Behavioural transitions: a reply to roper and crossland (1982)

SHORT C O M M U N I C A T I O N S I have previously found (Brooke 1981) that leatherjackets (tipulid larvae, predominantly Tipula paludosa) were the largest and presumably most valuable food items commonly brought to nestling wheatears. In the photographed food loads leatherjackets were typically 25 m m long while other larvae and adult arthropods brought to the nest rarely exceeded 15 ram. Let us suppose that the foraging bird swallowed other prey items until it encountered and retained a leatherjacket, an item sufficiently valuable to be profitably (Royama 1970) transported to the nest. The first item in the load would then be a leatherjacket which, being soft-bodied, might be particularly suited to the 'first' position, against the gape. Any items captured after the leatherjacket would then be h d d in the bill further towards the tip. Such items would be leatherjackets significantly less often than the first caught item if, as is likely, leatherjackets were less common than other small items in the prey population. The photographed loads provided evidence that the wheatear was following such a strategy. In loads containing both leatherjackets and other items, the first-caught leatherjacket was caught before those other items 13 times but after only twice (Binomial Test, P = 0.004). In multiple prey loads the first-caught item was a leatherjacket 19 times, something else 29 times. In contrast the second-caught item was a leatherjacket nine times and something else 39 times, a significantly different distribution (Z** = 4.08, P < 0.05). The initial capture of a leatherjacket was followed by the capture of fewer subsequent items. When a leatherjacket was the first-caught item, the mean number of items caught subsequently was 0.92, distributed as follows: 0 items (7 observations), 1 item (15), 2 or more items (4). When other prey was first loaded the mean number of further items was 1.43, distributed as follows: 0 items (11), 1 item (11), 2 or more items (18). These distributions are significantly different (X~ = 7.79, P ~ 0.02). Possibly, holding a leatherjacket causes a greater decrease in prey handling ability, with the result that fewer items, but not necessarily a lesser weight of food, are brought to the nest. Leatherjackets may have an aggregated distribution (Safriel 1967), a possibility supported by the capture sequence in wheatear loads. When the first item was a leatherjacket then the second item was also a leatherjacket in 36.8 % (7/19) of loads but when the first item was something else the second item was a leatherjacket in only 6.5 % (2/29) of loads (Fisher Exact Test, P = 0.012). If leatherjackets are aggregated a change in search strategy following the capture of a leatherjacket could be advantageous to the wheatear. In conclusion, wheatears often began loading w i t h leatherjackets, the largest common prey, but then took either leatherjackets or other smaller items. The circumstances in which it is optimal for the loading animal to specialize (on large items) or generalize (taking small or large items as they are encountered) at different points in the loading sequence is under consideration by A. I. Houston. I thank D r C. M. Perrins and the Edward Grey Institute for facilities and Luc-Alain Giraldeau, Alasdair Houston and Alex Kacelnik for comments. M. DE L. BROOKE

Edward Grey Institute, Zoology Department, South Parks Road, Oxford OX1 3PS U.K.

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References Brooke, M. de L. 1979. Differences in the quality of territories held by wheatears (Oenanthe oenanthe). J. Anim. Ecol., 48, 21-32. Brooke, M. de L. 1981. How an adult wheatear (Oenanthe oenanthe) uses its territory when feeding nestlings. J. Anim. Ecol., 50, 683-696. Davies, N. B. 1977. Prey selection and the search strategy of the spotted flycatcher (Muscicapa striata): a field study on optimal foraging. Anita. Behav., 25, 1016-1033. Orians, G. H. & Pearson, N. E. 1979. On the theory of central place foraging. In: Analysis of Ecological Systems (Ed. by D. J. Horn, G. R. Stairs & R. D. Mitchell), pp. 155-177. Columbus, Ohio: Ohio State University Press. Royama, T. 1970. Factors governing the hunting behaviour and selection of food by the Great Tit (Parus maior L.). J. AnOn. Ecol., 39, 619-668. Safriel, U. N. 1967. Population and food study of the Oystercatcher. D.Phil. thesis, University of Oxford. Tinbergen, J. M. 1981. Foraging decisions in Starlings (Sturnus vulgaris L.). Ardea, 69, 1-67.

(Received 15 June 1982; revised 15 October 1982; MS. number: sc-133) Behavioural Transitions: a Reply to Roper and Crossland (1982) In their introduction, Roper & Crossland (1982) complain that McFarland's (1969, 1974) concepts of disinhibition and time-sharing do 'not allow one to identify in absolute terms the activity whose CFS (causal factors) is changing (or, alternatively, the direction of the change).' The trouble starts with their interpretation of McFarland's (1969) Fig. 1, v i z . ' . . , the way his figures are drawn suggests that the lines were intended to depict absolute changes in CFS . . . . '. McFarland's (1969) figures were intended purely as illustration, the operational definitions being given in words. Moreover, McFarland (1969) makes it clear that, 'Although there does appear to be an operational distinction between competition and disinhibition, which can usefully be applied to the analysis of behavioural mechanisms, it is not necessary for particular mechanisms to be tied to particular behavioural situations, though this may be true for certain stereotyped activities. There are probably many mechanisms by which one activity can come to follow another, and many types of competition and disinhibition'. In seeking to identify competition and disinhibition with particular directional changes in the level of causal factors, Roper & Crossland (1982) are in my view making a mistake. The key to the problem seems to be contained in the first paragraph of their page 603. As a consequence of their interpretation of McFarland's graphs, Roper & Crossland (1982) criticize their own version of McFarland (1969), and conclude that it is worthless. I agree with them here. Others have also noticed the different ways in which McFarland and Roper use the term disinhibition. Houston (1982) points out 'Staddon does not relate his terms to those o f McFarland but it is clear that his use of disinhibition is the same as that of Roper (1978) and different from that of McFarland (1969)'. Roper & Crossland (1982) report some experiments on rats from the results of which they conclude that transitions between eating and drinking do not provide in-

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stances of disinhibition or time-sharing. In this. respect their conclusions are similar to those of McCleery (1977) who worked on rats, and dissimilar from those of McFarland (1969, 1970, 1974); McFarland & L'Angetlier (1966); McFarIand & Lloyd (t973); and Larkin & McFarland (1978) who worked on doves. This apparent difference between rats and doves does not permit Roper & Crossland to 'suggest that disinhibition rather than being a common mechanism of behavioural switching, is limited to a relatively small number of activities where for some special reason the decline in CFS consequent on performance is abrupt rather than gradual'. It is possible that rats and doves differ in some respects and it is incautious of Roper & Crossland to imply that their findings in rats should have precedence over other workers' findings on other species. In their general discussion, Roper & Crossland (1982) are clearly confused about the different levels at which interactions carl occur between motivational systems. They seem (final paragraph) to regard all interactions between causal factors as reciprocal and equivalent. I find this disappointing, because the possible levels of interaction and the ways in which they can be distinguished have been spelled out in detail by McFarland (1971, p. 223-228; 1978, p. 379-385). and McFarland & Houston (1981, p. 1-6). Possible interactions between the feeding and drinking systems and their implications in a time-sharing situation are discussed by McFarland (1974). So important do I regard the distinction between these different levels of motivational interaction that it seems worth giving an example. Epstein et al. (1970) observed that a starving rat, which h a d just been allowed to start eating, changed to vigorous drinking when injected with angiotensin intraeranially. The question is--in what sense does intracranial angiotensin inhibit feeding? We can imagine that angiotensin is such a powerfnl inducer of thirst that the rat would have changed to drilxking even if it had been copulating at the time of the injection. We would not want to conclude that anNotensin inhibited the tendency to copulate, because it is possible that the rat would have changed to drinking whatever it had been doing at the time of the injection. To determine whether angiotensin inhibited the tendency to feed rather than inhibiting feeding itself (by competition in the behavioural final common path), McFarland & Rolls (1972) tested rats in a situation in which they had prior experience of eating but no experience of drinking, and in which there were no drinking cues. They found that feeding was suppressed by angiotensin. To test whether this suppression was due to a direct effect of angiotensin on the feeding tendency, or due to an increase in thirst which then suppressed the feeding tendency, Rolls & McFarland (1973) administered rats with a gastric preload of water at the time of angiotensin injection. The preload was calculated to annul the thirst-inducing effects of the angiotensin. They found that the suppression of feeding by angiotensin was abolished by this procedure. Rolls & McFarland concluded that angiotensin does not act directly upon the feeding system, but rather acts on the thirst system which in turn suppresses the tendency to feed, for which there is also other evidence. The lesson from this study is that one has to be careful to distinguish between the apparent inhibitory effect of one motivational system on another which is due to interaction between the tendencies to perform the relevant activities, and that which is simply due to the fact that the animal can only perform one activity at a time and may have to abandon one in order to perform the other. If the discussion of Roper &

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Crossland is read with this example in mind, the reader can draw his or her own conclusions. Finally, it is perhaps worth emphasizing that an operational approach is logically distinct from a mechanistic or model-making approach. Thus it should not surprise Roper & Crossland (1982) that the 'operational definition is therefore an incomplete guide to the nature of the underlying processes'. The value of an operational approach is that it enables the investigator to make a sensible start in the analysis of complex processes. Too often, behavioural problems are approached on a basis of ad hoc preconceptions. In the area of analysis of behaviour sequences it was long assumed that the different activities have equal status, and that the greatest influence on a particular activity would be the activity that just preceded it. I never thought that these were very realistic ideas. By operationally defining behavioural transitions and activities it has become possible, by simple experimental methods, to assess the status of the components of behaviour sequences. Such an exercise may lead to interesting discoveries and it provides a prelude, but only a prelude, to analysis of the underlying motivational mechanisms. DAVID MCFARLAND

Animal Behaviour Research Group, University of Oxford, Oxford. References

Epstein, A. N., Fitzsimmons, J. T. & Rolls, B. J. 1970. Drinking induced by injection of angiotensin into the brain of the rat. d. Physiol., 210, 456474. Houston, A. E. 1982. Transitions and time-sharing. Anita. Behav., 30, 615-625. Larldn, S. & McFarland, D. 1978. The cost of changing from one activity to another. Anim. Behav., 26, 1237-1246. McCleery, R. H. 1977. Temporal organisation of feeding and drinking behaviour. D.Phil. thesis, University of Oxford. McFarland, D. J. 1969. Mechanisms of behavioural disinhibition. Anita. Behav., 17, 238-242. McFarland, D. J. 1970. Adjunctive behaviour in feeding and drinking situations. Rev. eomp: Anita., 4, 64-73. McFarland, D. J. 1971. Feedback Mechanisms in Animal Behaviour. London: Academic Press. McFarland, D. J. 1974. Experimental investigation of motivational state. In: Motivational Control Systems Analysis (Ed. by D. J. McFarland), pp. 251-282. London: Academic Press. McFarland, D. J. 1978. Hunger in interaction with other aspects of motivation. In: Hunger Models (Ed. by D. A. Booth). London: Academic Press. McFarland, D. J. & L'Angellier, A. B. 1966. Disinhibition of drinking during satiation of feeding in the Barbary dove. Anita. Behav., 14, 463--467. McFarland, D. J. & Houston, A. 1981. Quantitative Ethology. London: Pitman Books. McFarland, D. 3. & Lloyd, I. H. 1973. Time-shared feeding and drinking. Q. J. exp. PsyehoL, 25, 48-.61. McFarland, D. J. & Rolls, B. J. 1972. Suppression of feeding by intracranial injection of angiotensin. Nature, Lond., 236, 172-173.

SHORT C O M M U N I C A T I O N S Rolls, B. J. & McFarland, D. J. 1973. Hydration releases inhibition of feeding produced by intracranial angiotensin. Physiol. Behav., 11, 881-884. Roper, T. J. 1978. A possible function for tinae-sharing. Anim. Behav., 26, 1277-1278. Roper, T. J. & Crossland, G. 1982. Mechanisms underlying eating-drinking transitions in rats. Anita. Behav., 30, 602-614.

(Received 25 June 1982; revised 29 September 1982; MS. number: sc-134) Time Sharing: a Reply to Houston (1982) Houston (1982) claims to have discovered flaws in current conceptions of time sharing in animal behaviour. There are so many points that I disagree with that I think the best procedure is to quote passages from his paper and append my comments beneath. (1) 'With the definition of time sharing established, McFarland's use of 'inhibition' can be considered . . . '. (page 618). Up to this point I agree with Houston's exposition (apart from his remarks about Atkinson & Birch). In what follows, however, Houston adopts the same tactic as Roper & Crossland (1982). He takes specific hypothetical cases of changing causal factors and worries about whether or not time-sharing will occur. While there is nothing wrong with devising ad hoc models, if that is thought to be worthwhile, it is difficult to see how such models can be used to criticize an operational concept such as time-sharing. Houston's examples (Fig. 3) may or may not give rise to time-sharing, depending upon the exact details of the methods employed in recording the observed behaviour. 1 agree that it is legitimate to criticize the value of an operational concept, but I maintain that the value of the time-sharing concept lies in its challenge to conventional theory, particularly the implication that there are fundamental asymmetries in the temporal organization of behaviour (see below). Anyone interested in investigating time-sharing has first to demonstrate that it occurs, and this has been the aim of most of the studies so far published. There are many phenomena which are similar to time-sharing, such as temporary satiation and pacemaker phenomena. These can be experimentally distinguished from timesharing, but the question of what underlying mechanisms are responsible is not one that can be settled in an armchair. (2) 'In Fig. 2 imagine that in the diagram of time sharing, the changes in the level of causal factors for activity A o ~ u r at fixed times. Then over a wide range of the level of causal factors for activity B, the sequence will not change and so time sharing is occurring. But because the transitions occur as a function of time elaosed, each activity can b e masked, so there is no domint activity (page 619). In interpreting both this and the following passage it should be remembered that time-sharing is characterized by McFarland (1974a, b) as a situation in which the effects of interrulations are asymmetrical. In other words, interruption of activity A has one effect, while interruption of activity B has the other. There will obviously be many situations which show masking but not time-sharing. One of these is the pacemaker situation described in t h e above quotation. Houston seems to think, however, that these somehow invalidate interruption methods in general. MeFarland (1974b) shows that many different interrulation techniques can be used to detect time-sharing. None is perfect, but when the results of interruptions are systematically asymmetrical and

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when other evidence points in the same direction then it is reasonable to conclude that time-sharing is occurring. (3) I disagree with the following statements on purely factual grounds. Since available space does not permit me to spell out any details, I have simply appended references to counter-examples. (a) 'Evidence for positive feedback in the system controlling drinking in the Barbary dove was found by McFarland & McFarland (1968), but the importance of this for the interpretation of masking experiments has been overlooked' (page 622). See, however, McFarland (1969, 1974b), Sibly (1975) and Sibly & McCleery (1976). (b) 'All the experiments reported by Cohen & McFarland (1979) and McFarland (1974a) are tests for masking rather than time sharing' (page 623). I recommend reading Cohen & McFarland (1979) and McFarland (1974a). (c) 'The work of Brown & McFarland (1979) is the only systematic attempt to test for time sharing rather than masking' (page 623). See however, Cohen (1979); Cohen & McFarland (1979). (d) 'Much of the work in this area has been concerned with dominance boundaries (i.e. masking) rather than time sharing' (page 623). See however, McFarland (1970, 1974a). In short, there are a number of published studies in which implications of time-sharing theory were tested by methods which do not depend on masking. (4) 'It has been claimed by McFarland (1974b) that the dominance boundary may also be the switching line. I do not see how this can be so. The dominance boundary and switching line may sometimes have the same position in deficit space, but they are logically distinct' (page 622). What McFarland (1974b) actually said was 'it is worth noting that, from a priori considerations, there must be a boundary somewhere in the state plane, on one side of which hunger state is greater than thirst state, and vice versa. Whether this boundary is the same as the dominance boundary is, of course, an empirical matter. - - This does not mean that resumption of feeding or drinking following interruption can be used as evidence for hunger or thirst primacy. The question of complete concordance between dominance and primacy is a matter for further investigation' (page 266). McFarland & Sibly (1975) showed that the phenomenon of dominance-boundary rotation was consistent with their theory, if it was assumed that the dominance boundary and switching line were isomorphic. It is true, as Houston says, that the two are logically distinct, but the question is, are they logically incompatible. I think not. (5) 'It was not realized that time sharing is incompatible with many optimality models. To illustrate this point, consider the model of optimal feeding and drinking proposed by Sibly & McFarland (1976)' (page 620). In fact, the relationship between this model and the data on time-sharing has been the subject of lengthy discussions between various people. Sibly & McFarland (1976) were among the first to attempt to apply dynamic optimization ideas to animal behaviour. However, they did not make a distinction between optimization with respect to a cost function and optimization with resDeet to a goal function. A distinction of this type was first suggested by McFarland (1977), and is discussed at length by MeFarland & Houston (1981). In my view this distinction lies at the root of Houston's problem. Houston (1982) would be correct in asserting that time-sharing would be non-optimal with resgect to a cost function. In other words, I agree that the best policy for maximizing fitness in a given environment would not be achieved by time-sharing. However, the