Review
Nature’s Call and Experiential Nonlinearities David B. Miller
University of Connecticut Gilbert Gottlieb was an elegant experimentalist whose research was inspired in part by naturalistic observations of parent-offspring vocal-auditory interactions of waterfowl. Such observations are essential in identifying potential linear (obvious) as well as nonlinear (subtle) mechanisms underlying the development of species-typical behavior. His series of experiments on the development of species identification in birds illustrates the fruitfulness of his conceptual and theoretical approach, which also inspired my own work on alarm call responsivity of ducklings. The respective developmental systems we studied both in nature and in the lab are greatly influenced by nonlinear experiential factors and also illustrate multiple pathways toward developmental outcomes. Keywords: Naturalistic observation, Nonlinear experience, Transactionalism, Auditory communication
“Nothing happens in contradiction to nature, only in contradiction to what we know of it.” — Agent Dana Scully, The X-Files (Carter & Goodwin, 1996). As a graduate student in the early 1970s, I happened upon two books not assigned in courses that, unbeknownst to me at the time, would greatly influence my future. The first book caught my attention because it was a small paperback wedged between scholarly clothbound books in my university’s bookstore. With curiosity, I began thumbing through Zing-Yang Kuo’s The Dynamics of Behavior Development: An Epigenetic View. I recalled that Kuo was a radical behaviorist but, at the time, was unaware of his extensive work in behavioral development, including his series of 10 articles on embryonic development published in the 1930s in both psychological and zoological journals. The book appeared to offer a unique and broader view of behavioral development than what I had been exposed to previously, and the attractive $2.45 U.S. price (even for a “starving” graduate student) resulted in a purchase that would soon alter my entire way of thinking about behavioral development. Of particular interest to me was Kuo’s emphasis on the importance of considering five variables affecting behavioral development: morphology, biophysical and biochemical factors, stimulating objects, developmental history, and environmental context. This comprehensive view of behavioral development made sense, and I was especially interested in Kuo’s explicit recognition of the effects of environmental context on behavior because of my own concern regarding the artificiality of studying animal behavior in a laboratory setting. At the time, my experimental animals were behaving in unpredictable ways that I thought might be a function of the laboratory context in which I was observing them. European Journal of Developmental Science [EJDS]. 2007, Vol. 1, No. 2, 165–171 © Vandenhoeck & Ruprecht 2007, ISSN 1863-3811
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The second book, called to my attention by my ornithology professor, was Development of Species Identification in Birds, by Gilbert Gottlieb. What especially fascinated me about this monograph was the fresh theoretical perspective emphasizing the difference between “predetermined epigenesis” and “probabilistic epigenesis,” as well as experiential manipulations involving duck embryos, which immediately brought to mind Kuo’s book. When I saw that Kuo acknowledged Gottlieb’s help in the preface of his book and that Gottlieb, in turn, cited Kuo, I became all the more interested in Gottlieb’s approach. I was equally fascinated with the fact that Gottlieb began his studies by undertaking naturalistic observation, followed by a series of logical, elegant laboratory experiments aimed at assessing prenatal developmental mechanisms that affect postnatal species-typical behavior. (Perhaps it is less than surprising that in 1976, Gottlieb prepared and edited an enlarged clothbound edition of Kuo’s 1967 book.) After brief correspondence, I visited Gottlieb in 1972 with an eye toward working with him as a postdoc. As I entered his laboratory located on the seemingly unlikely grounds of a mental hospital in Raleigh, North Carolina, he quickly shuffled me off in an old pick-up truck to his field station in the country. Here, in the midst of a pond surrounded by wood duck (Aix sponsa) hole-nest boxes and mallard (Anas platyrhynchos) ground-nest boxes, he further elaborated on what I had gleaned from his monograph. He was eager to learn more about the nature of mallard and wood duck maternal assembly calls—the vocalizations that hens use to call their ducklings out of the nest, samples of which he had been using in his laboratory studies on the acoustic basis of species identification. As implied by the opening quotation from The X-Files, knowing what happens in nature is crucial in understanding what may otherwise seem to be unexpected outcomes. This realization is foundational to Gottlieb’s research, to what he taught me, and to what I would come to realize in my own work. Within a year, this field station would become my research “home” as I transitioned from laboratory investigations of animal learning to naturalistic observations of parent-offspring auditory communication in ducks under Gottlieb’s mentorship. Gilbert Gottlieb was certainly not the first comparative psychologist to base his laboratory investigations on field observations. Even John Watson and his student, Karl Lashley, did field experiments in the Dry Tortugas on nesting behavior of terns (Watson & Lashley, 1915), not to mention pioneering fieldwork on nonhuman primates by C. R. Carpenter (1964), as well as T. C. Schneirla’s (1971) observations of army ant social behavior in the tropics. But, naturalistic observation was far from the forefront of psychological research, and some investigators’ careers may even have suffered as a result of “wasting time” watching animals in nature (F. A. Beach, personal communication, August 30, 1976). But, Gottlieb used his field observations as a point of departure from which to formulate the important laboratory research questions that he would later address—a strategy that later inspired a paper that I wrote on how naturalistic observation can advance psychological research (Miller, 1977a). © Vandenhoeck & Ruprecht GmbH & Co. KG, Göttingen
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In its heyday, imprinting was studied primarily as a visual phenomenon, spawned by the writings of Konrad Lorenz and the many laboratory investigations of familial imprinting that followed in the 1950s and 1960s. Despite the laboratory research emphasis on redirecting species-typical visual preferences toward species-atypical visual objects in easily-contrived laboratory studies, even Lorenz had recognized the importance of vocal/auditory aspects of imprinting, albeit anecdotally (Lorenz, 1952). While monitoring mallard nests in the field, Gottlieb observed the extent of auditory stimulation provided by hens to their offspring (Gottlieb, 1963a). His early experiments teased apart the relative importance of auditory and visual components in an imprinting situation. In accord with what one might predict based on a naturalistic situation in which ducklings see and hear a hen calling them out of the nest, Gottlieb found that the audiovisual combination was more powerful than either component alone; however, he also found that the auditory component was more important than the visual component when ducklings were presented with a choice between the two components in opposition to one another (Gottlieb, 1963b, 1973). These early data led him to further investigate the auditory aspects of species identification and, ultimately, the developmental mechanisms associated with the effects of prenatal experience on postnatal behavior. But in order to identify actual prenatal mechanisms causally linked to postnatal auditory preferences, Gottlieb had to find a way to alter embryonic auditory experience. Incubating eggs in individual, soundproof compartments certainly attenuates auditory experience, but does not eliminate it. Domestic duck (Peking breed) embryos begin vocalizing inside the egg around Day 24 of incubation, two to three days prior to hatching (Gottlieb, 1968). Thus, they have extensive experience with self-produced sounds. Together with his zoologist colleague John G. Vandenbergh, Gottlieb devised an embryonic devocalization procedure to totally mute the embryos prior to the onset of vocal activity (Gottlieb & Vandenbergh, 1968). The perfection of the devocalization procedure resulted in a series of experiments demonstrating how subtle, nonobvious, or nonlinear experience plays a constructive role in the development of species-typical behavior. Specifically, self- and/or sibling-produced embryonic sounds are developmentally linked to the duckling’s postnatal responsiveness to the maternal assembly call. This is viewed as a developmental nonlinearity because behavior A (responding to the maternal call) is not linked to experience A (having heard the maternal call previously), but, rather, to experience B (having heard self- and/or sib-produced embryonic sounds). Identifying experiential nonlinearities is, by their very nonobvious nature, tedious and difficult. Yet, a truly developmental approach can only be achieved by accounting for as many components of a developmental system as possible, both linear and nonlinear. Failure to do so runs the risk of appealing to developmentally inadequate deterministic pseudoexplanations, both genetic and environmental. Naturalistic observation can often aid in the pursuit of identifying candidate nonlinearities by revealing the array of normally-occurring events that © Vandenhoeck & Ruprecht GmbH & Co. KG, Göttingen
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befall individuals of the species under study, as illustrated by Gottlieb’s research. It is the task of developmental scientists to experimentally ascertain the emergent nature of developmental systems resulting from the ongoing transactions among the system’s components, both linear and nonlinear (see also Oyama, 1985). And, as Gottlieb stated in a recent audio interview (Miller, 2006), “[the nature-nurture controversy] won’t be resolved until a fully developmental point of view has been widely adopted and widely implemented; to succeed, it will take the triumph of a fully developmental point of view.” Gottlieb’s theoretical teachings, coupled with our 7-years of collaborative field and laboratory investigations, helped me to pursue a research career on a developmental system that, in many ways, ran parallel to his own in that it also involved auditory communication in mallard ducklings. While recording assembly calls in the field for subsequent acoustic analysis, I observed an unusual behavior by mallard hens on nests. Occasionally, a hen would stretch her neck and extend her head upward while uttering a very low-amplitude call that I had never heard before. I came to realize that the hen’s behavior was triggered by disturbances in the vicinity of the nest, such as potential predators, and that the call was actually an alarm call, which silences her ducklings beneath her and causes any that might have been beside her to freeze (i.e., cease all vocal and locomotor activity). Subsequent laboratory experiments (Miller, 1980) revealed that incubator-hatched, maternally-naïve ducklings freeze upon initial exposure to this call, and that the most important acoustic feature differentially affecting behavioral inhibition versus excitation is the repetition rate (i.e., number of notes per second) of the burst of notes composing the call. Following Gottlieb’s lead on identifying nonlinear experiential influences that affect developmental systems, I found that rearing devocalized ducklings in individual auditory isolation significantly reduces the rate of freezing (Blaich & Miller, 1988), and that augmenting their auditory experience with normally occurring embryonic sounds restores species-typical alarm call responsivity (Miller & Blaich, 1988). What I was unprepared for was the realization that auditory experience is not necessary for the development of alarm call responsivity, but, rather, is sufficient. Further studies revealed that social rearing of devocalized ducklings is also sufficient to foster the development of freezing (Miller, 1994). In other words, there are multiple pathways in the development of this behavior. In the absence of social experience, auditory experience is important; but, when social experience occurs, even in a brood of nonvocal siblings, auditory experience is not important. A natural nest is a highly social environment. Perhaps I should have been less surprised that “nothing happens in contradiction to nature,” as indicated above. The actual mechanism underlying the nonlinear effect of social experience on alarm call responsivity is yet to be determined. Shortly after I began my laboratory studies on alarm call responsivity, and as Gottlieb became increasingly interested in the relationship between development and evolution (e.g., Gottlieb, 1992), we collaborated on a study that demonstrated behavioral heterochrony specifically in relation to alarm call responsivity and domestication. © Vandenhoeck & Ruprecht GmbH & Co. KG, Göttingen
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Gottlieb had previously stimulated my interest on the effects of domestication on species-typical behavior, or, more specifically, the lack thereof (Miller, 1977b), when we had to suspend our work on recording assembly calls because our entire population of waterfowl had been killed by botulism at our field station. What began as a study comparing alarm call production and perception in wild and domestic mallards turned out to yield an unexpected finding: It takes domestic mallards (Peking breed) two days longer to reach the level of behavioral arousal that their wild progenitors exhibit 24 hr after hatching. Thus, there is a behavioral lag in arousal consequent to domestication. Heterochrony refers to a change in the timing of developmental events over evolution and is a potential mechanism that can affect evolutionary change (e.g., de Beer, 1958). Charles Darwin (1859) used domestic animals, in part, as a microcosm for understanding evolutionary processes. Gottlieb and I had unwittingly demonstrated the first behavioral demonstration of heterochrony (Miller & Gottlieb, 1981). This was our final collaborative effort and one that I am most proud of. Among Gottlieb’s most important conceptual contributions was his delineation of the various roles that experience can play in the development of behavior and the nervous system by either maintaining a developmental system, facilitating the temporal onset of developmental events, or actually inducing development (Gottlieb, 1976). This framework provided a basis for scientists to more precisely consider the ways in which linear and nonlinear events contribute to development. In my own work on alarm calls, Gottlieb’s framework helped me more precisely understand how perinatal experience affects the development of freezing. My initial experiments suggested the existence of a possible postnatal critical period of auditory experience for the development of freezing. But, further testing, spawned by Gottlieb’s conceptual framework, revealed a maintenance experiential effect rather than a critical period (Miller & Blaich, 1988). Any premature conclusion of a critical period would have been due to a failure to experimentally examine the possible importance of the critical period-to-test interval (see also Bateson & Hinde, 1987). Adding another experimental condition to our studies revealed that continued exposure to normally occurring duckling sounds up to the time of testing is important for freezing. Had we not assessed that, we might have erroneously concluded that a postnatal critical period exists for the development of alarm call responsivity. We correctly concluded that normally occurring auditory experience maintains freezing. Indeed, if one were to reexamine the critical period literature in general and redesign studies with Gottlieb’s scheme in mind, one might very well find alternative explanations to what otherwise have been the delineation of critical periods for behavioral development. This literature is fraught with methodological difficulties (cf. Gottlieb, 1982). Gilbert Gottlieb’s influence on my own work is but a meager example of his influence on developmental science as a whole. Gottlieb’s own theoretical contributions are traceable to his undergraduate days at the University of Miami, where he read Dewey and Bentley’s (1949) book, Knowing and the Known, which advocated a new approach that went beyond “inter-action” called “trans-action.” Gottlieb studied their work carefully, and their influence greatly shaped the emergence of his own transactional view of development © Vandenhoeck & Ruprecht GmbH & Co. KG, Göttingen
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(Miller, 2006). For Gottlieb, the developmental system is best viewed as a complex transaction occurring among different levels of organization (i.e., genetic, neural, behavioral, environmental), such that at every point in development, events occurring at any level affect other levels. Essentially, the organism is a “new” organism at every point in ontogenetic time. This is the behavioral system of which the organism is part and parcel, and this is the “truly developmental point of view” that Gottlieb has so strongly advocated. In our audio interview (Miller, 2006), Gottlieb indicated that his most important theoretical contribution to developmental science is best represented in the title of one of the last chapters he wrote, “Developmental Neurobehavioral Genetics: Development as Explanation” (Gottlieb, 2007). Gottlieb’s earlier conceptual and theoretical insights and empirical contributions have had important impacts on developmental science. Those of us who knew him, worked with him, and/or embrace his view await with eager anticipation what he considered as his most important work, and its impact on present and future generations of developmental scientists. References Bateson, P. & Hinde, R.A. (1987). Developmental changes in sensitivity to experience. In M. H. Bornstein (Ed.), Sensitive periods in development. (pp. 19-34). Hillsdale, NJ: Erlbaum. Blaich, C.F., & Miller, D.B. (1988). Alarm call responsivity of mallard ducklings (Anas platyrhynchos): VI. Effects of sibling and self-produced auditory stimulation. Journal of Comparative Psychology, 102, 56-60. Carpenter, C.R. (1964). Naturalistic behavior of nonhuman primates. University Park, PA: Pennsylvania State University Press. Carter, C. (Writer) & Goodwin, R. W. (Director). (1996). Herrenvolk [Television series episode]. In J.P. Finn, K. Manners, & R. Bowman, (Producers), The X-Files. Beverly Hills, CA: 20th Century Fox Television. Darwin, C. (1859). On the origin of species by means of natural selection. London: John Murray. de Beer, G. (1958). Embryos and ancestors. (3rd ed.). London: Oxford University Press. Dewey, J., & Bentley, A. F. (1949). Knowing and the Known. Boston: Beacon Press. Gottlieb, G. (1963a). “Imprinting” in nature. Science, 139, 497-498. Gottlieb, G. (1963b). Following-response initiation in ducklings: Age and sensory stimulation. Science, 140, 399-400. Gottlieb, G. (1968). Prenatal behavior of birds. Quarterly Review of Biology, 43, 148-174. Gottlieb, G. (1971). Development of species identification in birds. Chicago: University of Chicago Press. Gottlieb, G. (1973). Neglected developmental variables in the study of species identification in birds. Psychological Bulletin, 79, 362-372. Gottlieb, G. (1976). Conceptions of prenatal development: Behavioral embryology. Psychological Review, 83, 215-234. Gottlieb, G. (1982). Development of species identification in ducklings: IX. The necessity of experiencing normal variations in embryonic auditory stimulation. Developmental Psychobiology, 15, 507-517. © Vandenhoeck & Ruprecht GmbH & Co. KG, Göttingen
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Gottlieb, G. (1992). Individual development and evolution. New York: Oxford University Press. Gottlieb, G. (2007). Developmental neurobehavioral genetics: Development as explanation. In B.C. Jones & P. Mormede (Eds.), Neurobehavioral genetics: Methods and applications (Second edition) (pp. 17-27). Boca Raton, FL: CRC Press. Gottlieb, G. & Vandenbergh, J. G. (1968). Ontogeny of vocalization in duck and chick embryos. Journal of Experimental Zoology, 168, 307-326. Kuo, Z.-Y. (1967). The dynamics of behavior development: An epigenetic view. New York: Random House. Kuo, Z.-Y. (1976). The dynamics of behavior development: An epigenetic view. (Enlarged ed., G. Gottlieb, Ed.). New York: Plenum Press. Lorenz, K. (1952). King Solomon’s ring. London: Methuen & Co., Ltd. Miller, D.B. (1977a). Roles of naturalistic observation in comparative psychology. American Psychologist, 32, 211-219. Miller, D.B. (1977b). Social display of mallard ducks (Anas platyrhynchos): Effects of domestication. Journal of Comparative and Physiological Psychology, 91, 221-232. Miller, D.B. (1980). Maternal vocal control of behavioral inhibition in mallard ducklings (Anas platyrhynchos). Journal of Comparative and Physiological Psychology, 94, 606-623. Miller, D.B., & Gottlieb, G. (1981). Effects of domestication on production and perception of mallard maternal alarm calls: Developmental lag in behavioral arousal. Journal of Comparative and Physiological Psychology, 95, 205-219. Miller, D.B. (1994). Social context affects the ontogeny of instinctive behaviour. Animal Behaviour, 48, 627-634. Miller, D.B. (2006). Gilbert Gottlieb (1929-2006). Retrieved November 1, 2006, from University of Connecticut Web site: http://web.uconn.edu/millerd/GG/GG.html Miller, D.B., & Blaich, C.F. (1988). Alarm call responsivity of mallard ducklings: VII. Auditory experience maintains freezing. Developmental Psychobiology, 21, 523-533. Oyama, S. (1985). The ontogeny of information. New York: Cambridge University Press. Schneirla, T.C. (1971). Army ants: A study in social organization. San Francisco: Freeman. Watson, J.B. & Lashley, K.S. (1915). An historical and experimental study of homing. Papers from the Tortugas Laboratory of the Carnegie Institution of Washington, 7, 7-60. Address for correspondence: David B. Miller, Dept. of Psychology, University of Connecticut, Unit 1020, 406 Babbidge Road, Storrs, CT 06269-1020, USA; Email:
[email protected] David B. Miller, Ph.D., Professor of Psychology since 1980 at the University of Connecticut and former postdoc with Gilbert Gottlieb (1973-1977, 1978-1980), and Alexander von Humboldt Fellow in Ethology at the University of Bielefeld, Germany (1977-1978). Editor of Bird Behavior since 1995. Research on the development of alarm call responsivity of mallard ducklings and auditory communication in birds.
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