Animal Behaviour 77 (2009) 785794

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Animal Behaviour
journal homepage: www.elsevier.com/locate/yanbe

Essay

Niko Tinbergen and the red patch on the herring gulls beak
Carel ten Cate*
Behavioural Biology, Leiden University

a r t i c l e i n f o
One of the classic studies in animal behaviour is that by Niko Tinbergen on the stimuli that elicit begging
Article history: behaviour in young herring gull, Larus argentatus, chicks. Tinbergen examined which features of the beak
Received 3 October 2008 induced chicks to peck by using various cardboard models of herring gull heads in different shapes and
Initial acceptance 10 November 2008 colours. Leiden University, home university to Tinbergen at the time, still has a summarizing overview of
Final acceptance 15 December 2008 the data of the initial experiment of the study. In that experiment, models with a yellow beak with
Published online 28 February 2009 patches in various colours and different positions were presented to young chicks. In this essay, I relate
MS. number: 08-00639 those earliest data to the various publications in which Tinbergen discussed them over the years.
Subsequent publications became more and more detached from the original data, resulting in sizeable
Keywords: discrepancies between the original study and later descriptions of when and how the experiment was
begging response
done and its outcome. I rst sketch the scientic context of the herring gull study. Next I present the
chick
original data and document the subsequent changes. I discuss what might have led Tinbergen to modify
colour preference
herring gull his account of the study over the years, relating it both to its historical context and to the issue of
instinct expectancy biases.
Larus argentatus 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
observer bias
releasing mechanism
Tinbergen
visual perception

No textbook on animal behaviour would be complete without
mentioning the important contributions of Niko Tinbergen, one of
the founding fathers of our discipline. Tinbergen received the
ultimate recognition for his work when the 1973 Nobel prize in
Physiology or Medicine was awarded jointly to him, Konrad Lorenz
and Karl von Frisch for their discoveries concerning organization
and elicitation of individual and social behaviour patterns (https://
nobelprize.org/nobel_prizes/medicine/laureates/1973/press/html).
Current day studies of animal behaviour owe a lot to Tinbergens
pioneering work and several of his studies serve as classic textbook
examples up to the present day. This paper is about one of those
studies: the stimuli that make young herring gull, Larus argentatus,
chicks peck at their parents beak to obtain food.
One of Tinbergens strengths was his ability to derive interesting
research questions from observing wild animals and then trans-
lating these questions into elegant and simple experiments. This
was often done by using articial models (dummies) to obtain
responses from free-living animals, thus introducing a method that
has become an indispensable tool for studies on animal behaviour.
* Correspondence: C. ten Cate, Institute of Biology, Leiden University, P.O. Box
9516, 2300 RA Leiden, Netherlands.
E-mail address: c.j.ten.cate@biology.leidenuniv.nl (C. ten Cate).
The herring gull study, carried out on the Dutch island of Tersch-
elling, was not the rst one in which Tinbergen used the technique
of presenting models (e.g. ter Pelkwijk & Tinbergen 1937; Tinber-
gen & Kuenen 1939), but it was certainly the most extensive.
Carried out over half a century ago, the study has been, and still is,
mentioned in many textbooks on animal behaviour (e.g. Wilson
1975; Gould 1982; Goodenough et al. 1993; Drickamer et al. 1996;
Manning & Dawkins 1998; McFarland 1999; Barnard 2004; Alcock
2005; Scott 2005) and on related disciplines (e.g. Pinel 2000;
Zupanc 2004), and hence has become a true classic. It also featured
prominently in a television programme (Moments of Genius, Pro-
gramme 17: An Instinct of Behaviour, produced by the BBC in 2000)
devoted to Tinbergen as a Nobel Prize recipient. Apart from its
pioneering experiments and its contribution to the emerging
ethological theory, another likely reason why it has become such
a classic may be that Tinbergen himself published frequently about
it, thus making it widely known inside as well as outside the animal
behaviour research community.
Leiden University, where Tinbergen worked until his move to
Oxford in 1949, kept some remnants of Tinbergens work from that
period including some material underlying the rst publications
about the herring gull study: a sheet with the summary of the data
from the rst eld season (1947, see Fig. 1a; for a larger image, see
Supplementary Material), the handwritten and typewritten drafts

0003-3472/$38.00 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.anbehav.2008.12.021
786 C. ten Cate / Animal Behaviour 77 (2009) 785794
of the rst more extensive publication (in Dutch) of the experi-
ments (Tinbergen 1949), some notes with tabulated data under-
lying some gures of the 1949 publication, and a few of the models
used in that study. I became intrigued when I noticed that the data
sheet and the 1949 publication did not quite seem to match, and
when I consulted my copy of the Study of Instinct (Tinbergen 1951)
it showed yet another picture of the experiments, one that no
longer seemed congruent with the original data. This essay
describes how Tinbergen used the data of the rst eld season in
subsequent publications. It provides an illustration of his devel-
oping insights, but also shows that his presentation of the data
became more and more detached from the actual experiment in
which they had been collected.
All textbooks discussing the experiments refer to later accounts
of the study that include several more important modications of
the original data, some of which are only apparent when comparing
them with the earliest publications and the original data. The
earliest published accounts are in Dutch and German and are not
only difcult to obtain for those interested, but also deviate in some
details from the original data. Therefore, it is of scientic and
historical interest to present the original data and trace the various
changes. As discrepancies between original data and published
accounts can easily give rise to the suspicion of intentional fraud I
want to emphasize upfront that I have no reason to believe that this
is such a case. On the contrary, it is because Tinbergen himself has
been explicit about some of the more important changes that it is
possible to reconstruct the chain of events resulting in the
discrepancies.
Below I rst provide some background, followed by a general
description of the study. Next I give a chronological account of the
various publications in which the data have been presented over
the years, describing the changes that have accompanied them. I
will end with trying to answer the question of what might have
brought Tinbergen to make the various changes. Several recent
books have provided a comprehensive account of Tinbergen as
a scientist and as a person (Roell 1996, 2000; Kruuk 2003; Bur-
khardt 2005). They pay attention to the context for Tinbergens
studies and therefore make it possible to put his modications in
a historical perspective as well as relating them to current notions
of desirable scientic conduct.
BACKGROUND OF THE HERRING GULL STUDY
One of the core scientic disputes in the study of animal
behaviour during the rst half of the 20th century concerned the
role of animal instincts: the tendency to show adequate behaviour
in a particular situation, seemingly without any relevant experience
or learning being involved. For many comparative psychologists at
the time, instinctive behaviour was outside their interests: spon-
taneously shown adequate behaviour in nave animals was ascribed
to the presence of an instinct or drive for that behaviour and that
was it. Their focus was on intelligent behaviour involving learning.
Instinctive behaviour was only of interest as an evolutionary
precursor of such intelligent behaviour. In contrast, to the early
ethologists such as Lorenz and Tinbergen, innate instincts were
seen as a major factor shaping the behaviour of animals and
considered a subject to be analysed experimentally (see Roell 2000
and Burkhardt 2005 for historical overviews of the different views).
This led to concepts such as the innate releasing mechanism (IRM),
a perceptual mechanism sensitive to specic sign stimuli or
releasers, that is, stimuli that evolved to produce (release) specic
adaptive behavioural responses within a particular context without
learning being involved. While Tinbergen himself started to think
in less rigid ways about the innateness of behaviour in later years
(e.g. Tinbergen 1955, 1963), instincts and their analysis played an
important role in his and Lorenzs early theorizing and in the
emergence of ethology as a separate discipline. The herring gull
study was a key study in this phase of conceptual development.
Although initially presented as a mainly curiosity-driven study
(Tinbergen 1948a, b), Tinbergen later on wrote that the general aim
of the herring gull study was to examine the begging behaviour as
an example of, and a way to get insight into, the release of
instinctive behaviour (the pecking of the chicks to the parents tip
of the beak) by sign stimuli that activate a releasing mechanism
(Tinbergen & Perdeck 1950).
Normally, young chicks direct their pecking mostly towards
the red patch on the lower mandible of the yellow beak of their
parents. By the time Tinbergen developed an interest in this
behaviour, earlier studies by Heinroth & Heinroth (1928) and
Goethe (1937) had shown that newly hatched chicks already have
a tendency to peck at red objects. To analyse the relevant stimulus
characteristics for the release of this pecking behaviour more
systematically, Tinbergen and his collaborators (mostly under-
graduate students from Leiden University) took young gull chicks
out of the nest and presented to them various two-dimensional
painted cardboard models and some three-dimensional models
that were gently moved in front of the chicks head. The number
of pecks by chicks over a period of about 30 s was used to assess
how strongly a particular model released the pecking. Over
a period of several years, models of different shapes and colours
were used to examine the role of stimulus characteristics such as
the presence, colour and position of the patch, the colour of the
beak and head, and the shape of the head. Among other results,
the various experiments indicated preferences for certain patch
and bill colours and shapes. Tinbergen was also able to demon-
strate that combining various attractive features could lead to
a so-called supernormal stimulus, a thin red rod with three
sharply edged white bands at its tip, which induced more pecks
than a naturalistic stimulus.
Most textbooks mentioning the herring gull study refer to the
paper by Tinbergen & Perdeck (1950). That paper incorporated and
extended the data presented in the earlier mentioned 1949 paper
(Tinbergen 1949). However, the 1947 data were mentioned in two
publications before 1949, along with studies on some other subjects
(Tinbergen 1948a, b). After 1950, the 1947 data were presented in
The Study of Instinct (Tinbergen 1951). Then, an extensive account of
the Tinbergen & Perdeck studies and their outcome was given in The
Herring Gulls World (Tinbergen 1953). In 1954 the ndings were
presented at a meeting of the Josiah Macy Foundation on group
processes (Tinbergen 1955), a meeting of historical importance in
which leading animal behaviour researchers from both sides of the
Atlantic met (see also Kruuk 2003; Burkhardt 2005). It is this series
of publications that I discuss in this essay.
Over the years the herring gull study has received not only
praise, but also criticism on both the methodology and its conclu-
sions. In his discussion of the study, Kruuk (2003) mentioned some
methodological issues, such as the nonstandardized way in which
the models were moved in front of the chicks and the lack of
statistical analysis. Later, more systematic studies on the pecking
response by, in particular, Hailman (1967, 1969) but also others (e.g.
Alessandro et al. 1989; Eypasch 1989) replicated several of the
ndings, but also conrmed the validity of several of the criticisms
and led to different conclusions on the stimuli releasing the
begging behaviour (see Discussion). Such a fate, however, is
certainly not specic to Tinbergens studies, and illustrate how the
discipline matured. They do not take away the value of Tinbergens
pioneering experiments as a source of inspiration and a prime
example of original eld experiments.
This essay does not focus on how the experiments were done,
but on how Tinbergen treated the data once collected. I will not
 (f)
(b) (d) KLEUR VLEK
100

RODE VLEK 100

ROOD
rot
105
105
ZWARTE VLEK
ZWART
schwarz
85 85
BLAUWE VLEK BLAUW

blau 71
70 WIT
WITTE VLEK

30
(a) weiss 938 REACTIES
30
TOTAAL 1095 REACTIES GEEN VLEK

RODE VLEK - ZWARTE VLEK

C. ten Cate / Animal Behaviour 77 (2009) 785794

24
100
100
ROOD VOORHOOFD ROOD

105 86
ZWART

1276 REACTIES
(e)
85 (g) PLAATS

100

71 24
809 REACTIES

30

74
13
24 (c) 73
70 70

13

1947 1948a 1948b 1949

Figure 1. (continued)

787
 788
(h) (k) (n)
100 100
Red
Red Red
1

86 105 Black 86

Black 2 Black

71 85 Blue 71
Blue
3 Blue

59 71 White
59
White
4 White

25 30
25

C. ten Cate / Animal Behaviour 77 (2009) 785794

5
938 Reactions 938 Reactions

(i) (l)
A
100

B
24

809 Reactions

(j) (o)
A 2
2

(m) 74
12 12

47 47

B
75 75
70

13
13
70 70
1950 1951 1953
 C. ten Cate / Animal Behaviour 77 (2009) 785794 789

deal with all the experiments on the begging response of herring

Figure 1. Various versions in which (a) the original data have been presented in (bo) successive publications. Each column presents gures from the same publication, indicated by reference to its year of publication by Tinbergen at

Verlag; 1949: Bijdragen tot de Dierkunde (copyrights 2008: Contributions to Zoology. All rights reserved. ctz@naturalis.nl); 1950: Behaviour, Koninklijke Brill Publishers NV; 1951: Study of Instinct, HarperCollins (Oxford University Press);
the bottom of the column. Arrows connect gures presenting the same data. For all gures presenting the results of different colours of the patch, the sequence of colours is always the same from top to bottom: red, black, blue, white,
no patch. Several gures give the relative number of responses. These are (again from top to bottom): (a) 100, 105, 85, 71, 30, 24; (b) 100, 105, 85, 70, 30, 24; (f) 100, 105, 85, 71, 30, 100, 86; (g) 100, 24; (h) 86/105, 71/85, 59/71, 25/30;
(i) 110, 24; (n) 100, 86, 71, 59, 25. See also Appendix with notes for variation in numbers between the gures. Figures are reproduced with permission of the various publishers: 1948a: De Levende Natuur; 1948b: Experientia, Birkhauser
gull chicks, but only those of the initial study, as presented in the
1947 data sheet. In doing so, I put just one tiny part of the herring
gull study under the microscope, to reveal details one would not
otherwise see. The danger of such an approach is that it will
inevitably distort the full picture of this study: I select this part of
the study not only because we have the original data, but also
because it shows the most striking modications over the years. I
want to emphasize that what follows should therefore not be
considered representative of the whole study or of everything
Tinbergen did.

CHRONOLOGICAL OVERVIEW OF TINBERGENS PUBLICATIONS

ON THE 1947 DATA

I discuss the different publications exclusively in relation to the

1947 data as presented in Fig. 1, in which also the relevant gures of
the various subsequent publications are reproduced.

1947 Data

The data sheet (Fig. 1a) presents the results under the heading
Pikreacties Zilvermeeuw (Pecking responses herring gull;
Terschelling 1947). It also provides the total number of responses
(1095). The score for the responses released by each of the
models is given in proportion to those released by the normal,
red-patched, model for which the score is normalized to 100. For
the model with the patch on the forehead, the number of
responses to different parts of the beak is given, adding up to
a total of 157 pecks. There are no notes left of the data as
collected in the eld.

De Levende Natuur

The paper in De Levende Natuur (in Dutch; Tinbergen 1948a;

Fig. 1b, c) is a very readable and stimulating account in a journal for
naturalists of various studies by Tinbergen and coworkers during
a 2-week animal behaviour course in the dunes of Terschelling. The
herring gull study was one of the studies. The paper provides the
background for the 1947 data sheet. The study is introduced by
noting that the conspicuous markings on skin, feathers and fur of
animals often serve as social signals releasing the instinctive
responses in conspecics. Tinbergen mentioned that an earlier
study by Goethe (1937) implied that young chicks pecked at various
red objects, which raised his interest in the pecking response. To
examine this behaviour in more detail, cardboard models were
made with patches in different colours, as well as one model
without a patch and a model with a patch on the forehead, thus
matching the six models shown on the data sheet. The models with
the differently coloured patches were offered to examine whether
1953: The Herring Gulls World, Oxford University Press.

any patch would be attractive and the model with the red patch on
the forehead to examine whether the chicks would peck at the
patch or at the tip of the beak. It is reported that chicks were
collected from the colony and tested in a hide. A chick was pre-
sented with two models sequentially, one of which was always the
standard model (red patch on the beak), for 30 s each. The same
models were presented up to 20 times after each other. To stimulate
the chicks to beg, the experimenters gave an imitation of the
parental mew call and moved the models slightly. Chicks stimu-
lated in this way could give up to 1 peck/s during the 30 s period.
Collecting the data presented on the pecking behaviour took no
more than 3 days, according to the paper. It is also mentioned that
the models were painted with watercolours and that the colouring
of some of the models got wet and spread out. The numbers pre-
sented in Fig. 1b are the same as on the 1947 data sheet (with one
790 C. ten Cate / Animal Behaviour 77 (2009) 785794
small exception; see note 1 in the Appendix). Tinbergen mentioned
that the results (Fig. 1b) were surprising, with the black and blue
patches giving rise to approximately equal numbers of pecks as the
red patch, with the white patch receiving fewer pecks. He wrote
that more experiments are needed to decide whether black does
indeed produce more responses than red. The model without
a patch got very few responses, but these were, according to Tin-
bergen, directed at the tip of the beak. A separate gure (Fig. 1c)
illustrates the distribution of pecks over various locations at the
head for the model with the red patch on the forehead (again with
a small deviation in numbers; see note 2 in the Appendix). Tin-
bergen concluded that the chicks do not peck at something red,
but at a dark patch at the tip of the beak, and also that the position
of the patch is important.
Experientia
Tinbergens (1948b) paper is Experientia (in German; Fig. 1d, e) is
based on several talks given at the University of Zurich in January
1948, again presenting the herring gull study together with several
others. The data are discussed in the context of the concept of sign
stimuli that release behaviour that is otherwise prevented from
being expressed. Tinbergen explained that animals respond to just
a few stimuli out of all those perceived. Referring to Fig. 1d, he
mentioned that the results of the experiments show that young
chicks do not respond to the colour of the patch, but to any patch
contrasting with the yellow beak, with a black patch giving an even
stronger response than a red one. Three pages later, he discussed
Fig. 1e as an illustration that it is not just the presence of particular
elements that release the begging behaviour, but that their mutual
arrangement is also of importance. He provided this as an example
that sign stimuli can be complex, consisting of a congurational
(Gestalt) relationship between different elements. He did not
mention how the pecks were distributed over the model. In this
gure, Tinbergen presented the data for the pecking at the model
with the patch on the forehead with those for pecking at the
standard model, not mentioning that these data originated from
the same experimental series as the data on patch colour
preference.
Bijdrage tot de Dierkunde
Tinbergens (1949) paper (in Dutch; Fig. 1f, g) is about the
herring gull study only, adding many new and interesting experi-
ments to the 1947 data, for instance using differently coloured
beaks, and models with a grey beak with patches in different
shades of grey. The paper begins with a description of the begging
behaviour of herring gull chicks, again mentioning that Goethe
(1937) did some preliminary studies suggesting that nave chicks
had a preference for pecking at red objects. Tinbergen next
mentioned that his own study was initiated with the aim of doing
a systematic experimental study on external stimuli that trigger
innate behaviour patterns. He stated that the studies were done
during the eld seasons of 1947 and 1948. The rst data presented
in the paper are the results obtained in 1947, collected over 3 days.
Tinbergen began by explaining that the model with the red patch
received substantially more responses than a model without
a patch, but also that patches in other colours received relatively
many responses, referring to Fig. 1f (see note 3 in the Appendix). He
mentioned that the model with a black patch received even more
pecks than the red-patched model. He then stated that during the
1948 season they discovered they had made a methodological
error: not all models had been presented equally often. The model
with the red patch, serving as a standard against which the other
models were tested, was thus presented much more frequently.
In 1948 they discovered that repeatedly presenting chicks with the
same model led to habituation of the chicks to that model. He
inferred that this led to a reduction in the number of pecks to the
red model. As a consequence, its attractiveness had been under-
estimated and hence the relative preference of other patch colours
was overestimated. For this reason, a separate experiment was
done in which a model with a red patch was tested against one with
a black patch. The outcome, shown at the bottom of Fig. 1f, was that
the red-patched model now indeed received more pecks. Based on
the nding that the black-patched model received 86% of the
number of pecks to the red model, Tinbergen explained he used this
value to adjust the values for the models with the all other patch
colours by multiplying them by 0.82 (86/105), arriving at the values
indicated by the vertical white bars in Fig. 1f. The adjusted data
were now discussed as being the real ones, leading to the conclu-
sion that they showed two effects: the degree of contrast between
patch and beak colour was a relevant factor, but in addition the
chicks had a preference for the colour red. These two factors were
next tested separately, and conrmed, in several experiments in
1948, also described in the paper.
At the end of the paper Tinbergen presented the data for the
model with the red patch on the forehead (Fig. 1g). He noted the
outcome of the experiment as a typical demonstration of
a congurational stimulus situation, indicating that the responses
of the chicks are based on complex processes within the senses and
the nervous system. He mentioned that this experiment was also
done during 1947, but presented it as a direct comparison of this
model with the standard one, which is different from the descrip-
tion in 1948 where he wrote that all models were part of the same
set. Being part of the same data set, here too the results will have
suffered from the habituation effect, leading to an overestimation
of pecks to the model with the patch on the forehead. However, in
this case the outcome was not corrected (see note 4 in the
Appendix).
Behaviour
Tinbergen & Perdecks (1950) paper (Fig. 1h, i, j) is the one to
which most textbooks refer. This will not only be because it is the
most extensive paper, but also because it is the rst one in English.
Essentially it presents the same data as the earlier papers, but adds
experiments done by Perdeck during one additional eld season
(1949). Again, the introduction mentions the work by Goethe. Then
it introduces the concepts of sign stimulus and the IRM (innate
releasing mechanism), with reference to Lorenz (1935). The herring
gull study is presented as an experimental study of these concepts,
using the pecking at the red patch as a model system. The
description of the methodology explains that over the years the
methods became more sophisticated, outlining the issue of habit-
uation and how that was avoided in later years by a balanced
design. Again the rst data presented are the 1947 ones (see note 5
in the Appendix). To our astonishment, black got more responses
than red, Tinbergen wrote (page 7). He explained that afterwards
they began to suspect that this was due to negative conditioning
and that this led to a series of tests with the red-patched beak
against the black-patched one. As in the previous paper, the original
data and the corrected ones are presented in one gure (Fig. 1h; see
note 6 in the Appendix).
The paper then presents several other experiments before the
position of the red patch is discussed and presented in Figure 13B of
the paper (reproduced as Fig. 1j). It is mentioned (page 18) that
some models were made in which the red patch, while of the usual
size, was situated at abnormal places. The text notes that usually all
pecks are directed to the red patch when it is in the normal posi-
tion, but that the results show that the patch loses impact the
 C. ten Cate / Animal Behaviour 77 (2009) 785794
further away it is from the tip of the beak. Later in the paper a note
adds that experiments done in 1950, for which no details are pre-
sented, indicate that the crucial factor for getting fewer responses
to models with the patch further away from the tip of the beak is
that the chicks respond to the lowness of the patch, rather than to
distance from the tip. Lowness is next mentioned as the basis for
the congurational effect that is demonstrated by the nding,
presented in Figure 26 of Tinbergen & Perdeck (Fig. 1i), that the total
number of responses to the model with the patch on the forehead is
lower than that to the standard model. In the discussion on the
results of the various experiments presented in this paper, Tin-
bergen proposed the existence of seven sign stimuli that release or
direct the pecking response, among them the mew call, lowness,
nearness, and a red patch at the tip, characterized by colour and
by contrast. Of these seven, Tinbergen identied the mew call and
the red patch as true releasers, in the sense as characters evolved as
adaptations to a communicative function (Tinbergen & Perdeck,
page 38).
Although not mentioned explicitly, the text suggests that the
data for the models presented in Figures 13A and B (Fig. 1j) origi-
nate from one and the same experiment. However, the data in B are
clearly the ones collected in 1947 (see note 7 in the Appendix),
while the other data most likely originate from 1949 and hence
were collected using a different methodology. The legend of the
gure mentions that Model B had an eye at the usual place and
that this was not drawn by mistake. For Figure 26 (Fig. 1i) the text
refers to Tinbergen (1948b). No mention is made of the fact that the
Figures 13B and 26, which are remarkably different in how the
models are drawn, refer to the same model and concern the same
experiment, being part of the experimental series of 1947.
The Study of Instinct
In this classic book (Tinbergen 1951; Fig. 1k, l, m) the herring gull
study is mentioned in three places. First, Tinbergen used the study
to illustrate the concept of a sign stimulus. He presented three
gures that all refer to Tinbergen (1949). One of these gures is
Fig. 1k. Tinbergen now presented the corrected data only, without
mentioning the original outcome or the correction. These results,
Tinbergen stated, demonstrate that both the contrast between
patch and beak and the colour red contribute to the releasing value
of the red patch on the parents beak.
At page 77 in the book Tinbergen presented the comparison of
the model with the patch on the forehead with the standard
model (in this case referring to Tinbergen 1948a), using it to
demonstrate the concept of congurational stimuli (Fig. 1l).
Finally, in a discussion on the difference between releasing and
directing stimuli he presented Fig. 1m (page 83) as a demonstra-
tion that the red patch has both a releasing and a directing effect.
However, the 13 pecks given between the tip of the beak and the
forehead patch are left out and not mentioned in the text (see note
8 in the Appendix). Again all gures are presented separate from
each other.
The Herring Gulls World
In this popular account of the herring gull and its behaviour
(Tinbergen 1953; Fig. 1n, o), chapter 22 is devoted to the studies
on the begging behaviour of the chicks. As in earlier papers,
Tinbergen began by referring to Goethes study. As in Tinbergen
& Perdeck (1950), he stated that the rst experiments were done
during 2 weeks on Terschelling during 1946. He noted that the
chicks were presented with the models using a design in which
different chicks received different models as the rst one of
a series. No mention is made of the fact that the original series
791
tested each model against the standard model. Instead, it is
stated (page 188) that we had to take care that every model got
the same chances next describing a design in which all models
are presented equally frequently and in a systematically varied
sequence. This might have been so for later experiments
(reported in Tinbergen & Perdeck 1950), but not for the rst
ones. The text of the chapter closely follows Tinbergen & Perdeck
(1950). It also mentions that all gures are the same as in that
paper. Indeed they are, but with the exception of Fig. 1n. This
gure now provides the corrected data only, without mentioning
that they had been corrected. Tinbergen states (pp. 191192)
that he was forced to conclude that the red patch acted both
through its colour and through its contrast with the bill.
Figure 1o is identical to Fig. 1j, but lacks the earlier note that in
reality the models had eyes and that, by accident, these were
missing in the gure. The description of the results mentions
that the gure shows that the red patch was a directing stim-
ulus, but received fewer pecks the further away it was from the
tip of the beak.
Group Processes
At the Macy Foundation conference Tinbergen again presented
the herring gull experiments. He illustrated them with gures
taken from The Study of Instinct. The book about the meeting
(Tinbergen 1955) reports Tinbergens presentation including all the
discussion arising from it. About Fig. 1n, he said (page 89) that it
showed the relative number of responses to bills with patches in
various colors, and presented as outcome: Two interesting nd-
ings emerge: red stimulates more strongly than anything else, and
yet other colors also release quite a few responses. He did not
mention the corrections on the data. Tinbergen was questioned
about many details of the experiments and his interpretations
(Tinbergen 1955). In particular Schneirla, a well-known and
important comparative psychologist, wondered whether Tinbergen
was successful in controlling the presentation of the models to
young gulls. Tinbergen admitted that his method had been crude.
Nevertheless, he replied in the afrmative to a question about
whether the chicks were raised from the egg and had not seen an
adult gull. Again, this may have been so in some later experiments,
but it was not true for the earliest experiments, as also noted
by Kruuk (2003). The method descriptions in the early papers
(Tinbergen 1948a, b; Tinbergen & Perdeck 1950) all mention that
chicks were collected from nests. As parents brood newly hatched
chicks, most, if not all, chicks used in the rst experiment saw
adult gulls. Also, although Tinbergen mentions (page 5) that they
succeeded in acquiring a fair proportion of inexperienced chicks
with respect to feeding (Tinbergen & Perdeck 1950), some chicks in
the rst experiments had already been fed by parents. This can be
inferred from the very rst paper (Tinbergen 1948a) which ascribes
particular behavioural responses of some chicks to having experi-
enced parental feeding.
DISCUSSION
It is remarkable to see how some exploratory experiments have
gained such a prominent role in Tinbergens publications. Perhaps
even more remarkable is to see how subsequent publications get
more and more detached from the original data. While the changes
from each paper to the next are limited, and to some extent
understandable, they accumulate to a sizeable discrepancy
between the original data and the latest accounts. If one reads
about the experiments as presented in The Herring Gulls World,
without knowledge of the intermediate publications, one would
believe that the study was done during 1946 instead of 1947; that
792 C. ten Cate / Animal Behaviour 77 (2009) 785794
the methodology consisted of a balanced design offering each
model with equal frequency instead of repeated testing against
a standard model; that Fig. 1n and o were based on separate
experiments; that the experiment reported in Fig. 1o was done with
models lacking the eyes, and that Fig. 1n represented the proper
responses to models with differently coloured patches on their
beak. In fact, when I gave students both the 1948a paper and
chapter 22 of The Herring Gulls World to compare, quite a few
believed these must have been different experiments. The data in
The Study of Instinct also deviate from the 1947 summary, and
suggest the presence of three separate experiments. In addition,
Fig. 1c, j and m, based on the 1947 data, differ in numbers from the
original data (albeit marginally), as well as from each other (see
Appendix). In fact, none of the publications matches the original
numbers.
We cannot be sure about the causes for the changes over the
years, but may speculate about these. One factor might be related
to Tinbergens move from Leiden to Oxford during 1949. By all
available accounts (Roell 1996, 2000; Kruuk 2003; Burkhardt
2005), it is obvious that this was a very hectic period in his life. He
had to teach many students, was coping with an increasing burden
of administrative duties and was disappointed about the atmo-
sphere in postwar Holland. Anyone makes mistakes and small
inaccuracies such as wrong numbers for N values or mixing up
dates might be consequences of this hectic period. They may be
sloppy, but these issues are details and irrelevant to the main
conclusions of the herring gull study. However, the modications
to the original data, such as presenting the corrected data as the
real ones without mentioning the corrections, presenting data as
though they originate from different experiments, or presenting
the methodology as different from what is has been, extend
beyond such details. The fact that Tinbergen in the 1949 and 1950
papers extensively discussed the methodological error of pre-
senting the standard stimulus more frequently than the other
models shows he had no intention to manipulate or manufacture
the data. Tinbergen also stated that in subsequent experiments he
altered the test procedure to avoid the problem, and hence the
correction affects only a small subset of the data. Nevertheless, the
question remains why he changed the early data and presented
these as the proper data, rather than repeating the experiment in
a more balanced way.
In his biography of Tinbergen, Kruuk (2003) expressed worries
that the herring gull study may have suffered from observer
biases, expectations of how the chicks should behave. Such biases
may unintentionally have affected the way in which the experi-
menters presented the various models and hence the outcome of
the experiments. The studies discussed above suggest that the
inuence of biases did not stop here, but also affected the
subsequent interpretation and presentation of the results.
The majority of the herring gull publications present the results
not as a test, but rather as an illustration of ethological concepts.
The corrected data for the rst experiment in the herring gull
study tted better with the expectations Tinbergen expressed
early on, and the experiment to test the effect of habituation
probably convinced him that the early data were anomalous. From
this it is a small step to considering and treating the corrected data
as the real ones. It may also explain why Tinbergen apparently saw
no problem in separating the data obtained with the model with
the patch on the forehead from the other ones and in recombining
and presenting them in different contexts. While such data use
may reect the less rigid procedures of those early days, it also
seems an example of Tinbergens tendency, observed by Kruuk
(2003), to t the data to his ideas rather than the other way
around. It raises the question whether Tinbergen went too far in
his adjustments of the data.
Over the years, discussions on the issue of desirable or
responsible conduct in research have identied strong views and
expectations on the outcome of experiments as a risk factor that
may, intentionally or unintentionally, bias researchers in consid-
ering the evidence (Anonymous 1995; Bateson 2005) and result in
irresponsible scientic conduct. The herring gull story seems
a clear illustration of how an expectancy bias can colour the data
treatment and conclusions. Nevertheless, opinions of what is
irresponsible conduct vary between people (Montgomerie &
Birkhead 2005) and are likely to vary over time. Hence, views may
differ on the extent to which Tinbergens behaviour should be
seen as irresponsible. In my view it should if we apply todays
standards. However, Tinbergen did the study in another era.
Todays practice that papers are subject to independent and crit-
ical refereeing, which can serve to counteract such biases, was not
an established practice at the time, and is very unlikely to have
happened. More importantly, the postwar years were a decisive
period for the new discipline to establish itself as a serious and
competitive branch of science, particularly in relation to the
comparative psychologists dominating the study of animal
behaviour in the U.S. (Burkhardt 2005). Apart from Tinbergens
strong expectations, one can imagine that, put in the context of
the scientic controversies surrounding the birth of the discipline,
he was tempted to present the data as more clear-cut than they
were. Although it cannot be a justication, one might even argue
that the discipline might not have been where it is today had he
not done so.
Finally, how about the conceptual insights provided by the
study? Overlooking the publications, it can be noted that what
started off as a relatively simple experiment on what stimulated
chicks to beg grew into a story about the analysis and complexity
of sign stimuli, releasers and releasing mechanisms in general. It is
a story that denitely contributed to the rise of ethology. However,
one might also say that the same story, rather than making these
concepts widely acceptable, may have contributed to their demise.
This is because Tinbergens inference about the presence of more
and more abstract and complex congurational sign stimuli as
nearness or lowness required the concepts, and therefore the
proposed releasing mechanisms needed to explain them, to
become more and more intricate. At the same time, the experi-
ments were not sufciently rigorous to support these ideas. This
was already questioned by Schneirla and others at the Macy
conference mentioned before, and to some extent admitted by
Tinbergen. Later on, this was conrmed by extensive and more
controlled experiments on the begging of gull chicks, in particular
and most thoroughly by Hailman (1967, 1969) and Gould and
coworkers (Gould 1982; Margolis et al. 1987; Alessandro et al.
1989) but also others (Evans 1979; Eypasch 1989; Zippelius 1992).
With respect to the colour preferences, studies by Hailman (1967)
and Eypasch (1989), while conrming that nave chicks did have
a preference for red objects over blue ones, and for blue over
yellow, showed that these preferences were not so clear as Tin-
bergen thought at the time (see also ten Cate et al. 2009 for
a discussion). As for other features, Hailman (1967, 1969) and
others (Alessandro et al. 1989) demonstrated that chicks collected
from the eld and with some experience with parents had specic
preferences, also for some congurational features. However, truly
nave chicks, that is, hatched in an incubator rather than collected
from the eld were less clear in their preferences and the results
showed no need to invoke a sensitivity to complex, congura-
tional sign stimuli. For instance, when movements of the model
were controlled for, nave chicks pecked equally often at the patch
wherever it appeared on the head. Hence they appeared to
respond to discrete features, rather than congurations. So, these
studies demonstrated that it was possible to link several of the
 C. ten Cate / Animal Behaviour 77 (2009) 785794
phenomena that Tinbergen claimed to be complex and innate to
simpler perceptual properties of the sensory system or to inter-
pret them as the outcome of a learning process. Evans (1979) and
Eypasch (1989), for instance, demonstrated that a few feeding
trials and 510 min of exposure were sufcient to give chicks
a preference for a variety of odd, nongull-like, models. How-
ever, whether this, in combination with some methodological
problems, should serve as a basis to dismiss the study altogether,
as argued by Zippelius (1992), is a different matter. Rather,
Tinbergens outcome might be considered to reect the prefer-
ences of chicks with some experience with the parents, which is to
be expected with chicks obtained from the eld.
What has so far remained an open question is whether
Tinbergens corrected data do, as he assumed, match the outcome
that would result using a balanced design. This question has been
addressed in a recent experiment using replicates of Tinbergens
models (ten Cate et al. 2009). It shows that Tinbergens intuitions
were largely correct.
To conclude, looking backwards it is important to note that the
herring gull study was an inspiring piece of experimental work
that fullled an important role by making clear how questions
about the mechanisms underlying behaviour can be tackled with
ingenious experiments and that fostered theoretical progress as
well as subsequent studies. At the time the study was carried out,
behavioural biology still had to nd its place as a scientic disci-
pline and the appeal of the herring gull study has certainly
contributed to achieving that aim. The many publications
Tinbergen devoted to the study helped spread the message to
a wider audience, as is reected in the many textbooks that still
refer to the study. Tinbergen deserves the credit for this. Also, as
stated above, the part of the herring gull study presented here was
selected because of its anomalies, not because it is representative
of the study as a whole, let alone of everything Tinbergen did.
Nevertheless, it seems that even a great scientist may not have
been immune to the scientic biases and prejudices that can affect
any of us.
Acknowledgments
It took time for this paper to materialize. While it was not too
difcult to get an overview of the various publications, I wondered
whether it was a story that should be published. The responses I got
upon presenting some of the material at a few small meetings and
in my teaching encouraged me to give it a try and send a draft to
various colleagues. Some expressed worries: the story might be
detrimental to Tinbergens heritage or to our eld. Others, however,
convinced me that both the Tinbergen legacy and our eld do not
depend on this story and found it evident that it should be
published. I took all comments to heart, and can only hope that, in
the end, I managed to present the story in a balanced way, doing
justice to Tinbergen. If I did not succeed, I take the full blame for it.
For their comments and views on the issue I am most grateful to Pat
Bateson, Innes Cuthill, Rob Lachlan, Kevin Laland, Katharina Riebel,
Candy Rowe, Hans Slabbekoorn, Fritz Trillmich (who also provided
access to the studies by Eypasch and Zippelius), Dirk van Delft, Jos
van den Broek, Ed van der Meijden, Peter Slater, four anonymous
referees and Louise Barrett. All the material left from Tinbergens
period at Leiden has been donated as a permanent loan to the
Boerhaave science museum at Leiden.
Supplementary Material
Supplementary material associated with this paper can be
found, in the online version, at doi:10.1016/j.anbehav.2008.12.021.
793
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APPENDIX
Note 1: Fig. 1b gives 70 as the value for the model with the white
patch, instead of 71 as on the 1947 data sheet.
Note 2: the number of pecks at the forehead is mentioned as 73
in this gure, while the number in the 1947 data is 74.
Note 3: the value for the model with the white patch, which was
reduced to 70 in Tinbergen (1948a, Fig. 1b), is now again at the
original value of 71.
Note 4: there is a puzzling feature about these data. According to
the gure, both models together got 809 responses. A hand-written
note about this gure reveals that the responses consist of 652
pecks to the standard model and 157 pecks to the model with the
patch on the forehead. However, as mentioned above, Tinbergen
noted that all models were tested against the standard model, but
while the 157 pecks to the model with the patch on the forehead
have been subtracted from the 1095 pecks mentioned in the 1947
data sheet, the 652 pecks to the standard model are not. This
suggests that the total number of responses as mentioned in both
the data sheet (1095) and in the gure (938 pecks) are an adjusted
gure, perhaps using the average number of pecks to the standard
model, rather than the total.
Note 5: surprisingly, the introduction of the paper mentions that
the rst experiments were done in 1946. This does not match with
the statements in the earlier papers (Tinbergen 1948a, 1949), nor is
there any hint in the Behaviour paper, or elsewhere, that herring
gull data were or might have been collected in 1946.
Note 6: the corrected values that are given for the blue and the
white patch are 71 and 59, whereas a proper correction of the
original data should have led to the maximum values of 70 and 58.
Note 7: the number of pecks at the red patch is now given as 75,
rather than the original 74.
Note 8: the number of pecks at the forehead is now again
provided as 74.