Do male zebra finches learn their fathers' songs?

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A:lim. Behav. 38, 637-642 12 Wolff, 1.0. (19891 in Advances in the Siudy of Peromyscus (Kirkland, G.L., Jr and L;:yne. J.N., edsl, pp. 271-291, Texas Tech Utliversity Press I3 jeppsson, B. (19861 Behav. &co/. SI Iciobiol. 19, 293-296 I4 Wolff, I.O., Freeberg, M.H. and Dueser, 12, R D. ( 19831 Behav. Ecol. Sociobiol. 2 ; 7-242 I4 Wolff, J.O.11985) Anim. Behav. 33, 117-123 lb McShea, W.1. and Madison, D.M. (1984) C,tn. 1. Zoo/. 62, 344-346 I:’ Madison, D.M. and McShea, W.I. II9871

Am. Zoo/. 27,899-908 18 Madison, D.M. in Social

Systems and Population Cycles in Voles (Tamarin, R.H., C jtfeld, R.S., Pugh, S.R. and Bujalska, C., e&l, Birkhaiiser Verlag (in press) 1’1 Ostfeld, R.S. and Klosterman, L.L. in Social Systems and Population Cycles in \/(,/es ITamarin, R.H., Ostfeld. R.S., Pugh, S.R and Bujalska, G., edsl, Birkhatiser Verlag (in p -essl

20 Ostfeld, R.S., Lidicker, W.Z., lr and Heske, E.]. (1985) Oikos 45,433-442 21 Ims. R.A. II9871 Am. Nat. 130, 475-484 22 Myllymiki, A. (1977) Oikos 29, 553-569 23 Viitala, I. ( 19771 Ann. Zoo/. Fenn. 14, 53-93 24 Wolff, 1.0. and Cicirello, D.M. Anim. Behav. (in press) 25 Ims, R.A. II9881 Nature 335, 541-543 26 Emlen, ST. and Oring, L.W. II9771 Science 197. 2 15-223 27 Alibhai, S.K. and Gipps. I.H.W. (1985) in

The Ecology of Woodland Rodents, Bank Voles and Wood Mice (Flowerdew, I.R., Curnell, I. and Gipps, I.H.W., edsl, pp. 277-3 13, Oxford Science Publications 28 Mares, M.M. and Lather, T.E., Ir (19871 Am. Zoo/. 27, 293-306 29 Schoener, T.W. (1987) Am. Zoo/. 27, 259-29 I 30 Ims. R.A. II9871 Oikos 50, 103-I I3 31 McShea. WJ. (1989) Oikos 56, 182-186 32 Kawata, M. (1985) Oikos 45, 181-190 33 Knowlton, N. (19791 Anim. Behav. 27, 1022-1033

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A4ale zebra finches learn their songs wry early in life, before they are sexus//y mature. The father has been suggested as a likely song model at this stage. But do they actually learn from him? Though several recent pspers examine this issue, it is not an e 3sy matter to resolve. -. All songbirds studied to date have been found to learn details of their songs from other individuals’. In s3me cases, learning may take place throughout life, but it is usually res tricted to a shorter period when the bird is young. In most species, song is restricted to males, and several cases have been described where they learn at the time when they are setting up territories2. This probably allows them to match the songs of their neighbours and thereby interact with each other by countersinging. In other cases, young males may learn earlier than this so that their song is memorized while they are juveniles, even though it is not produced until they are young adults3. This process of memorizing song long before it is recalled and used is a very remarkable one, but it remains i‘nclear just what advantage the young bird gains by it. What is becoming increasingly clear from recent work is that social interaction is an important factor in song learning4. The young of some species will not learn from tape-recordings, and even P.J.B. Slater and N.I. Mann are at the Dept of Biology and Preclinical Medicine, University of St Andrews, Fife KY16 9TS, UK.

34 Davies, N.B. and Houston, A.I. (19841 in Behavioural Ecology: An Evolutionary Approach (Krebs, I.R. and Davies, N.B., edsl, pp. 148-169, Sinauer Associates 35 Getz, L.L., Hofmann, I.E. and Carter, C.S. ( 1987) Am. Zool. 27,909-920 36 FitzGerald, R.W. and Madison, D.M. (19831 Behav. Ecol. Sociobiol. 13, 183-187 37 Boyce, C.C.K. and Boyce, I.L., Ill (1988) 1. Anim. Ecol. 57, 71 l-722 38 Cetz. L.L. and Hofmann, I.E. (19861 Behav. Ecoi. Sociobiol. 18, 275-282 in 39 Gittleman, I.L. ( 1989)in Perspectives Ethology (Vol. 8) (Bateson, P.P.C. and Klopfer, P.H., edsl, pp. 55-81, Plenum Publishing 40 Ridley, M. (19831 The Explanation of Method Organic Diversity: The Compararive and Adaptations for Mating, Clarendon Press 41 Saitoh, T. (1985) 1. Ethel. 3, 143-149 42 Boonstra, R. and Rodd, F.H. (19831 I. Anim. Ecol. 52, 757-780 43 Bujalska, C. ( 19851 Ann. Zoo/. Fenn. 22, 33 l-342

DoMaleZebraFinches Learntheir Fathers’ Songs? P.J.B. Slater and N.1, Mann in those that will do so, they may be more prone to learn from a live tutoF. Song learning may thus be guided by interaction with other individuals. This is certainly true of the relationship between young males and their territorial neighbours in some species*. In cowbirds (Molothrus ater), which are brood parasites, it has even been found that the prefer1ences of females can influence the songs that males develop”; males that are housed with females of another subspecies develop songs typical of that subspecies rather than of their own. That both territorial neighbours and potential mates can affect song development should not surprise us, given that song is well established as having a role in both the repulsion of rivals and the attraction of mates. But what of song that is learned well before maturity, when the young bird is a fledgling and probably still in the area where it hatched? Could it be that young males that learn at this stage do so from their fathers? Given the fact that social relationships have been found to be important in song learning, this seems very likely. Song and kinship There has been long-standing interest in the idea that male birds might learn their songs from their

0 j :990 ElsrvierScterce Pubshers Ltd UK! 0169~5347'90,$0200

fathers. If they did so, there would be some very interesting possibilities: for example, males might cooperate more with individuals sharing songs with them, and females might use song as a cue in mate choice to achieve an optimal degree of inbreeding or outbreeding’. Unfortunately, the evidence lags sadly behind. While many bird species are known to learn song as fledglings, direct evidence that it is their father that they learn from is missing. Young male Darwin’s finches of at least three species (Geospizaspp.) tend to sing the same song types as their fathers, but then so do other males8,g. One could only be sure that they had learned from him if their song matched his more precisely than that of any other male. In the laboratory, bullfinches (Pyrrhula pyrrhula) have also been found to copy from their fatherslO, but the artificiality of laboratory housing, keeping them close to the father for longer than normal, might have forced this upon them. When do zebra finches learn? A third species for which learning from the father has been suggested is the zebra finch (Taeniopygia guttata), a favourite for the study of song learning ” . It occurs in Australia in semi-arid environments, where it 415

TREE vol. 5, no. 72, December

trasts with those of other studies”, the explanation may be quite simple. Bohner’s birds were placed in visual and partial auditory isolation after separation from their parents. Those isolated at 35 days thus lacked stimulation from other birds after independence, and this may have been why they recalled and used songs heard much earlier in life than those they would usually copy. Bohner’s result thus gives an interesting insight into the mechanisms of development, but not one likely to shed light on the normal course of events in the wild.

An adult male zebra finch shows directed ling. Drawing by N.I. Mann.

song to a fledg-

forms loose colonies in which breeding occurs rapidly in responseto rainfall. The species is also easily kept and bred in the laboratory and, with young males maturing at around 90 days, it has the advantage that song learning experiments do not require a long wait for results. The original laboratory studies were carried out by Immelmann. He found that young males would learn the song of a Bengalese finch (Lonchura striata var. domestica) foster father very precisely, if kept with him in the until 60-80 days ‘*. However, wild, young males become independent much earlier than this, at about 35-40 days old13. Experiments by Eales suggested that males moved from their father to a second tutor at this age learned predominantly from that second bird14. But this, in its turn, may be unrealistic. Birds do not suddenly get wrenched away from their parents in the wild, as they do when moved from one cage to another in captivity. They are more likely to become slowly more independent over a period, especially as males become increasingly aggressive to their offspring as they start to breed again themselves. Clayton found that young males preferred to learn from tutors who were more aggressive to them, and this could lead them to learn from the father in the period after 35 days as their independence growsJ5. The difficulty of resolving this issue in either the field or the laboratory is neatly illustrated by three recent papers’&‘* which, at first sight, seem to come to very different conclusions. Birds learn from father In the first study, Bohner16 has found that young male zebra finches kept with their fathers for 35-40 days develop songs as close to those of their fathers as do birds not separated till 100 days. While this result con416

No they don’t A recent laboratory experiment by Williams” has greater realism. She placed 12 birds of each sex in an aviary with 12 nest boxes, and left them to pair and breed. Ten pairs formed and 35young were produced. As well as recording and analysing the songs of the adult males and of the 16 young that were male, she watched interactions between the adults and young until the fledglings were 40 days old. She observed only at this early stage, apparently in the belief that sensitivity for song learning would have ceased by then, although this does not fit in with many findings in the literature”,‘*. Nevertheless, the observations did allow Williams to see how the songs developed by young males related to the interactions they had had at this stage with particular adult males. All birds were left in the aviary until the young were 90 days old, when their songs were fully developed and could be recorded. Williams’ results run counter to the idea that young birds simply copy their fathers’ songs. She found no such preference overall, though one large brood of males did learn from their father. All the males were copied by some young ones, and most young incorporated elements from more than one adult in their songs. Two adult males were copied more than the others, and these were the two that associated with and fed the young more than the others. However, these results are not as easily interpreted as it might seem. Most of the young formed a single creche in one corner of the aviary, and were thus liable to have limited and rather similar experience. The aviary was also very small (20m3) for the number of birds involved: this may have led to the creching, as well as encouraging copying from more than one adult through closer than normal exposure to many singing adults. Our own aviary experiments, as yet unpublished, involved much more

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space and found no creching, the young tending to remain in broods after fledging. Most young males learned from a single adult and in about half the cases this was the father, though there were eight males present. Clearly, the exact conditions in such laboratory studies have a great impact on the findings, and it is dangerousto generalize from a single group of birds, especially where housing is very restrictive. Yes they do The last word must come from the wild. Zann has been studying the development of calls and song in zebra finches in Australia for many years. His results on song are shortly to be published18. A difficulty in the wild is that young zebra finches tend to disperse after independence and are hard to find again. Zann has overcome this, as well as examining the timing of song learning, by catching birds at various stages from 36 days onwards and housing them in an aviary in the midst of his wild colony until he could record their songs. His conclusion is that the majority of young birds did learn from their fathers, but that the tendency to do so was less in those that were confined early, and were thus deprived of the father’s close influence during the time they would be becoming increasingly independent. This nicely confirms the period following 35 days as being the main sensitive phase for song learning. The father may indeed be the usual song tutor, but more detailed study will be needed to pin this down. Zann compared the song of each young male with that of his father and that of a likely alternative tutor: a male that was actively singing in the colony at the time. The closer resemblance to the former than the latter does not necessarily mean that the father was the tutor, as about half the males in the colony would have songs more similar to him than to the control male. An added consideration is that young zebra finches given a choice of two tutors after independence tend to learn from the one whose song is most like their father’s15. Thus, they may not learn from their father, but their father’s song may guide them to copy a tutor with similar characteristics. The answer to the question posed in our title is therefore: maybe. Despite a great deal of work on zebra finch song development, which has taught us a lot about mechanisms of development, it is still difficult to link the results to the situation in the wild. It is the classic bind of behavioural research: in the laboratory we can control the situation very precisely

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bJt it lacks realism, while in the field the animals are exposed to all sorts of experiences that limit the conclusions we can reach. References 1 Slater, P.J.B. (1989) Rho/. Ecol. Evol. 1, 13-46 2 Payne, R.B. (1981) Anim. Behav. 29, 6 38-697 3 Marler, P. and Peters, S. (1987) Rhology 76,89-100 4 Pepperberg, I.M. (1985) Auk 102, 8 54-864

Worldwide, the majority of current j;troposals to release genetically modified organisms concern plants; most are for small changes in common crop plants and present little spparent hazard. However, there is much confusion about how plants become pests, and implausible risk factors are appearing in the literature 2nd before committees. It is dangerous to estimate the risks from first principles because of the immaturity of plant population biology and the lack of empirical data. Regulatory agencies should concentrate on obtaining realistic assessment of hazards, and not attempt to balance !,otional benefits and disbenefits.

In April 1988, at the time of the REGEM meeting’ in Cardiff, UK, TREE published (jointly with Trends in Biotechnology) a special issue on the lllanned release of genetically engineered organisms. REGEM was concerned only with microbes, but it is nevertheless remarkable how little was said about plants at that time. Now, only two years later, plant proposals are the commonest, and look likely to remain so for a while. This article comments on the state of play regarding the release of what are now generally called genetically modified plants, and the present unsatisfactory means of assessing the hazards from these introductions. Two background events are relevant: Ihe European Community, at the cZouncil of Environment Ministers on .?2 March 1990, adopted a directive2 cln the release of genetically engineered organisms; and the Organis*ation for Economic Co-operation and Ievelopment (OECD) is encouraging snide discussion of a paper on good .Jevelopmental practice3, which deals Nith safety assessment of small-scale Mark Williamson, James Perrins and Alastair Fitter are at the Dept of Biology, University of York, York YOI 5DD,UK.

5 Petrinovich, L. and Baptista, L.M. (1987) Anim. Behav. 35,961-974 6 West, M.J. and King, A. (1988) Nature 334,244-246 7 McGregor, P.K. (1989) &ho/. Ecol. Evol. 1,124-127 8 Grant, B.R. (1984) Behaviour 89, 90-116 9 Millington, S.J. and Price, T.D. (1985) Auk 102.342-346 10 Nicolei, J. (1959) J. OmiTho/. 100, 39-46 11 Slater, P.J.B., Eales, L.A. and Clayton, N.S. (1988) Adv. Study Behav. 18, l-34

12 Immelmann, K. (1969) in Bird Vocalizations (Hinde, R.A., ed.), pp. 61-74, Cambridge University Press 13 Immelmann, K. (1962) Zoo/. Jahrb. Syst. 90, 1-196 14 Eales, L.A. (1985) Anim. Behav. 33, 1293-1300 15 Clayton, N.S. (1987) Anim. Behav. 35, 714-721 16 BBhner, J. (1990) Anim. Behav. 39, 369-374 17 Williams, H. (1990) Anim. Behati. 39, 745-757 18 Zann, R.A. Anim. Behav. (in press)

Releasing Genetically Engineered Plants:PresentProposals and Possible Hazards Mark Williamson, James Perrins and Alastair Fitter field trials, particularly of genetically engineered plants. The European directive lists points to be considered, as do numerous other documents (e.g. Refs 4-7). Unlike any of these, which are very general, our intention is to concentrate on the hazards of proposals as they exist at present. The proposals coming before committees The number of proposals coming forward to national regulatory committees is now increasing quite rapidly. Both OECD and GBFB (the Gesellschaft fiir Biotechnologische Forschnung mbH in Braunschweig, FRG) have started databases to track releases worldwide. The GBF database is set up under the acronym BIKE (Biotechnologie Informations-Knotten fiir Europa), and Table 1 shows the counts published in March 1990. Some releases contain more than one construct, so the totals differ. Slightly over 60% of the recorded releases have been of plants. Only 25% are of microbes, increasing to 38% if viruses are added. The commonest releases among plants have been those with herbicide-resistance genes, constituting about a third of all releases (apart from those that merely carry markers). This has caused controversy in Americas,lo, but not as far as we know in Europe, though there has been a conference on the topic”. The next commonest category, at just over a quarter of non-marker releases, contains those conveying resistance to insects, and includes both plants and microbes; 38 of these 46 involve the delta endotoxin from

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Bacillus thuringiensis, almost equally divided between plants (20) and bacteria (18). Lists of possible environmental applications of genetically modified organisms (GMOs) have been compiled by bodies such as the Office of Technology Assessment (OTA) of the Congress of the United States12. As well as plants resistant to herbicides, insects and diseases, it is expected that there will be plants with increased tolerance to adverse factors such as drought and heavy metals, and with the ability to fix nitrogen. A trickle of proposals in these fields has started and can be expected to produce more ecologically interesting problems than those of herbicide resistance. Also of ecological interest are proposals, not mentioned by OTA, to alter the constitution of the plant to make a more useful commercial product. Non-squashy tomatoes (Lycopersicon esculentum) and changed proteins in seeds of oilseed rape (Brassica napus) are two examples. Plants as pests A major question with all these proposals for plants is whether the genetic changes are more likely to make the plants into pests. With the European directive in place, plant breeders may have to think more about the possible ecological consequences of their work, about the effects of the changes they induce on factors such as seed survival or pollen dissemination13, or more generally about the pleiotropic effects14 of their genetic changes. 417