylindrical pastry baits scattered on the surface of metal trays (0 . 7 x 0 . 8 m)

filled with small pebbles set in casting plaster (described more fully by Lawrence 1985a) . The baits were coloured green using food dye and they were placed either on a matching (painted green), or contrasting (brown) background . For convenience the prey under the first condition were termed `cryptic' and under the latter termed 'conspicuous' . Each subject was familiar with eating pastry prey before test 1, the tests lasted 15-72 s and prey depletion was insignificant (maximum 50 prey eaten per bout) . I have concentrated on the behaviour of the five wild birds shown in Table III of Lawrence (1985b) . Each bird received a random sequence of eight tests : four tests with conspicuous prey and four tests with cryptic prey (spread over 7-30 days) . From a frame-by-frame analysis of the video recordings of each bird's first cryptic test and its fourth cryptic test, I measured the scan time : i .e . the time (ms) that the bird's head remained stationary immediately following swallowing an item until the commencement of the next prey-strike . This period excludes the time in which the bird adopted a vigilant stance (Lawrence 1985c) . (The use of this

Short Communications measure assumes, as in starlings, Sturnus vulgaris, that the eyes converge to bring objects into focus on the temporal, `near-focus' visual field during foraging; Martin 1986, personal communication .) I subdivided scan times between the first and second halves of the birds' cryptic tests (which, on average, corresponded to the first 16 and last 16 prey) . I further subdivided scan times between prey detection that was successful and that which was unsuccessful (the bird proceeded to peck the gravel background by mistake, or hesitated by cocking its head for further scrutiny, the `Looks' recorded by Lawrence 1985a) . When presented with cryptic food for the first time (test 1), the blackbirds' average scan times during the first half of the feeding bout were longer than those during the latter half (F1 , 1 2=10 . 3, P<0-01, Fig . la) . They also reduced their average scan times between tests 1 and 4 (F1 , 16 =7 . 7, P < 0- 05, Fig. I a) . (For an explanation of statistical methods see Lawrence 1985b, 1986) . Intervening tests with conspicuous prey do not affect this result (Lawrence 1985b) . (A test is defined by the presentation of one or other prey/background combination to each bird .) Furthermore, inexperienced blackbirds had relatively long scan times before making detection errors (Fig . lb) . Clearly, the blackbirds did not adopt the strategy of having a number of scan times that were individually too short to detect the cryptic prey . These data are consistent with predictions 1-3 of the search image hypothesis . Two additional lines of evidence that support a search image interpretation are provided by the scan times of six juvenile blackbirds which were tested on the same food in captivity (experiment 3 of Lawrence 1985b) . First, despite having free access to the food on the background, two of the birds failed to learn to detect the cryptic food . As with the adult birds, the mean scan time of the two unsuccessful subjects during test 1 was approximately 40% longer than that taken by the successful subjects (720 ms versus 520 ms) . Second, the four `successful' blackbirds learnt to speed up their assessment of empty patches (Fig. 4b of Lawrence 1985b) and their scan times fell from 490 ms in test 1 to 340 ms in test 4, a similar trend to the open bars in Fig . lb . In this analysis, I measured the stationary head period of blackbirds while foraging . However, it is possible that scan times could be subdivided because of eye movements into multiple intersaccadic intervals, with the assumption that during eye movement saccades searching is not possible . This, however, seems unlikely since in the little eagle (Haliaetus morphnoides, Wallman & Pettigrew 1985) the majority of inter-saccadic intervals

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are relatively long (between 0 . 5 and 5 . 0 s), and these values are comparable in range to those found in the pigeon, Columba livia, and chicken, Gallus gallus domesticus (J . D . Wallman & B . Frost, unpublished data) . Thus, the stationary head period (scan time) of blackbirds, which was less than 0. 5 s even on the first cryptic prey test (Fig . 1), is likely to be synonymous with the bird's stationary eye position . Finally, it is possible that the two hypotheses discussed by Guilford & Dawkins (1987) are not mutually exclusive . It may in fact be necessary to take account of the type of predatory behaviour exhibited by each species and not to assume that all cryptic prey situations present the same problem . For example, granivorous birds search and detect food items in stereotyped, short, repetitive behaviour sequences which are often inaccurate even with apparently highly conspicuous prey (Zeigler et al . 1980), whereas insectivores appear to adopt relatively `precise' and less stereotyped prey detection methods which are highly accurate . For example, when a Barbary dove, Streptopelia risoria, is searching for conspicuous seeds the mean stationary head period is 200 ms (Friedman 1975) . Other granivores, like the bobwhite quail, Colinus virginianus, and the domestic pigeon, range in accuracy from 60 to 80% on conspicuous food (Bond 1983 ; Gendron 1986) . On the other hand, at `maximum' feeding rate on conspicuous pastry pellets, the average scan time of the five blackbirds used in this analysis is longer than that of the granivores (ca . 260 ms), but of much higher accuracy (mean % accurate pecks=0 . 98) . From this one can conclude that the evidence for search image in birds, with the exception of Lawrence (1985a, b) and Pietrewicz & Kamil (1979), has been based on experimentally `convenient' but perhaps inappropriate subjects which do not in life search for prey which has evolved crypsis and hence whose search technique does not reveal the plasticity implied by the search image hypothesis (e .g . the domestic hen, pigeon and bobwhite quail (Dawkins 1971 ; Bond 1983 ; Gendron 1986) . I thank Christine Lawrence for drawing the figure ; Marian Dawkins, Tim Guilford and Graham Martin for constructive discussion, and the SERC for financial support . E . SIMON LAWRENCE* Department of Biology, University of Southampton, Medical & Biological Sciences Building, Bassett Crescent East, Southampton S09 3TU, U .K. * Present address : Department of Zoology, University of Glasgow, Glasgow G12 8QQ, U .K .

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References Bond, A . B . 1983 . Visual search and selection of natural stimuli in the pigeon : the attention threshold hypothesis . J. exp . Psychol . : Anim . Behav. Proc ., 9, 292--306 . Dawkins, M . 1971 . Perceptual changes in chicks: another look 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 . 181 204 . New York : Elsevier. Gendron R. P. 1986 . Searching for cryptic prey : evidence for optimal search rates and the formation of search images in quail . Anim . Behav ., 34, 898-912 . Guilford, T . & Dawkins, M . S . 1987 . Search image not proven : a reappraisal of recent evidence . Anim . Behav ., 35,1838-1845 . Lawrence, E . S . 1985a . Evidence for search image in blackbirds (Turdus merula L .) : short-term learning . Anim . Behav ., 33, 929-937 . Lawrence, E . S . 1985b . Evidence for search image in blackbirds (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) acquire search images? Oikos, 47, 3- 12 . Martin, G . R . 1986 . The eye of a passeriform bird, the European starling (Sturnus vulgaris) : eye movement amplitude, visual fields and schematic optics . J. comp . Physiol. A ., 159, 545-557 . Pietrewicz, A . T . & Kamil, A . C . 1979 . Search image formation in the blue jay Cvanocitta cristata. Science, N. Y., 204, 1332-1333 . Wallman, J . & Pettigrew J . D . 1985 . Conjugate and disjunctive saccades in two avian species with contrasting oculomotor strategies. J . Neurosci ., 5, 1418-1428 . Zeigler, H . P ., Levitt P. W . & Levine R . R . 1980 . Eating in the pigeon (Columba livia) . Movement patterns, stereotypy 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 and search rate hypotheses (defined elsewhere : Guilford & Dawkins 1987), Lawrence (1988) has reanalysed some of his blackbird, Turdus merula, foraging data with respect to what he calls 'scan times' . Lawrence is entirely correct that measurements of the time it takes to detect the presence or absence of food items are potentially the best way to decide between the two hypotheses . But his own scan time data can only be used in this way if (1) we can be sure that a single scan corresponds to a single decision or view, and (2) causes of the reduction in

scan time with experience other than increased detection ability (e .g . preference changes, motor ability changes) have been eliminated . We are unhappy with Lawrence's data on both accounts . (1) What is a scan? To answer our (1987) criticism of his 'residual search time' (Lawrence 1985b) being used to measure detection times, Lawrence (1988) has reanalysed his videotapes directly measuring 'scan times' . . .'the time (ms) that the bird's head remained stationary immediately following swallowing an item until the commencement of the next prey-strike' . The crucial question is whether his measured scan times are made up of just one (as he claims), or several, views each involving a decision about whether a cryptic prey item is present . If a 'scan' is made up of several such decisions, then our original objection (Guilford & Dawkins 1987), that long periods before a prey item is eaten could include several unsuccessful views, still holds . The problem with Lawrence's scans is that they are, by definition, always terminated either by prey capture (successful scans), or by a backgrounddirected peck, look, or period of vigilance (unsuccessful scans) . This seems to imply that birds never viewed more than a single piece of the background before switching to one of these different behaviours, and that it was always possible to judge every time a bird rejected a view as empty (wrongly or rightly) . We find this situation hard to accept, and we suspect, therefore, that scans do in fact sometimes constitute multiple views . Lawrence does consider this point, but rejects it on the grounds that his scan times are too short . This rejection is based on the comparability of the majority of the endogenous intervals between the eye movements (saccades) of laboratory restrained birds . However, in the study cited inter-saccadic intervals are measured under conditions 'far from what the animals would experience in their natural circumstances' (Wallman & Pettigrew 1985, page 1418), where there is little or no need for the bird to search at all . This study was done specifically in order to investigate endogenous activity rather than that associated with the search for specific targets, and it seems likely that saccades would be much more frequent (hence views much shorter) in a bird actively searching a complex environment for hidden prey . Actively foraging ring doves, Streptopelia risoria, have inter-saccadic intervals peaking at about 200 ms . For house sparrows, Passer domesticus, the modal interval is even shorter, about 100 ms (Friedman 1975) . Although Friedman's experiments measured head movements, and cannot tell us about possible eye movements within head-stationary periods, they clearly illustrate that birds can and do make use of