On parental investment during the breeding season

SHORT C O M M U N I C A T I O N S telephone but it is not identical when sonagraxm~aed. The first of the two trills which normally make it up is rather brief and is mainly frequency- rather than amplitudemodulated, as well as showing a slower pulse repetition rate at the outset. Occasionally, the bird produced three trills, in which case the third was like the second. The interval between trills is slightly shorter than that of the telephone, the frequency range is rather broader and centred about 200 Hz lower. When the bird produced two pairs of trills in a row, as it often did, these were less than 1 s apart (see Fig. lc). The number of pulses in the second trill ranged from 9 to 12 over four examples, and the pulse repetition rate from 28.5 to 30.l/s, giving a very accurate match to the telephone. There seems no doubt that this particular song thi'ush phrase has been copied from a trinaphone: the proximity of such a phone to the bird suggests that this individual may have copied it directly, although the lack of precise match may mean that the sound has passed through a number of tiu-ushes since originally learnt. While it has not been previously documented, the copying of trimphones by thrushes appears to be a very connnon occurrence. It has been commented on to me by several peopIe from other areas of Britain: in two cases, in Surrey and Claekmarmanshire, the bird involved was a blackbird (Turdus merula) rather than a song thrush. Tretzel (1965, 1967) has also described the incorporation of man-made sounds into song traditions amongst birds. In one case, blackbirds were found to sing a series of whistles originally copied from a man, with the quality of the copy being greater in those birds closer to where the man lived (Tretzel 1967). This suggests that some birds within the group had copied from each other rather than directly from the man. Song thrushes have a highly varied song, each bird having approximately 150-200 phrases, some of which are shared between individuals close to each other (Ince 1981). This suggests that, like many other passerine birds (Kroodsma 1978), they do copy phrases from each other; however, mimicry of other species or sounds is not a normal feature of their song. Because it can be learnt independently from many sources all over the country, and then be passed from thrush to tka'ush, the trimphone imitation has the potential to become widespread amongst British thrushes. Why should it, of all possible sounds, have been the one to penetrate into song thrush repertoires ? The answer seems to be that it provides a near perfect match with what Marler (1976) calls the sensory template of the species, the filter that normally only lets species-specific sounds past. Its frequency is close to that of other elements in the song, and the fact that each phrase consists of two units which are repeated after a short interval also makes it like a song thrush. Each song thrush phrase consists of one or more elements, and if there are more than one these are produced in quick succession and may be the same as each other or different. The most distinctive feature of the species is that each phrase tends to be repeated several times with a short interval between the repetitions. These features are exactly those shown by the trimphone: it has a phrase consisting of two identical trills which is repeated every 2 s. A 2 s interval would be long for that between repetitions of the same phrase in a song thrush and, indeed, the bird described here incorporated a shorter one in its imitation: Although not as striking perhaps, the phenomenon described here has similarities to that of milk-bottle-top opening in tits (Fisher & Hinde 1949; Hinde & Fisher

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1951); a change in animal behaviour brought about by a h u m a n artefact and then passed culturally from one individual to another. I refer to it as the Buzby phenomellon in honour of the bird of that name used in British Telecom advertising. Its species is somewhat indeterminate, but it seems likely that it should be placed in the genus Turdus. P. J. B. SLATER

Ethology & Neurophysiology Group, School of Biology, University of Sussex, Brighton BN1 9QG. References

Fisher, J. & Hinde, R. A. 1949. The opening of milk bottles by birds, Br. Birds, 42, 347-357. Hinde, R. A. & Fisher, J. 1951. Further observations on the opening of milk bottles by birds. Br. Birds, 44, 392-396. Ince, S. A. 1981. Comparative studies of singing in thrushes. D.Phil. thesis, University of Sussex. Kroodsma, D. E. 1978. Aspects of learning in the ontogeny of bird song: where, from whom, when, how many, which and how accurately. In: The Develop-

ment of Behavior: Comparative and Evolutionary Aspects (Ed. by G. M. Burghardt & M. Bekoff),

pp. 215-230. New York: Garland Publishing. Mm'ler, P. 1976. Sensory templates in species specific behavior. In: Simpler Networks and Behavior (Ed. by J. C. Fentress), pp. 314-329. Sunderland, Mass. : Sinauer Associates. Tretzel, E. 1965. Imitation und Variation yon Sch~iferpfiffen durch Haubenlerchen (Galerida c. cristata (L.)). Ein Beispiel fiir spezielle SpottmotivPrfidisposition. Z. Tierpsychol., 22, 784-809. Tretzel, E. 1967. Imitation menschlicher Pfiffe dutch Amseln (Turdus m. meruIa). Ein weiterer Nachweis relativen Lernens und akustiscber Abstraktion bei V6geln. Z. TierpsychoL, 24, 137-161.

(Received 9 September 1982; revised 4 November 1982; MS. number: so-141) On Parental Investment During the Breeding Season Biermann & Robertson (1981) maintain that the parental investment of female redwinged blackbirds (Agelaius phoeniceus) increased during the breeding season, thus comfirming a prediction of parental investment (PI) theory (Trivets 1972; Planks 1974). However, I question (1) their method of assessing PI, (2) their analysis of the data, rind consequently, whether they have demonstrated an increase in PI. Fttrthermore, their results do not constitute a test of PI theory because (3) the 'prediction' they tested does not necessarily follow from Pianka's (1974) original prediction, and (4) results opposite from those obtained could have been used to cortfirm the same 'prediction' with equal facility. (1) Aggression toward a nest predator (a rubber snake) was used as a measure of 'relative parental investment'. Aggressive behaviour constitutes an appropriate measure of PI only if, (Trivers 1972) aggression increases the offspring's chance of survival; this has yet to be demonstrated. Aggression toward a potential predator may even decrease the survival of current offspring, since, were the female to be killed defending the nest, her offspring would likely die as well. Aggression was measured by assigning 'behavioural scores' to behavioural acts and multiplying by a 'duration

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ANIMAL

BEHAVIOUR,

score'. The scores were scaled 'to reflect what we felt were differences in aggression', and consequently were subjective. Biemaann & Robertson's insight that PI is multidimensional (i.e. involving movement, vocalization, etc.) is undoubtedly correct, but the problem lies in their attempt to reduce the multidimensionality to a single scalar. Using their approach, the conclusion that PI increases or decreases may hinge on the subjectively determined function that weights the behaviourat dimensions. (2) Since the stated intention of the investigators was to 'rank the females' aggression', non-parametric analysis o f the data would have been most appropriate. Their analysis, using standard parametric techniques, is not valid since the scale they constructed was not an interval scale (Siegel 1956). (3) The original formulation of the prediction that Biermann & Robertson claimed to test w a s , ' . . , that as an organism's reproductive value falls.., its reproductive effort should rise' (Pianka 1974, page 213). Pianka was referring to residual reproductive value (v% = residual reproductive value at age x) which is defined (Pianka & Parker 1975, page 454) as the product of reproductive value at age x + 1 ( = v~+D and the probability of surviving from age x to age x + l ( = p~). If reproductive effort at age x ( = R~) increases as v% declines, this implies Rx+l > Rz provided that v% > v%+1. If we let a = age of a female breeding early and a + 1 = age of a female breeding late in the season, then we seek conditions under which v% > v*,+~. We can substitute V*a = ffaVa+l, by definition, and v*a+~ -- va§ -- m,~ (where m~ -- fecundity at age x) by definition of v~+l. U p o n rearrangement we obtain the inequality ma+l > (1--pa)va+l.

(1)

Thns whether R,+I is greater thau R~ depends on the values that m,+l, p , and v,+z take. For most birds p , will be high (close to 1) and v,+l will vary little, but ma+l will vary markedly depending on the likelihood of nest-predation. When the probability of nest-destruction is sufficiently high m~+~ will be low and reproductive effort should decrease from a to a + 1. That is, relatively low investment in reproduction at a is adaptive only if fecundity at a + 1 is high and the probability of surviving from a to a + l is high. Biermann & Robertson do not provide sufficient data to calculate whether equation (1) holds and so we cannot predict whether R ,~hould increase or decrease during the breeding season. (4) If we do accept the authors' application of Pianka's prediction, were the observed changes in aggressive behaviour as predicted ? Biermann & Robertson found that the response scores of females with clutches late in the nesting period were lower than the scores of females nesting in the early and mid-season. In contrast, latenesting females with broods showed a higher level of nest-defence than did earlier-nesting females. Biermann & Robertson argue that this set of observations is consistent with PI theory, but an equally plausible argument could be constructed had the opposite results been obtained (i.e. a decrease in brood-defence and an increase in clutch-defence during the breeding season). Such latitude is possible because Pianka's prediction did not distinguish between stages of the breeding cycle and because we are ignorant of the costs and benefits associated with nest-defence. Since antithetical sets of results

31,

1

could each be considered consistent with PI theory, no one set of results can be considered to confirm a prediction of such theory. Biermann & Robertson's argument is neither compelling nor consistent with their data. They suggest that the low level of nest-defence of late-nesting females with clutches may act to 'improve their chances of surviving to the next breeding season', but this factor should apply with equal force to early and mid-season nesting females, as well as to late-nesting females with broods. They argue that late in the season females with broods are more aggressive than females with clutches because the reproductive value of a clutch (which is less than that of a brood) does not justify the risk of nest-defence. This argument applies equally well to earlier-breeding females yet the mean response of females with broods was lower, though not significant, than that of females with clutches. They explain these results as follows, 'During these periods the probability of a nest being preyed upon was small (Fig. 1) so that the females could devote more energy to other forms of parental investment'. This a posteriori explanation is doubly flawed: (i) Biermann & Robertson have assumed that these females have witheld investment in nest-defence because the energy is best invested in other activities. However, energy is probably not the critical variable with respect to nest-defence. The critical variables are the anticipated benefit if the female successfully defends the nest, the probability of successfully rearing a replacement brood, and the anticipated co~t of defending the nest. Note that Pianka's prediction referred to total reproductive effort and not to the way effort might be partitioned into nest-defence and other activities. In effect, Biermann & Robertson are arguing that the proportion of total PI represented by nest-defence varies with the season and that therefore nest-defence is not a reliable indicator of total PI. (ii) The overall probability of predation may be low early in the season, but the behaviour of the female confronted with a nest predator should reflect the risk of nest-destruction given that a predator is in or at the nest. I do not deny that female nest-defence behaviour changed during the breeding season nor that we can formulate hypotheses, consistent with PI theory, to account for the changes. However, there is much reason to doubt that Biermann & Robertson have demonstrated 'an increase in parental investment during the breeding season'. Meanwhile a test of PI theory will have to wait until investigators can quantify the costs and benefits associated with a behavieur pattern. I thank K. Yasukawa and G. Biermann for helpful comments. NADAV NUR

Department of Zoology, Tel Aviv University, Tel Aviv, Israel, 69978 References Biermann, G. C. & Robertson, R. J. 1981. An increase in parental investment during the breeding season. Anita. Behav., 29, 487-489. Pianka, E. R. 1974. Evolutionary Ecology. New York: Harper & Row. Pianka, E. R. & Parker, W. S. 1975. Age-specific reproductive tactics. Am. Nat., 109, 453-464. Siegel, S. 1956. Nonparametric Statistics.for the Behavioral Sciences. New York: McGraw-Hill.

SHORT C O M M U N I C A T I O N S Trivers, R. L. 1972. Parental investment and sexual selection. In: Sexual Selection and the Descent of Man, 1871--1971 (Ed. by B. Campbell), pp. 135179. Chicago: Aldine.

(Received 27 January 1982; revised 21 July 1982; MS. number: AS-170A) Residual Reproductive Value and Parental Investment Parental investment theory (Trivers 1972) coupled with theories on age-specific reproductive tactics predict that an individual will increase investment in a given reproductive event as its residual reproductive value decreases (Pianka 1974, page 213). A clear distinction should be made between two types of temporal change in parental investment (PI). (1) Through a given breeding cycle (e.g. nest building to fledging), changes in PI are largely a function of increasing reproductive value of the offspring, and the expected cost/benefit ratio of succeeding with the present breeding effort versus renesting. (2) Through a breeding season (e.g. early spring to late summer), after removing effects of stage of the breeding cycle, changes in PI are largely a function of the residual reproductive value of the parent. Due to the decreasing probability of successfully renesting in the present season, and the high probability of over-winter mortality, residual reproductive value is much lower at the end of the season. Our study removed breeding cycle effects by examining nest defence aggression at particular stages of the cycle through the season. Contrary to Nur's claim (Nur 1983), studies by Robertson & Norman (1977), Andersson et al. (1980), Greig-Smith (1980) and Blancher & Robertson (1982) all indicate that nest defence does in fact increase the offspring's probability of survival. Searcy (1979), cited by Nur as evidence that predator defence might increase rather than decrease rates of predation on young, was based only on nests in which at least one young fledged. Thus, it is possible that males with low response scores had their entire nests preyed upon during the egg or nestling stage, whereas males with greater response scores had only partial losses of young. In criticizing o u r system for scoring nest defence aggression, Nur argues that vocalization represents decreased PI. Vocalization and associated behaviour are likely to involve a high level of risk since it may attract the attention of both the nest predator and any other predators in the area. Any risk incurred can be considered PI if it increases the probability of survival for the present offspring while it reduces the probability of the parent being able to invest in future offspring (Trivers 1972). Searcy (1979), Andersson et al. (1980), Greig-Smith (1980), and others, have also used calling rate or intensity as an indicator of level of nest defence aggression. It is true the assessment of levels of nest defence behaviour involves some subjective evaluation by the observer. However, if the scoring scheme is consistently applied and involves reasonable assumptions regarding the risk of various behaviours to the bird, then quantification of nest defence can be undertaken. Nur properly criticizes our use of parametric statistics. Reanalysis of the scores using the Kruskal-Wallis rank test and the Mann-Whitney U-test (Conover 1980) results in probability values similar to those reported in the original paper. In his analysis of residual reproductive value early in the season relative to late in the season, and the consequences on reproductive effort at those times, N u t over-

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looked the fact that nests lost late in the season cannot be replaced until the next breeding season, and that the probability of surviving to the next season is much lower than the probability of surviving from tile begin1ring to the end of a given breeding season. It is precisely these factors that reduce residual reproductive value late in the season and favour increased nest defence at that time. Although the probability of nest predation is higher late in the season, it is not sufficiently high to counteract the effect that the low over-winter survivorship has on increasing potential reproductive effort at tile end of the season. Contrary to Nut's claim that 'an equally plausible argument could be constructed had the opposite results been obtained', such results would not have been consistent with PI predictions: females would have incurred a greater risk for a less valuable nesting attempt, because clutches represent a lower potential reproductive success with a larger expected cost than do broods (Dawkins & Carlisle 1976; Boucher 1977). N u t makes an important point regarding the multidimensionality of PI. Risk, time, and energy are separate tbrms of investment that are not always correlated at any particular part of the breeding cycle or season. However, according to the principle of allocation (Cody 1966), there would likely be a negative correlation between these forms of investment, especially for time and energy. As Nur points out, energy is not the critical variable with respect to nest defence. The greatest costs are likely to be measured in units of probability of survival (risk). With nest defence, it is the willingness to undertake risk, rather than the average risk taken, that should be considered as the level of PI. Defence also involves some time and energy costs, so a female confronted with both a predator and hungry nestlings would have to resolve the conflict whether to defend or feed. In a hierarchy of types of PI, nest defence should have top priority, since if a nest is lost to a predator, other forms of PI would be meaningless. Yet a female, having found the predator (model snake) immune to her attack, may give up sooner to forage for her nestlings than if she did not have this conflicting demand. Our earlier work (Robertson & Biermann 1979) and Greig-Smith's (1980) indicates there are trade-offs be.tween level of defence and other forms of time and energy expenditure. Clearly, further experimental approaches to investigating how these conflicts are resolved are needed. We thank D. Leffelaar and P. Weatherhead for helpful comments on the manuscript. GLORIA C. BIERMANN*

*Department of Zoology, University of Manitoba, Winnipeg, Manitoba Canada R3T 2N2. RALEIGH J. ROBERT$ONt

t Department of Biology, Queens' s University, Kingston, Ontario Canada K7L 3N6. References Andersson, M., Wilklund, C. G. & Rundgren, H. 1980. Parental defenee of offspring: a model and an example. Anim. Behav., 28, 536-542. Biermann, G. C. & Robertson, R. J. 1981. An increase in parental investment during the breeding season. Anim. Behav., 29, 487-489. Blancher, P. J. and Robertson, R. J. 1982. Kingbird aggression: does it deter predation? Anim, Behav., 30, 929-930.