Developmental Psychology
1991, Vol. 27, No. 1, 35-39

Copyright 1991 by the American Psychological Association, Inc.
0012-1649/91/$3.00

Experiential Canalization of Behavioral Development: Results
Gilbert Gottlieb
University o f North Carolina at Greensboro
In exploring the possible experiential canalization of development, it was found that the mallard
duck embryo's contact call plays a canalizing role in species-specific perceptual development.
When mallard ducklings were prevented from hearing the contact call, they were susceptible todeveloping a preference for an extraspecific maternal call over the mallard maternal call. Exposure
to the contact call prevented the ducklings from developing a preference for the extraspecificmaternal call. Thus, normally occurring experience, in concert with genetic and other activities,
can canalize behavioral development. Canalizing influences account for developmental stability,
so that what we think of as normal or typical for a species repeats itself generation after generation.
In order for evolution to occur, through genetic mutation or otherwise, the canalizing influences
associated with normal development must be overcome. Canalization is thus a conservative featureof development that prevents evolution from occurring in a ready fashion.

groups are 4 and 5. It is essential to demonstrate the inductiono f a preference for the chicken call in devocal-isolates and thebuffering effect when vocal-isolates are exposed to the embryocontact call and the chicken call. The other groups are necessary control groups.

My preceding article (Gottlieb, 1991 a) established the theoretical framework for examining the possibility that normally occurring experience can canalize behavioral development. The
present article presents empirical evidence for the experiential
canalization o f species-specific maternal attachment. The present hypothesis is that normally occurring experience helps toachieve species-specific development by m a k i n g the developing organism unresponsive to extraspecific influences. For example, if the mallard duck (Anas platyrhynchos) embryo is devocalized, the usually highly selective response to the mallard
maternal call is weakened: After hatching, the duckling is as
responsive to a chicken (Gallus gallus) maternal call as to amallard maternal call in a simultaneous-choice test (Gottlieb,
1978). Exposing otherwise devocalized embryos to a recordingo f mallard embryo contact vocalizations causes t h e m to show
the usual preference for the mallard call versus the chicken callin the postnatal test (Gottlieb, 1985). Exposure to other types o fsibling vocalizations in embryo, or exposure to the contact callafter hatching, is ineffective, so the kind o f experience and thetiming o f the experience are highly specific.
If the experiential canalization hypothesis is correct, embryo n i c d e v o c a l i z a t i o n should m a k e the m a l l a r d e m b r y o andhatchling more susceptible to exposure to an extraspecific maternal call, assuming that the contact vocalization is acting as acanalizing or buffering experience. With the necessary control
groups, five experimental conditions are necessary to test thecanalization hypothesis, as indicated in Table 1.
In Table 1, X indicates the predicted preference and X----X
indicates prediction o f no preference. The two most critical

MethodSubjects
Peking ducklings are a domestic form of mallard duck. Despite theirdomestication, this breed has been shown to be similar to their wilder
counterparts in the specificity of their auditory perception of maternalcalls, as well as in various other forms of species-typical behavior(Gottlieb, 1971; Johnston & Gottlieb, 198 l; Miller, 1977, 1980; Miller& Gottlieb, ! 981 ). Unincubated eggs were received weekly from a largecommercial supplier and incubated in the laboratory under conditions
described in previous publications (Gottlieb, 1971, 1975).

Conditions
1. Vocal-communal. The vocal-communal mallards were incubated together and brooded together in groups of 15 to 25 in individual opaque boxes after hatching. Thus, they could hear themselves andeach other both before and after hatching but could not see each otherafter hatching.
2. Vocal-isolated(Vl). At the beginning of Day 24 of incubation, 2
to 3 days before hatching, when the embryo is first able to vocalize, theVI mallards were put in individual soundproof incubators where they
were able to hear their own vocalizations but not those of siblings.
These birds served as controls for the devocal conditions below.
3. Devocal-isolated(Dl). As indicated in Figure 1,2 to 3 days before
hatching, during the first 8 hours of Day 24 of incubation, these embryos were muted and placed in individual soundproof incubators.
They were muted in a brief operation in which their syringeal ("voicebox") membranes were coated with a nontoxic surgical glue (collodion). Collodion forms a rigid sheath over the membranes, and when
they are thus rigidified, the embryo (and later the hatchling) cannot
vocalize (Gottlieb & Vandenbergh, 1968). Our "hit" rate on devocalization is around 90%; if an embryo or hatchling can utter even thescratchiest vocalization it was eliminated from the experiment. There

Research was supported by National Science Foundation Grant
BNS-8419011 and National Institute of Mental Health Grant MH44813.
Margaret Horton, Ramona Rodriguiz, Wayne Kelly III, and April
Gray provided excellent assistance with the experiments reported inthis article.
Correspondence concerning this article should be addressed to Gilbert Gottlieb, Department of Psychology, University of North Carolina, Greensboro, North Carolina 27412-5001.
35

36

GILBERT GOTTLIEB

Table 1

Conditions Favoring Canalization or Malleability o f SpeciesSpecific Perceptual Preference
Predicted preference
Condition
1. Vocal communal
2. Vocal-isolated
3. Devocal-isolated
4. Devocal-isolated, exposed
to chicken call
5. Vocal-isolated, exposed
to chicken call andmallard duck embryocontact vocalization

Note. X = preference; X . . . . . . . .

MallardX
X
X ..........

ChickenX
X

X
X = no preference.

is a small toll associated with the operation: About 10% fewer birds
hatch than from unopened eggs.
4. Devocal-isolated, exposedtochickencall. The DIsexposed to thechicken call received that exposure in their soundproof incubator
compartments, where a speaker repetitively broadcast a single burst ofa chicken maternal call for 30 min per hour from Day 24 until 48 hr
after hatching, at which time the birds were tested. (The call was actually on for 22.5 min o f the 30-min period.) The call peaked at 65 dB(Scale B, fast) in the incubator and in the test (described below).
5a. Vocal-isolated, exposed to chicken call. These birds were treatedthe same as above with the exception that they could hear themselves
vocalize, as well as being exposed to the 30-min chicken call each hour.
(In Groups 5a and 5b, the embryos' heads were extricated from theshell in the same manner as for Group 3 and 4 birds, but they were notdevocalized.) The prediction here, as indicated in Table 1, was thefailure of the exposure to the chicken call to induce a preference for it
because the birds had been permitted to hear their own contact call.

Although I did not monitor the vocalizations of these particular birds,
I knew from unpublished observations that isolated birds produce thecontact call numerous times both before and after hatching.
5b. Vocal-isolated, exposed to chicken and embryo contact calls.
These VIs were treated the same as Group 5a, except that they were
exposed to l 0 min of the variable-rate embryonic contact call (Gottlieb, 1985) after 30 min of exposure to the chicken call each hour.
Because I did not monitor the self-produced vocalizations of the birds
in Group 5a, this group provided a more precise f.x on a known
amount o f exposure to the contact call that is required for the buffering
effect. The choice of the amount of exposure to the contact call was
originally arbitrary. In the 10-min period, the call was actually on for
4.6 min, which we now know from monitoring studies is at the bottomof the range produced by individual birds in isolation (4.8-6.2 min perhour, from unpublished observations). This amount of "sib stimulation" is well below the amount that would be received under natural
incubation and brooding conditions, in which the birds would be exposed to as many as 8 to 13 conspecific siblings. Thirty min per hour of
exposure (actually 22.5 min) to the extraspecific chicken call was
shown to be effective in a previous study of malleability in devocalized
ducklings (Gottlieb, 1987a), but those ducklings were tested with thechicken call versus the wood duck maternal call, not versus the mallard maternal call. The presence of the mallard call in the simultaneous auditory choice test with the chicken call provided a muchsterner test of malleability than using two extra-specific maternalcalls.
Test. Each bird was tested individually at 48 hr 0:4 hr) after hatching, as illustrated in Figure 2.
A speaker was mounted behind each of the two elliptical areas, eachbroadcasting the chicken or mallard calls over the 5-min test period.
As the bird entered the elliptical area in the vicinity of a speaker, theduration of its stay (in seconds) was measured. The duration scores foreach call were analyzed by the Wilcoxon test to get a preference foreach group (condition) in the experiment. A further measure of preference for each bird was derived as follows: I f a bird stayed in one approach area more than twice the time it spent in the opposing area, apreference was registered. This measure of preference gives a useful

Figure 1. Pulmonary respiration begins on Day 23 of incubation in the domestic mallard duck embryoand is well established by Day 24. When respiration is established, the embryo survives the devocalization
operation, which requires extricating its head from the eggshell and painting its syringeal membranes withsurgical glue.

SPECIAL SECTION: EXPERIENTIAL CANALIZATION

37

Figure 2. Overview of simultaneous auditory-choice test. (l) Duckling placed equidistant between two
speakers (not visible), in front of which are painted elliptical approach areas. (2) Duckling on its way
toward approach area on its left. (3) Duckling in approach area. (4) Duckling snuggling to curtain andorienting to nonvisible speaker broadcasting a maternal call of its own (or another) species.

summary tabulation of the behavior of each bird in the experiment andallowed further statistical treatment of preference in terms of the chisquare test (between conditions) and the binomial test (within conditions). The latter almost always agreed with the duration measure described earlier and thus lent strength to the results, whether for a preference or the absence of a preference in the choice test. A preference wasindicated by a two-tailed p value of.05 or less. Ps greater than .05 wereindicative of no preference. In all cases but one, the results of thebinomial test and the Wilcoxon test were in agreement as to the presence or absence of a preference, so to conserve space and avoid repetition, only the former are reported in detail. The single exception concerned Group 5b's performance at 48 hr, for which the binomial was
nonsignificant and the Wilcoxon indicated a mallard preference.
To assess the "durability" of the 48-hr test results, each bird inGroups 4, 5a, and 5b was retested at 65 hr. Because exposure to thechicken call (and contact call) was terminated at 48 hr, the 65-hr test
results give some indication of the enduring effect of the earlier experience.

Results
As can be seen in Table 2, the v o c a l - c o m m u n a l and VI birds
showed, as expected, a u n a n i m o u s preference for the mallard
call over the chicken call, whereas the unstimulated Dis did notshow a preference. Furthermore, as predicted, the DI birds exposed to the chicken call showed a preference for the chicken
call over the mallard call at 48 hr and continued to show that
preference at 65 hr. Also as predicted, the VI birds exposed tothe chicken call (Group 5a) did not develop a preference for it,
as evidenced by their behavior in the 48- and 65-hr tests. The
buffering effect o f the contact call was even more clearly inevidence in G r o u p 5h, in which the birds received explicit exposure to the contact call, as well as the chicken call: These birds
preferred the mallard over the chicken call in both tests. The
results from G r o u p 5a indicate a blockage o f the chicken preference by self-stimulation, but, to maintain the species-typicalpreference for the mallard call in the face o f exposure to thechicken call, exposure to contact calls produced by siblings isrequired (Group 5b). G r o u p 5b heard the broadcast o f only one
sibling's calls, which would be considerably less than would
occur under n o r m a l incubation and brooding conditions innature.
According to the chi-square test, when the preferences o f thegroups are c o m p a r e d across conditions, the unstimulated vocal-intact (Group 2) birds showed a greater preference for themallard call than did the unstimulated DI (Group 3) birds, As
predicted, the DI birds that were exposed to the chicken call

38

GILBERT GOTTLIEB

Table 2Preferences of Mallard Ducklings & Simultaneous
Auditory-Choice Test
Preference
Condition

N

1. Vocal-communal 30
2. Vocal-isolated
20
3. Devocal-isolated 83
4. Devocal-isolated,
exposed tochicken call
26
Retest23
5a. Vocal-isolated,
exposed tochicken call
36
Retest36
5b. Vocal-isolated,
exposed tochicken andcontact calls
41
Retest38

N
responded

Mallardcall

Chicken
call

Both

24
14
43

24***
14"**
26

0
0
15

0
0
2

21
17

3
2

17**
15**

1
0

26
30

11
16

15
12

0
2

31
28

19
20*

12
6

0
2

Note. Results of Conditions I and 3 are from Table 2 in "Developmentof Species Identification in Ducklings: IV. Change in Species-Specific
Perception Caused by Auditory Deprivation" by G. Gonlieb, 1978,
Journal of Comparative and PhysiologicalPsychology, 92, p. 380. Copyright 1978 by the American Psychological Association. In the first testof Group 5b, the binomial test is nonsignificant, whereas the Wilcoxon analysis of differences in approach duration scores favoringmallard is significant (p < .02). Otherwise, all Wilcoxon outcomes
agree with the presence or absence o fpreference according to the binomial test.
*p<.01. **p_<.004. ***p<.00006.

(Group 4) showed a greater preference for it than did the unstimulated DI (Group 3) birds. As predicted, the stimulated DI(Group 4) birds also showed a greater preference for the chicken
call than did the stimulated VI (Group 5b) birds, which showed
a greater relative preference for the mallard call. For all o f theabove differences, p < .00006.
Discussion
To my knowledge, this is the first explicit demonstration of
the canalizing influence of normally occurring sensory experience. Exposure o f mallard ducklings to their variable-rate contact call not only fosters species-specific perceptual development (i.e., ensuring selective responsiveness to the maternal callo f the species), it also buffers the duckling from becoming responsive to social signals from other species. In the absence o f
exposure to the contact call, the duckling is capable o f becoming attached to the maternal call of another species even in thepresence o f its own species call (in simultaneous auditorychoice tests). My previous demonstration o f malleability in devocalized mallard ducklings (Gottlieb, 1987a) involved the induction of a preference for either a chicken maternal call or awood duck (Aix sponsa) maternal call; the birds were tested
with the chicken versus wood duck calls, not the mallard maternal call. To be quite frank, I did not believe that it was possible to demonstrate malleability in the presence o f the species-

specific maternal call. It was only when I began to think o f thepossible canalizing effect o f experience that it became apparent
that devocalization might permit such a degree of malleability
that exposure to an extraspecific maternal call would overridethe "innate" attractiveness o f the species maternal call. Clearer
thinking about what genes do and do not do in individual development gave rise to the idea that canalization must take place
not only at the genetic level but at all levels of the developing
system (Gottlieb, 1991a, Figure 1), including the developing
organism's usually occurring experiences. The fact that canalizing influences are potentially present at all levels of the developing system has not been widely appreciated. Because the developmental ramifications of canalization were described fully inthe foregoing article (Gottlieb, 1991a), I limit the present discussion to the evolutionary implications o f canalization.

Canalization and Evolution
Canalizing influences account for developmental stability, sothat what we think of as normal or typical for a species repeats
itself generation after generation. For evolution to occur,through genetic mutation or otherwise, the canalizing influences associated with normal development must be overcome.
Canalization is thus a conservative feature o f individual development that prevents evolution from occurring in a readyfashion.
Elsewhere (Gottlieb, 1987b), I took Kuo's (1976) idea o f behavioral neophenotypes and applied it to the problem of evolution.
In essence, the creation of a new behavioral phenotype (behavioral neophenogenesis) requires a change in normal or usual
rearing circumstances that ordinarily function to canalize development along species-typical lines. An altered behavioral
phenotype causes the affected individuals to change their way
o f life, exploiting new habitats, diets, and so on, which will
eventually lead to morphological change and perhaps eventually to genetic change (through long-continued selective breeding among the descendants of the affected individuals). Behavioral change is widely considered to be the first step in thepathway to evolutionary change (Bonner, 1983; Hardy, 1965;
Lamarck, 1809/1984; Larson, Prager, & Wilson, 1984; Leonovicovfi & Novfik, 1987; Piaget, 1978; Reid, 1985; Sewertzoff,
1929; Wyles, Kunkei, & Wilson, 1983), and behavioral change ismost readily accomplished by overcoming or changing the experiential canalizing influences that are present in the usual
course of individual development. Behavioral neophenogenesis
allows evolution to proceed at a much more rapid rate than isthe case when a species must await a severe environmental
change or catastrophe such as oceans drying up or months ofdarkness to prune individuals that are capable of adapting to
the change from those that are not. Such extreme environmental changes are rare and widely spaced in time compared withthe frequency and tempo o f evolution that could be instigatedby behavioral neophenotypes.
Thus, an understanding of the experiential canalization of
behavioral development has potentially significant implications for our understanding of evolution (and especially theresistance to evolution). The present proposal is unconventional in relation to the neo-Darwinian concept ofevolntion inthat it postulates an extragenetic "behavioral mutation" rather

SPECIAL SECTION: EXPERIENTIAL CANALIZATION
than a genetic mutation as the instigator of evolutionarychange. Along these lines, it has been demonstrated that certain extragenetic behavioral and morphological changes are"heritable" in the sense that they recur in subsequent generations (Clark & Galef, 1988; Denenberg & Rosenberg, 1967; Ho,
1984; Skolnick, Ackerman, Hofer, & Weiner, 1980).
It is important to realize that although experimentally produced genetic mutations and selective breeding have produced
many new varieties or subspecies, such mutations have neverproduced a new species, even when the experimental program
extended over 30 years and involved tens of thousands of generations (e.g., Goldschmidt, 1933). Ever since the time of W. Bateson (1894), a minority of biologists have despaired of a new
species evolving from a new variety that has been produced bygenetic mutation and selective breeding. Thus, while I do notwant to present the behavioral mutation idea as a mutually
exclusive alternative to genetic mutation, I do think that it isworthwhile to consider the experiential dissolution of canalization and the behavioral route to evolutionary change as a potentially valid pathway. The behavioral-developmental pathway toevolutionary change is described in detail in Gottlieb (1991 b).
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Received October 10, 1989
Revision received March 5, 1990
Accepted July 16, 1990 •