Tools and Brains in Birds: Louis Lefebvre Nektaria Nicolakakis and Denis Boire

TOOLS AND BRAINS IN BIRDS
by
LOUIS LEFEBVRE1) , NEKTARIA NICOLAKAKIS and DENIS BOIRE 2,3,4)

(1 Department
of Biology, McGill University and 2 Département des Sciences Biologiques,
Université de Montréal, Montréal, Québec, Canada)
(Acc. 14-V-2002)
Summary
Tools are traditionally de ned as objects that are used as an extension of the body and held
directly in the hand or mouth. By these standards, a vulture breaking an egg by hitting it
with a stone uses a tool, but a gull dropping an egg on a rock does not. This distinction
between true and borderline (or proto-tool) cases has been criticized for its arbitrariness
and anthropocentrism. We show here that relative size of the neostriatum and whole brain
distinguish the true and borderline categories in birds using tools to obtain food or water.
From two sources, the specialized literature on tools and an innovation data base gathered
in the short note sections of 68 journals in 7 areas of the world, we collected 39 true (e.g.
use of probes, hammers, sponges, scoops) and 86 borderline (e.g. bait shing, battering
and dropping on anvils, holding with wedges and skewers) cases of tool use in 104 species
from 15 parvorders. True tool users have a larger mean residual brain size (regressed against
body weight) than do users of borderline tools, con rming the distinction in the literature. In
multiple regressions, residual brain size and residual size of the neostriatum (one of the areas
in the avian telencephalon thought to be equivalent to the mammalian neocortex) are the best
predictors of true tool use reports per taxon. Innovation rate is the best predictor of borderline
tool use distribution. Despite the strong concentration of true tool use cases in Corvida
and Passerida, independent constrasts suggest that common ancestry is not responsible for
the association between tool use and size of the neostriatum and whole brain. Our results
demonstrate that birds are more frequent tool users than usually thought and that the complex
1)
Corresponding authors’s e-mail address: louis.lefebvre@mcgill.ca
3) Current address: Ecole d’Optométrie, Université de Montréal.
4) We are grateful to Simon Reader for comments on earlier versions and to Sarah
Timmermans for alerting us to the existence of Mlikovsky’s data. We also thank Simran
Kurir, Yutaka Nishioka and Johan Bolhuis for help with the German, Japanese and Dutch-
language papers. This work was funded by an NSERC grant to LL and an FCAR fellowship
to NN.
© Koninklijke Brill NV, Leiden, 2002 Behaviour 139, 939-973
Also available online -
940 LEFEBVRE, NICOLAKAKIS & BOIRE
cognitive processes involved in tool use may have repeatedly co-evolved with large brains in
several orders of birds.
Introduction
When used by humans, hammers, sponges, pokers, anvils and vices are
all classi ed as tools. In other animals, however, only the rst three are
considered legitimate. This is because the de nition of ‘true’ tools in the
literature speci es that they must be detached from the substrate and directly
held by the animal in the hand or mouth (van Lawick Goodall, 1970; Beck,
1980; McFarland, 1982). In this view, a vulture breaking an egg by hitting
it with a stone is using a tool, but a gull dropping an egg on a rock is
not. Several authors have criticised the arbitrariness (Hansell, 1987) and
anthropocentrism (Shettleworth, 1998) of this distinction .
Studies of tool use in animals tend to focus on manipulative, large-
brained species that are closely related to humans, e.g. primates (Fragaszy
& Visalberghi, 1989; McGrew, 1992; Whiten et al., 1999). Birds, unlike
primates, lack both hands and close hominid parentage and are generally
thought to be poor tool users. A review from the 1960’s, for example,
concludes that the entire class (close to 10 000 species) features only one
documented case of true tool use, the insertion of twigs in crevices by the
woodpecker nch of the Galapagos Islands (Thomson, 1964). The recent
description in Nature of leaf tool manufacture in New Caledonian crows
(Hunt, 1996) is all the more noteworthy because of the apparent rarity of
such reports in birds.
In a series of review papers, Boswall (1977, 1978, 1983a, b) pointed
out that cases of tool use in birds may be more numerous that we think.
He classi ed the literature into two categories, ‘true’ and ‘bordeline’ cases.
Following the traditional de nition, borderline cases (called ‘proto-tools ’
by Parker & Gibson, 1977) involve the use of objects that are part of a
substrate, e.g. anvils on which prey are battered or dropped, wedges and
thorns with which food is held, bait that is deposited on water to attract sh.
True tools are detached from the substrate, e.g. hammers, probes, scoops,
sponges and levers held directly in the beak or foot. If true tool use is
cognitively more demanding than is borderline tool use (Parker & Gibson,
1977; Hansell, 1987; Vauclair, 1997), relative size of key brain structures
could also distinguis h the two categories (Gibson, 1986).
TOOLS AND BRAINS IN BIRDS 941
In birds, there is large taxonomic variation in the relative size (regressed

against body weight or divided by brainstem size) of neural structures
thought to underlie cognition. For example, the neostriatum /hyperstriatum
ventrale complex (Rehkämper & Zilles, 1991; Dubbeldam, 1989, 1991,
1998) is ve and a half times larger in carrion crows than it is in quail
(Rehkämper et al., 1991). Reader & Laland (2002; Reader, 1999; see also
Gibson, 1986) have shown that the taxonomic distributio n of tool use
cases is positively correlated with size of the neocortex and striatum in
primates. In this study, we look for similar neural correlates of tool use in
birds. Volumetric data on the neostriatum , hyperstriatum ventrale and other
telencephalic areas (see Fig. 1) are available for 32 avian species covering
17 parvorders (Boire, 1989; Rehkämper et al., 1991; Timmermans et al.,
2000; avian taxonomy according to Sibley & Monroe, 1990), while whole
brain size is available for 737 species from 35 parvorders (Mlikovsky, 1989a,
b, c, 1990). We use both the 737 species data set on whole brains and
the 32 species data set on telencephalic areas to test the idea that neural
structure size is positively correlated with the taxonomic distribution of tool
use reports in birds and provides an independent criterion for distinguishin g
the true and borderline categories. For the 32 species data set, we compare
relative size of the neostriatum and hyperstriatum ventrale with that of two
other telencephalic structures that are thought to be less closely involved in
cognition, the wulst and the striatopallida l complex. Like the mammalian
neocortex, the neostriatum and hyperstriatum ventrale play a crucial role
in several kinds of learning (McCabe et al., 1982; Horn, 1990; Nottebohm
et al., 1990; MacPhail et al., 1993). In contrast, the wulst is a sensory
projection area for visual and somatosensory information (Karten et al.,
1973; Shimizu et al., 1995), while the striatopallida l complex is involved
in stereotyped, species-speci c responses (Reiner et al., 1984; Dubbeldam,
1998). Both the wulst and striatopallida l complex play some role in learned
behaviour (wulst: MacPhail, 1976; Shimizu & Hodos, 1989; Deng & Rogers,
1997, 2000; striatopallida l complex: Parent, 1986; Stewart et al., 1996;
Mezey et al., 1999), but they are less specialized in complex integration than
are the neostriatum and hyperstriatum ventrale. In a multiple regression, the
size of the wulst and striatopallida l complex should consequently be less
closely correlated with the number of tool use reports than should size of the
neostriatum and hyperstriatum ventrale.
Fig. 1. Coronal sections of the telencephalon of Alectoris chukar, illustrating the hypers-
triatum ventrale (HV), the neostriatum (Neo), the archistriatum (Archi), the nucleus basalis
(n Bas), the wulst (W), and the striatopallidal (Paleo) complex. Top: rostral section; bottom:
caudal section. Scale bars in upper left-hand corner represent 1 mm.
We use two data sources for estimating the number of tool use cases. First,
we review the specialized literature, starting from Boswall’s (1977, 1978,
1983a, b) comprehensive papers and incorporating cases published since
then (e.g. Andersson, 1989; Marks & Hall, 1992; Hunt, 1996; Caffrey, 2000).
Secondly, we use feeding innovation data accumulated for several areas
of the world (Lefebvre et al., 1997, 1998, 2001; Nicolakakis & Lefebvre,
2000; Timmermans et al., 2000). At present, this data base includes close
to 1800 cases of new, unusual or rare foraging techniques or food types

used by birds, found by exhaustively searching the short note section of 67
ornitholog y journals over an average of 30 years. Reader & Laland (2002;
Reader, 1999) have shown that the number of tool use reports is positively
correlated with innovation rate in primates. We look for a similar relationship
in birds. According to Wyles et al. (1983) and Wilson (1985), innovation ,
social learning, brain size and cognitively-comple x behaviours like tool use
are all expected to co-vary in opportunisti c taxa that exploit a wide array of
rapidly-changin g environmental conditions.
Methods
Tool use cases
The specialized literature on tool use was rst searched for all true and borderline cases
related to feeding and drinking, starting with the classic reviews of van Lawick Goodall
(1970), Beck (1980) and Boswall (1977, 1978, 1983a, b). To these were added all cases
found in the literature after 1983, the year of Boswall’s last exhaustive review. These include
Andersson (1989), Hunt (1996) and the review by Switzer & Cristol (1999), as well as papers
from the bibliographies of innovation notes (e.g. Duyck & Duyck, 1984, found in Clayton and
Jollife, 1996) and articles listed under ‘tool-using’ in The Zoological Record. Other tool use
functions (e.g. grooming: Dubois, 1969; defence: Caffrey, 2001) are sometimes mentioned
in the literature, but we focused only on feeding and drinking because these are the only
behaviours covered by our other source, innovation reports.
Cases were classi ed in ve categories, true tool use and four sub-categories of borderline
tool use (dropping prey on a hard substrate, battering on an anvil, baiting, holding prey
with a wedge or skewer). We excluded all cases considered unreliable by Boswall, unless
later reports concluded otherwise. For example, egg-breaking with stones in Hamirostra
melanosternon is listed in Wilson (1975), excluded by Boswall (1983a), but con rmed
by Debus (1991) and Pepper-Edwards & Notley (1991). Use of leaves for grasping nuts
in Probisciger aterrimus is also excluded by Boswall (1983a); this negative judgement is
con rmed by Bertagnolio (1994). Save for two exceptions, string-pulling was also excluded
because van Lawick Goodall (1970) and Boswall (1977) argue that the visual continuity
between the food and the string make the latter no different from a stem or branch. The two
exceptions we decided to include are the ice shing cases described by Holmberg (cited by
Scott, 1974 and Boswall, 1977). In these cases, Boswall points out that there is no visual
continuity between the line and the sh hidden under the ice. The impact of our decision
is evaluated later in the results section by comparing inclusion and exclusion of the two
cases. The effects of a second decision, inclusion or exclusion of cases from captivity, is also
evaluated in a similar way. A total of 71 cases of true or borderline tool use were found in the
specialized literature.
The second set of tool use cases was obtained by searching through the innovation data
base collected over the years in our laboratory. This data base currently contains 1796
innovations in 6 areas of the world (North America, western Europe, India, Australia, New
Zealand, southern Africa), collected by exhaustively searching the short note sections of
67 ornithology journals over an average of 30 years (see Lefebvre et al., 1997, 1998 and
Nicolakakis & Lefebvre, 2000, for examples and details on the collection method). For
the purpose of this paper, a 68th journal was also searched, Noticias de Galapagos, which
covers a geographical zone outside the six included in our normal data base, but where
several tool using cases have been reported (e.g. Hundley, 1963; Curio & Kramer, 1964;
Millikan & Bowman, 1967). Innovations are de ned as the ingestion of a new food type or
the use of a new foraging technique, based on terms in the short note such as ‘ rst report’,
‘unusual’, ‘unknown’, ‘rare’, ‘opportunistic’, ‘adaptable’, ‘strange’, ‘not noted before’, ‘not
recorded’, ‘not mentioned in the literature’. All measures taken up to now indicate that
innovation frequency is a valid and reliable operational estimate of feeding exibility in birds.
Correlations between the taxonomic distribution of innovation rates obtained by different
readers (usually blind to the hypothesis) on the same sets of journals vary between 0.827
and 0.910 (p < 0:001; Lefebvre et al., 1998; Nicolakakis & Lefebvre, 2000). Inter-
taxon differences in innovation rate correlate with problem-solving differences found in
the literature (Timmermans et al., 2000) and in experimental tests conducted in the eld
and in captivity (Webster & Lefebvre, 2001). Nine potential biases have been examined:
number of species per taxonomic group, avian population size, research effort per taxon,
interest by ornithologists, reporting bias, journal source, editorial style, juvenile development
mode, phylogeny. Only the rst of these variables, species number, needs to be included in
multiple regressions to express innovation rate as an unbiased index (Lefebvre et al., 1998,
2001; Nicolakakis & Lefebvre, 2000). The ve tool use categories taken from the specialized
literature were used with the innovation data base. 61 cases of true or bordeline tool use
were found in the data base; seven of these also appeared in the specialized literature and
were eliminated. Among the dropping cases, we included breaking of booby eggs on rocks
by Geospiza dif cilis (Köster & Köster, 1983; Grant, 1986). In this case, the eggs are not
dropped from the air, but thrown down by pushing, rolling, bracing and levering with the bill
and feet; substrate use is thus the same as in other dropping cases, even if the bird is not in
ight when it drops the egg.
Once all tool use cases in the innovation data base had been identi ed, they were removed
from the data set in each geographic zone. For each zone, innovation frequency per taxon
was then regressed against its most important confound, species number, obtained from
standard ornithology texts (India: Ali & Ripley, 1995; New Zealand: Falla et al., 1979;
Australia: Simpson & Day, 1996; North America: Scott, 1987; Europe: Hagemeijer & Blair,
1997; southern Africa: Sinclair & Hockey, 1996) and reclassi ed according to Sibley &
Monroe (1990) if initially given in non-molecular taxonomy. Standardized residuals were
then determined for each zone where a taxonomic group was present and a weighted average
innovation rate calculated by taking into account the number of innovation cases yielded
by each zone, similar to the procedure used by Timmermans et al. (2000). Sampling error
potentially caused by a small regional data set is minimized when each zone is weighted
by the number of cases it contributes to the total. A large avifaunal zone with extensive
literature coverage (e.g. western Europe: 701 innovations in 24 journals) is likely to yield
a more reliable measure than is a smaller zone with fewer journals (e.g. New Zealand: 57
innovations in only one journal).
Neuroanatomical data
Data on whole brains were taken from Mlikovsky (1989a, b, c, 1990). These data include cra-
nial volumes (with appropriate corrections to estimate actual brain mass) measured by the au-
thor on museum specimens for 615 species (Mlikovsky, 1989a), as well as fresh-weight data
on 151 species taken from previously published sources (e.g. Crile & Quiring, 1940; Port-
mann, 1947; Armstrong & Bergeron, 1985). We rst checked all secondary data included in
Mlikovsky’s tables against the previously published source and averaged sets of species listed
as separate by Mlikovsky but now considered monospeci c by Sibley & Monroe (1990). We
then took standard body weights from the CRC Handbook (Dunning, 1993) and regressed
log brain size against log body weight for all species. From the residuals of this regression,
we looked for outliers that could potentially indicate an unreliable source; any species whose
residual brain size was more than 2 standard deviations away from the mean of its family
was eliminated. We reran the regression of log brain size against log body weight for the 737
remaining species and used the residuals of this regression as our nal data. Mean residuals
were calculated for each parvorder, following the procedure used in previous papers on inno-
vations and neural structure size (Lefebvre et al., 1997, 1998, 2001; Nikolakakis & Lefebvre,
2000; Timmermans et al., 2000). In the analyses below, the species level residual is used
whenever a tool using species is included in Mlikovsky’s data base (61 of the 125 cases of
tool use). When it is not, the mean residual of the closest available taxonomic level (genus:
21 cases; family: 36 cases; parvorder: 1 case; suborder: 6 cases) is used as an estimate. Mean
residual at the parvorder/suborder level predicts 73% of the variance at the species level, while
means at the genus and family level respectively predict 91% and 82% of the species level
variance. Mlikovsky’s data base includes the 32 species featured in Boire (1989) and Rehkäm-
per et al. (1991); the correlation between the brain sizes measured in the two data sources is
0.998 (N D 32, p < 0:001), indicating that Mlikovsky’s measurements are reliable.
Volumetric data for the four telencephalic areas (Fig. 1) were taken from Boire (1989;
28 species) and Rehkämper et al. (1991; 4 species). Rehkämper et al. (1991) cover 6
species, but two of these, Coturnix coturnix and Phasianus colchicus, are also included in
Boire (1989); for these cases, we used the mean of the data reported in the two sources.
Of the four telencephalic areas used in the analysis, only the hyperstriatum ventrale is
anatomically de ned in identical terms in Boire (1989) and Rehkämper et al. (1991).
For the other three structures, areas are lumped or split in different ways and must be
regrouped at a level where they are are identical. The neostriatum of Rehkämper et al. (1991)
includes the archistriatum, neostriatum and nucleus basalis prosencephali of Boire (1989).
The striatopallidal complex comprises the paleostriatum in Rehkämper et al. (1991) and
the basal telencephalon, paleostriatum augmentatum and paleostriatum primitivum in Boire
(1989). The wulst is measured as a single structure in Boire (1989), whereas it corresponds
to the sum of the hyperstriatum accessorium (incorporating the hyperstriatum intercalatus
superior) and hyperstriatum dorsale in Rehkämper et al. (1991). As was done for the whole
brain, volume of each of the four structures was regressed (after log transformation) against
the body weight of the subjects given in Boire (1989) and Rehkämper et al. (1991); average
residual deviations were then calculated for each of the 17 parvorders present in the sample.
Regressions, phylogeny and independent contrasts

All regressions were conducted on Systat (Wilkinson, 1995). Depending on the analysis, the
dependent variable was the taxonomic distribution of either true or borderline tool use reports.
The number of reports was log transformed before analysis to normalize its distribution,
since the data include very large numbers (true tool use in Corvida represents 40% of the
sample) and very small ones (several parvorders with zero cases). Depending on the analysis,
the independent variables were (1) mean residual brain size per taxon; (2) mean residual
size per taxon of each of the four telencephalic areas; (3) innovation rate (calculated as a
weighted average per taxon for the 6 zones of the world, excluding tool use cases); (4) number
of species per taxon (log transformed), an obvious confounding variable of the number of
tool use reports (a parvorder like Passerida, which has 3556 species according to Sibley &
Monroe, 1990, is likely to yield more reports than the parvorder Odontophorida, which has
only six species); and (5) juvenile development mode, a known confounding variable of avian
brain size (Bennett & Harvey, 1985; nidicolous, altricial birds have larger brains as adults than
do nidifugous, precocial ones).
Three estimates of tool use were used in the multiple regressions. The rst one used
all cases found (39 true tools, 86 borderline), tabulated them at the level of the parvorder
and entered them in the regressions as independent cases. The second estimate eliminated
potential pseudoreplication and phyletic confounds caused by genera with many tool use
reports. Some genera include several species that use one or more techniques. For example,
there are 10 cases of borderline tool use in Larus (dropping and baiting), ve in Pitta (all
battering) and 11 in Corvus (dropping and battering). These multiple entries could bias the
results by arti cially creating many data points with similar relative brain size values. We
eliminated the 48 cases where more than one species and/or more than one technique are
reported in a genus and redid the regressions on these genus-level data. The third estimate
was based on independent contrasts, not frequencies per taxon. If Passerida and Corvida both
have large brains and a high number of tool use reports, the association between these traits
could be caused by the relatively recent divergence of the two parvorders; a similar phyletic
confound is less likely to be the case for Corvida and Psittaciformes, which are very distantly
related (see phyletic trees in Figs. 3 to 6). We used the CAIC computer program written
by Purvis & Rambaut (1995), a technique that factors out common ancestry by estimating
trait values at ancestral nodes, averaging empirical values for related extant taxa weighted by
phyletic distance. The phyletic branch lengths entered in the CAIC regressions are taken from
Sibley & Ahlquist (1990) and are based on DNA hybridization distances. Multiple regressions
(forced through the origin) are then conducted on the contrasts, not the actual parvorders used
in our rst two estimates.
Results
Tool use distributio n
A total of 125 cases were found in the two data sources, after removal of
the 7 overlapping reports. Despite the low degree of overlap, the two data
sources provide similar taxonomic distribution s of total tool use reports:
the correlation between the two sources is 0.806 (p < 0:001, N D
35 taxonomic groups). The 125 cases are listed in Table 1 by tool use
category and taxonomic group. Several trends are immediately obvious in
this table. The cases are widely distributed amongst 104 species in 15
parvorders. Nineteen species use more than one technique, seven of them
in the genus Corvus. The common crow Corvus brachyrhyncho s is the
species showing the most techniques; it uses stone hammers to open acorns,
sharpens a piece of wood to probe a hole, drops palm fruits and nuts on
asphalt roads (but may not systematically use cars to break the food open,
Cristol et al., 1997, contra Maple, 1974 and Grobecker & Pietsch, 1978;
see however Caffrey, 2001), batters sh on hard sand (also scaling it on
the sand by scraping), and, in captivity, uses a scoop to carry water to
dry food. Several tool use categories are concentrated in particular taxa.
Twenty-eight of the 39 cases of true tool use occur in two Passeriforme
parvorders, Passerida and Corvida (suborder Passeri). All four cases of tool
use in Psittaciformes involve captive birds. Holding food with a wedge or
a skewer is reported in Corvida and Piciformes. Dropping food to break
it open on a hard surface is equally distributed among three parvorders,
Charadriida, Accipitrida and Corvida. There are no tool use reports in large,
well-studied taxa like Phasianida, Anseriformes, Columbiformes, Falconida,
Apodiformes and Podicipedida, nor in smaller, poorly-studie d groups like
Coliiformes, Galbuliformes, Trogoniformes, Phaethontida and Pteroclides
(see phyletic trees in Figs. 4 and 6).
The relationship between brain size and each of the tool use categories is
illustrated in Fig. 2. Brain sizes are directly available for the species involved
in 61 cases. In the 64 others, the species are assigned the mean residual brain
size of its genus (N D 21/, family (N D 36/, parvorder (N D 1/ or suborder
(N D 6, all Tyranni). As can be seen in Fig. 2, dropping, baiting and battering
on an anvil are used by birds with a wide range of brain sizes. Several of these
(e.g. gulls, herons, anhingas, roadrunners) have negative brain size residuals.
In contrast, true tool use is overwhelmingly shown by birds with positive
residuals. The two notable outliers are a captive oystercatcher that uses sticks
to dislodge invertebrates in a zoo (residual brain size ¡0:598; Olney, in
Boswall, 1978) and the bristle-thighe d curlew, who throws coral stones at
albatross eggs on Paci c islands (Marks & Hall, 1992). It is noteworthy that
this species, Numenius tahitiensis , is the one with the largest brain in its
parvorder, Scolopacida (residual D ¡0:236; parvorder mean D ¡0:757,
N D 20).
On average, true tool users have a larger residual brain size than do
borderline tool users; the mean for the rst category (1.060, SEM D 0.130,
T ABLE 1. Borderline and true tool techniques used by different species, classi ed by taxon. Brain size given as
948
residual deviation from log-log regression against body weight

Taxon Species Technique Reference Brain size
Bait sh
Coraciiformes Ceryle rudis Bait with bread Root, in Boswall 1983a 0.161
Grui Eurypya helias Bait with maggots Alders, in Boswall 1977 ¡0:066
Charadriida Larus fuscus Bait with bread; captive Sinclair 1984 0.155
Accipitrida Milvus migrans Bait with bread Roberts 1982 0.325
Ciconiida Ardeola ralloides Bait with insects Crous 1994 ¡0:761
Butorides striatus Bait with bread, Higuchi 1986; Keenan 1981; ¡0:308
insects, twigs, feathers Foxall & Drury 1987;
Wood 1986; English 1987;
Batter on anvil
Coraciiformes Ceryle rudis Batter crab on rocks Cooper 1981 0.161
Dacelo novaeguineae Batter rat and bone Roberts 1961 0.790
Halcyon smyrnensis Batter frog on branch Tehsin 1989 0.193
Cuculiformes Geococcyx californianus Batter reptiles on rocks Meinzer 1993 ¡0:246
Caprimulgi Podargus strigoides Batter feathers off Wheeler 1943 0.716
prey against dead bough
Ralli Eulabeornis castaneoventris Batter shells on anvils Woinarski et al. 1998
LEFEBVRE, NICOLAKAKIS & BOIRE
¡0:577*
Scolopacida Numenius tahitiensis Batter crabs on rocks Marks & Hall 1992 0.236
Accipitrida Buteo jamaicensis Slam snake on rock in ight Ellis & Brunson 1993 0.843
Gypaetus barbatus Batter bones on rocks Fleming 1955 0.860
Sulida Anhinga anhinga Batter sh on branch Wellenstein & Wiegmann 1986 ¡1:342
Ciconiida Threskiornis molucca Batter mussels on anvils Vestjens 1973 ¡0:021
Tyranni Xenicus gilviventris Batter grasshopper Sibson 1974 0.771*
on corrugated iron
Pitta erythrogaster Batter hard-shelled prey McDonald 1974 0.771*
T ABLE 1. (Continued)
Pitta guajana Batter hard-shelled prey Chasen 1939 0.771*
Pitta moluccensis Batter hard-shelled prey Robinson 1927 0.771*
Pitta sordida Batter hard-shelled prey Robinson 1927 0.771*
Pitta versicolor Batter hard-shelled prey Hindwood 1966 0.771*
Corvida Lanius collaris Batter grasshopper on Gore 1981 0.318
post then skewer on thorn
Corvus brachyrhynchos Batter sh on sand, Phillips 1978 2.121
wipe on sand (to scale?)
Colluricincla harmonica Batter mouse on stump, Tilt 1962; Reilly 1966 1.554*
wren and robin on rock
Corcorax melanorhamphos Batter mussels Hobbs 1971 1.554*
Ailuroedus dentirostris Batter snails on stones Marshall 1954 1.313*
Daphoenositta chrysoptera Bash insects on branch Noske 1985 1.554*
Falcunculus frontatus Bash insects on branch Noske 1985 1.554*
Passerida Ficedula hypoleuca Batter snails Page 1978 ¡0:045*
Myiophonus caeruleus Batter shells on rocks Smythies, in Boswall 1978 ¡0:045*
Oenanthe leucura Batter lizard on stone Heselden et al. 1996 ¡0:045*
Oenanthe oenanthe Batter caterpillars King 1978 ¡0:045*

Saxicola rubetra Batter caterpillars King 1978 ¡0:234
Saxicola torquata Batter snails Fisher 1979 ¡0:234*
Saxicoloides fulicata Batter frog and gecko Sivasubramanian 1991 ¡0:045*
Turdus iliacus Batter snails Richards 1977 0.364
Turdus pelios Batter snails on rocks Walsh & Walsh, in Boswall 1983b 0.379
Turdus philomelos Batter snails on rocks Boswall 1977 0.088
Anthus petrosus Batter snails Tutt 1990 ¡0:846*
Passer domesticus Batter wings Hammond 1997 0.402
off damsel ies
949
950
Ploceus philippinus Batter frogs George 1973 ¡0:347*
on electrical wire
Pycnonotus cafer Batter gecko on wall Bharos 1999 0.455*
Acridotheres fuscus Batter mouse Johnsingh 1979 0.496*
Drop on substrate
Grui Cariama cristata Drop eggs on stones Kooij & van Zon 1964 ¡0:013*
Scolopacida Numenius tahitiensis Drop eggs Marks & Hall 1992 0.236
Charadrida Catharacta skua Drop penguin eggs Sladen, in Boswall 1977 ¡0:198*
Larus argentatus Drop rabbits on rocks Young 1987 ¡1:179
Larus canus Drop molluscs Cristol & Switzer 1999 0.142
Larus delawarensis Drop molluscs Cristol & Switzer 1999 ¡0:198*
Larus dominicanus Drop egg on water Moon 1992 ¡0:098
Larus glaucescens Drop molluscs Cristol & Switzer 1999 ¡0:198*
Larus marinus Drop crabs on hard sand; Cramp & Simmons 1983 ¡0:287
drop rat Harber & Johns 1947
Larus melanocephalus Drop molluscs Cristol & Switzer 1999 ¡0:198*
Larus occidentalis Drop molluscs Cristol & Switzer 1999 ¡0:198*
Larus paci cus Drop mussels on road Wheeler 1946 ¡0:198*

Accipitrida Aquila chrysaetos Drop tortoises Leshem 1985 0.164
Gypaetus barbatus Drop bones and tortoise Boswall 1977 0.860
Haliaeetus leucocephalus Drop tortoises Bindner 1968 0.403
Neophron percnopterus Drop tortoise and lizards Leshem 1985 0.264
Pandion haliaetus Drop conches on Leshem 1985 0.810
concrete- lled drums
Corvida Corvus albicollis Drop tortoises Uys 1966 1.780
Corvus brachyrhynchos Drop nuts on freeway Grobecker & Pietsch 1978; 2.121
Maple 1974; Cristol et al. 1997
Corvus caurinus Drop shells Zach 1978, 1979 1.694*
Corvus corax Drop bones Lorenz, in van Lawick 1.973
Goodall 1970
Corvus corone Drop shells on roads, Conder & Everett 1979 1.530
place nuts at traf c lights Nihei 1995
Corvus frugilegus Drop mussels Priestley 1947 1.554
Corvus monedula Drop horse chestnuts Gibson 1992 1.278
Corvus moneduloides Drop nuts Hunt 1996 1.694*
Corvus rhipidurus Drop ‘egg’ on soil Andersson 1989 1.694*
Corvus splendens Drop gerbil Fitzwater 1967 1.694*
Passerida Geospiza dif cilis Push, lever, bill brace Köster & Köster 1983; 0.230*
eggs down on rocks Grant 1986
Hold with wedge or skewer
Piciformes Dendrocopos major Wedge in enlarged hole Sielmann, in Boswall 1977 1.435
Dendrocopos syriacus Crack in wall as Gorman 1998 1.352*
wedge and anvil

Melanerpes lewis Wedge in enlarged hole Law 1929 1.189*
Melanerpes carolinensis Wedge seed in crevice Erlwein 1996 1.189*
Picoides villosus Wedge seed in crevice Erlwein 1996 2.215*
Picoides pubescens Knothole as vice Davis 1995 2.215*
Sphyrapicus varius Wedge seeds in bark Labedz 1980 1.427*
Corvida Cracticus spp Thorns to impale prey Boswall 1977 1.554*
Cracticus torquatus Wedge in forks and Sedgwick 1947 1.554*
crevices; skewer on branch
951
952
Pica pica Wedge nuts in crevice Rolando & Zunino 1992 1.916
Lanius spp Thorns to impale prey Boswall 1977 0.381
Passerida Thryothorus ludovicianus Wedge sun ower seeds Haney 1982 0.187*
between bricks
Sitta carolinensis Knotholes as vice Davis 1995 0.929*
True tools
Piciformes Melanerpes uropygialis Gouges bark chips to Antevs 1948 1.189*
bring honey to young
Psittaciformes Amazona ochrocephala Bell to scoop seed, captive Murphy, in Boswall 1983a 1.900
Cacatua galerita Bottle top to scoop Longthorp, in Boswall 1983a 1.310
water, captive
Psittacus erithacus Pipe to bail water, captive Smith 1971 1.606*
Anodorhynchus hyacinthinus Leaf to steady nutcracking; Bertagnolio 1994 2.913
captive
Scolopacida Numenius tahitiensis Throw stones at eggs Marks & Hall 1992 0.236
Charadriida Haematopus ostralegus Stick to dislodge Olney, in Boswall 1978 ¡0:598
invertebrates; captive
Accipitrida Neophron percnopterus Stones to hammer van Lawick Goodall 1970 0.264
ostrich eggs, smash lizard Iankov 1983
Hamirostra melanosternon Throw stones at eggs; Debus 1991; Pepper- 0.543*
captive Edwards & Nottley 1991
Ciconiida Ciconia ciconia Wring moss in beak to Rekasi 1980 0.287
give chicks water
Leptoptilos crumeniferus Stick to get prey in hole Marshall 1982 1.393
Corvida Colluricincla harmonica Twigs for probing Mitchell, in Boswall 1977 1.554*
Corcorax melanorhamphos Empty shells to hammer Hobbs 1971 1.554*
open closed mussels
Corvus brachyrhynchos Stone to smash acorn Duvall, in Boswall 1978 2.121
Corvus brachyrhynchos Cup to carry water to Beck 1980 2.121
dry mash, captive
Corvus brachyrhynchos Sharpen wood to probe Caffrey 2000 2.121
Corvus caurinus Stick to pry peanut Jewett, in Boswall 1983a 1.694*
from bamboo, captive
Corvus corax Pull shing lines to Holmberg, in Boswall 1977; 1.973
get sh under ice Scott 1974
Corvus corone Pull shing lines to Holmberg, in Boswall 1977; 1.530
get sh under ice Scott 1974
Corvus moneduloides Twigs, leaves as Orenstein 1972; Hunt 1996 1.694*
probes, hooks
Corvus rhipidurus Hammer ‘egg’ with rock Andersson 1989 1.694*
Corvus splendens Leaf to get ants from hole Rajan & Balasubramanian 1989 1.694*
Cyanocitta cristata Tear paper, use as Jones & Kamil 1973 1.621
rake and sponge, captive

Cyanocorax yncas Twig under bark Gayou 1982 1.181
Daphoenositta chrysoptera Use and carry twigs to Green 1972 1.554*
open wood-borer grub
Falcunculus frontatus Twigs for probing Richards, in Boswall 1977 1.554*
Passerida Camarhynchus heliobates Twigs for probing Curio & Kramer 1964 0.230*
Camarhynchus pallidus Wood chips scrapers Greenhood & Norton 1999 0.230*
Camarhynchus pallidus Twig probes and levers Millikan & Bowman 1967 0.230*
Certhidea olivacea Twig probes Hundley 1963 0.230*
953
954
Euphagus cyanocephalus Dunked prey as sponge Koenig 1985 0.230*
to bring nestlings water
Bradornis microrhynchus Grass stem in hole McNaughton, in Boswall 1983b ¡0:045*
to sh for termites
Turdus merula Twig broom to search Priddey 1977 ¡0:110
for food in snow
Parus caeruleus Twig to push nuts Coombes, in Boswall 1977 0.510
Parus gambeli Splinter in crack Gaddis, in Boswall 1983b 0.680*
Parus major Pine needles in crevices Duyck & Duyck 1984 0.626
Parus palustris Sponge up food powder, Clayton & Jollife 1996 0.430
wrap to store; captive
Sitta pusilla Bark scale levers Morse 1968; Pranty 1995 0.929*
Sitta carolinensis Bark lever Mitchell 1993 0.929*

* Data unavailable for this species; value is mean residual for the genus, family or suborder.
Fig. 2. Residual brain size for the species using true tools and the four sub-categories of
borderline tools. The dotted line represents the mean residual for all birds.
N D 39/ is signi cantly different from the mean for the second category
(0.581, SEM D 0.090, N D 86; F1;123 D 8:99, p D 0:003/. The difference in
residual brain size between true and borderline tool users is robust; it remains
signi cant when we restrict the analysis to one case per genus, eliminating
49 reports (p D 0:017/, and when we exclude the 11 cases from captivity
(p D 0:035/, the two line pulling reports (p D 0:005/, or the 64 cases
where a species’ brain size was estimated from the mean of its genus, family,
parvorder or suborder (p D 0:009/.
True tools and telencephalic areas

The difference between true and borderline tool use is also evident in the
taxonomic distribution of reports. Overall, the distributio n of borderline tool
reports is most consistentl y correlated with innovation rate, while neural
structure size is the best correlate of true tool use reports (Tables 2 and 3).
Species number per taxon (an obvious confounding variable of the number of
tool use reports) also remains in most of the nal multiple regression models.
Tables 2 and 3 rst present the individual correlation .r, then p) of each
independant variable with true or borderline tool use, then the p value for
that variable at the end of the multiple regressions. As predicted, size of

the neostriatum and hyperstriatum ventrale is more strongly correlated with
true tool use than is size of the striatopallida l complex and wulst (Table 2).
In the multiple regressions, the neostriatum is the only structure that remains
along with species number. The four telencephalic areas are highly correlated
with each other (r of residual neostriatum size with that of hyperstriatum
ventrale: 0.989; with wulst: 0.798; with striatopallida l complex: 0.962; all
p < 0:001, N D 17/. The one with the highest correlation with true tool use,
the neostriatum , thus accounts for the common variance of the four areas in
the multiple regression, causing all others to drop out. Innovation rate also
drops out of the nal model despite a strong individual correlation with true
tool use before the multiple regression. This is because innovation rate is
correlated with size of the telencephalic areas; its share of the variance in
true tool use reports is accounted for by the stronger effect of neostriatum
size. Note that innovation rate is even more highly correlated with size of
the hyperstriatum ventrale (individual correlation D 0.653; p after multiple
regression D 0.006) than it is with size of the neostriatum (individual
correlation D 0.611; p after multiple regression D ns); if we omit tool
use from the multiple regression and put innovation rate as the dependent
variable, then the hyperstriatum ventrale is the only structure that remains in
the nal model (r 2 D 0:385, F1;14 D 10:39, p D 0:006/.
Identical conclusions apply whether we include all reports or keep only
one per genus (Table 2). Independent contrasts also yield similar results to
regressions on phyletically-uncorrecte d taxa (Table 2), despite an obvious
concentration of cases in Corvida and Passerida (Fig. 3). Juvenile develop-
ment mode is non-signi cant in all analyses here and below, both in the in-
dividual correlations and multiple regression models. Figure 3 illustrates the
taxonomic distributio n of true tool use residuals (regressed against species
number), as well as residual size of the neostriatum (regressed against body
weight) for the 17 parvorders (phyletic tree proportional to DNA hybridiza-
tions distances in Sibley & Ahlquist, 1990).
True tools and whole brains
The results on telencephalic areas are con rmed at the level of the whole
brain for three of the four estimates of true tool use distribution . Relative
brain size is (with species number) the only variable that remains in the
T ABLE 2. Association between true and borderline tool use frequency and
relative size of the four telencephalic areas, species number per taxon and
innovation rate (see text for details)
True tools Borderline tools
individual p p in multiple individual p p in multiple
correlations regression correlations regression
Total frequency/taxon
Neostriatum 0.803 <0.001 0.001 0.598 0.014 ns
HV 0.790 <0.001 ns 0.581 0.018 ns
Pallidal 0.756 0.001 ns 0.536 0.032 ns
Wulst 0.658 0.006 ns 0.455 0.076 ns
Species 0.694 0.003 0.020 0.589 0.016 ns
Innovation 0.728 0.001 ns 0.656 0.006 0.006
r 2 D 0:739, F2;14 D 23:70, p < 0:001 r 2 D 0:389, F1;14 D 10:55, p D 0:006
Without multiple entries/genus

Neostriatum 0.815 <0.001 0.001 0.614 0.011 ns
HV 0.811 <0.001 ns 0.596 0.015 ns
Pallidal 0.794 <0.001 ns 0.522 0.038 ns
Wulst 0.634 0.008 ns 0.585 0.017 ns
Species 0.690 0.003 0.013 0.622 0.010 ns
Innovation 0.730 0.001 ns 0.624 0.010 0.010
r 2 D 0:751, F2;14 D 25:11, p < 0:001 r 2 D 0:346, F1;14 D 8:94, p D 0:010
Independent contrasts
Neostriatum 0.745 0.001 0.002 0.493 0.062 ns
HV 0.729 0.002 ns 0.457 0.087 ns
Pallidal 0.708 0.003 ns 0.418 0.121 ns
Wulst 0.544 0.036 ns 0.324 0.239 ns
Species 0.576 0.025 0.031 0.444 0.097 ns
Innovation 0.526 0.044 ns 0.567 0.027 0.022
r 2 D 0:670, F2;13 D 14:72, p < 0:001 r 2 D 0:322, F1;14 D 6:64, p D 0:022
nal multiple regression model for phyletically-uncorrecte d frequencies, for

the data set that eliminates multiple entries per genus and for one of the
two regressions on independent contrasts. Two versions of the independent
contrasts are needed here, because the contrast produced by CAIC at the
node where suborders Tyranni and Passeri meet is an outlier that skews the
distributio n of true tool use cases, causing it to signi cantly differ from
normality (p < 0:05/. The problem is caused by the very large difference
T ABLE 3. Association between true and borderline tool use frequency and
mean residual brain size, species number per taxon and innovation rate (see
text for details)
True tools Borderline tools
individual p p in multiple individual p p in multiple
correlations regression correlations regression
Total frequency/taxon
Brain size 0.493 0.004 0.034 0.456 0.008 ns
Species 0.597 <0.001 0.002 0.653 <0.001 0.001
Innovation 0.467 0.006 ns 0.510 0.002 0.037
r 2 D 0:413, F2;32 D 12:94, p < 0:001 r 2 D 0:472, F2;30 D 15:30, p < 0:001
Without multiple entries/genus

Brain size 0.516 0.002 0.021 0.454 0.008 ns
Species 0.602 <0.001 0.002 0.650 <0.001 0.001
Innovation 0.466 0.006 ns 0.533 0.001 0.022
r 2 D 0:434, F2;32 D 14:04, p < 0:001 r 2 D 0:483, F2;30 D 15:97, p < 0:001
Independent contrasts
Brain size 0.389 0.028 ns 0.373 0.035 ns
Species 0.415 0.018 ns 0.575 0.001 <0.001
Innovation 0.422 0.016 0.014 0.433 0.013 ns
r 2 D 0:178, F1;31 D 6:73, p D 0:014 r 2 D 0:331, F1;31 D 15:31, p < 0:001
in true tool use cases between Passeri (Passerida plus Corvida, 28 cases)
and Tyranni (no reported cases), given the small genetic distance between
the suborders (Fig. 4). We therefore ran mutiple regressions with the outlier
and without it. When the Tyranni-Passeri node is omitted, brain size is
the only variable (with species number) that remains in the nal model;
note that exclusion of this node does not eliminate the 28 Passeri cases,
but simply contrasts them with other taxa at higher nodes in the phyletic
tree. When the outlier is included, brain size is signi cantly correlated with
true tool use distributio n in individual correlations, but drops out of the
multiple regression because of the higher contributio n of innovation rate.
Innovation rate is correlated with relative brain size (r D 0:499, p D 0:003,
N D 32/, which is why it accounts for the common variance with true tool
use distributio n in the nal step of the regression. Figure 4 illustrates residual
true tool use per taxon (regressed against species number) and residual size
Fig. 3. (A) Phyletic tree of the 17 taxa for which telencephalic areas are available; branch
lengths are proportional to DNA hybridisation distances given in Sibley & Ahlquist (1990).
(B) Residual true tool use reports per taxon. (C) Residual size of the neostriatum.
of the whole brain (regressed against body weight) for the 35 parvorders
(phyletic tree proportional to DNA hybridizations distances in Sibley &
Ahlquist, 1990).
Borderline tools
In ve of the six analyses conducted on borderline tools (Tables 2 and 3),
frequency per taxon is more strongly associated with innovation rate than it is
with size of the whole brain or of speci c telencephalic areas. At the level of
the whole brain, innovation rate is the only variable remaining (with species
number) in the nal multiple regression model on phyletically-uncorrecte d
frequencies and on data that eliminate multiple entries per genus. In the
independent contrasts, the effect of innovation rate falls just short (0.087) of
the 0.05 level of signi cance. Contrary to the case seen above for true tools,
the contrast between Tyranni and Passeri does not yield an extreme value in
this analysis (Fig. 5). At the level of the four telencephalic areas, relative size
of the neostriatum and hyperstriatum ventrale is signi cantly correlated with
borderline tool use per taxon in the individual correlations, but drops out for
two of the three mutiple regressions due to a stronger effect of innovation
rate (illustrated in Fig. 6). Relative size of the neostriatum remains in the
nal model only for independent contrasts (Table 2).
Fig. 4. (A) Phyletic tree of the 35 taxa for which whole brain data are available; branch
lengths are proportional to DNA hybridisation given in Sibley & Ahlquist (1990). (B) Resid-
ual true tool use reports per taxon. (C) Residual brain size.
Discussion
Two conclusions can be drawn from our results. First, tool use in birds is
much more common than is often thought. Contrary to Thomson’s (1964)
statement, we found over 120 cases in 104 species, with 39 cases in the
true tool category. A search through the innovation data base, an often
disregarded, low impact factor section of the literature, allowed us to double
the data set obtained from specialized reviews, yielding taxonomic trends
that were highly correlated with those of the specialised literature. Secondly,
three lines of evidence show that true tool users differ from borderline tool
users in the size of key neural structures: true tool users show a larger average
brain size, as well as a positive relationship between frequency of cases
per taxon and both size of the whole brain and size of the neostriatum. In
contrast, innovation rate is the best predictor of borderline tool use per taxon
in most of our regressions.
Fig. 5. (A) Phyletic tree of the 35 taxa for which whole brain data are available; branch
lengths are proportional to DNA hybridisation given in Sibley & Ahlquist (1990). (B) Resid-
ual borderline tool use reports per taxon. (C) Weighted innovation rate.
Our data con rm the distinction between true and borderline tool use em-
phasized by van Lawick Goodall (1970), Parker & Gibson (1977), Beck
(1980), Boswall (1977, 1978, 1983a, b) and McFarland (1982). Compared
to borderline cases, true tool use probably involves a more sophisticate d in-
tegration of the potential uses of an object (Hansell, 1987), as well as the
intricate movements needed for its manipulation . This integration should be
favoured by larger brain areas involved in tool use control. Our results sup-
port Parker & Gibson’s (1977) and Vauclair’s (1997) suggestions that bor-
derline and true tool use categories represent different degrees of cognitive
ability, perhaps associated with differences in Piagetian sensorimotor stages
(see Parker & Gibson, 1977). Whether a species is capable of using a given
degree may depend on the relative size of its neostriatum , but even species
capable of true tool use may rst try simpler techniques. This is illustrated
by Andersson’s (1989) description of ‘egg’-breaking attempts by a fan-tailed
crow in Kenya. Because the ‘egg’ (a ping-pong ball mistakenly treated as an
egg) could not be broken, the crow used a sequence of increasingly com-
Fig. 6. (A) Phyletic tree of the 17 taxa for which telencephalic areas are available; branch
lengths are proportional to DNA hybridisation distances given in Sibley & Ahlquist (1990).
(B) Residual borderline tool use reports per taxon. (C) Weighted innovation rate.
plex techniques: it rst simply pecked at the shell with its beak, then ew
up with the ‘egg’ and dropped it, then attempted to hammer the shell with
an oversize stone, switching at last to a stone of manageable size to increase
hammering ef ciency. In a similar vein, some individuals and population s
in a normally tool-using species may not utilise tools as a result of local
ecological conditions or lack of learning. Tebbich et al. (2001) report that
woodpecker nches do not use tools in habitats and seasons where gleaning
for insects yields higher payoffs. Tebbich et al. also show that some wild-
caught individual s never use twig tools despite extensive exposure to social
and trial-and-error learning possibilities .
In the fan-tailed crow example, and in several others, the co-existence
of true and borderline techniques in the same species suggests that true
tool use may have evolved from simpler borderline tools, but the data offer
only ambiguous support for this idea. On the positive side, 16 of the 39
true tool use cases occur in taxa where borderline cases are reported in
the same species or genus. This is particularly evident in the seven Corvus
species that use both true tools and dropping, as well as in the genus
Turdus (use of a broom in T. merula, battering on anvils in three other
Turdus spp) and Melanerpes (use of a sponge in M. uropygialis, holding
in a wedge in M. lewis and M. carolinensis). In six species (Numenius
tahitiensis, Neophron percnopterus, Corcorax melanorhamphos, Corvus

brachyrhynchos, C. moneduloides, C. rhipidurus), similar prey are handled
with a proto tool (batter or drop on an anvil) and a true tool (hammer,
probe). On the negative side, true tool use shows no borderline equivalents
in Paridae, Psittaciformes, Charadriidae or Ciconiidae; gulls also have no
true tool alternative to their frequent use of dropping. Overall, the data thus
provide poor evidence that proto tool users are preadapted for the use of true
tools.
As predicted, the two telencephalic areas thought to be avian equivalents
of the mammalian neocortex come out as the strongest predictors of the
taxonomic distributio n in tool use reports (Table 2). This does not mean that
the wulst and striatopallida l complex play no role in tool use, but that the
high correlation between the four telencephalic areas leads to the elimination
of those that contribute less in the multiple regression. Contrary to feeding
innovations (Timmermans et al., 2000; this study), the neostriatum comes out
slightly ahead of the hyperstriatum ventrale and is thus the only remaining
telencephalic predictor in the nal multiple regression models. This result
is not due to the fact that we measured innovation rate on a larger sample
here (6 geographical areas, 1796 innovation reports) than did Timmermans
et al. (1030 reports; only 5 of the 6 geographical areas covered, to the
exclusion of southern Africa). In our sample, the hyperstriatum ventrale is
still the best telencephalic predictor of innovation rate both with and without
phyletic corrections. Caution should be exercised because the data set for
tools is much smaller than the one for innovations . If, however, the difference
between tool use and innovation rate is not due to sample size, this may
mean that the intricate control of movement present in tool use but not in
most feeding innovation s (often simply the ingestion of a new food) could be
most strongly associated with a different telencephalic structure (Fig. 1). The
hyperstriatum ventrale consists of higher order, multimodal processing areas.
The neostriatum features tertiary areas of this type, but also includes primary
projection elds from both somatosensory (nucleus basalis) and visual
(ectostriatum ) pathways, as well as secondary areas that receive input from
these primary termination elds (Rehkamper et al., 1985). The neostriatum
thus has the necessary features for both the cognitive and sensory-motor
aspects of tool use. True tool use in particular requires a subtle coordination
of visual and somatosensory information. Probes, for instance, are held in
the beak and must be moved in very precise ways inside crevices to force out
insects, using both tactile and visual feedback. Ascending visual pathways
to the forebrain terminate in the ectostriatum, located in the core of the
neostriatum, and in the wulst. Sensory representation for the bill is located
in the nucleus basalis prosencephali, included here in the neostriatum . The
nucleus basalis is particularly large in tactile feeders like the Scolopacida
(Boire, 1989). It is striking that a species from this small-brained, non-
innovative parvorder, the bristle-thighe d curlew, has evolved three types of
tool use, stone throwing, egg dropping and food slamming on rocks (Marks
& Hall, 1992). N. tahitiensis has the largest brain in its parvorder. As pointed
out by Marks & Hall (1992), the specialised somatosensory receptors on its
bill may, in an island context where birds are often more opportunisti c than
on continents, favour exibility in the use of this food handling organ.
In Fig. 2, one borderline category, holding food with a wedge or skewer,
is associated with the same range of brain sizes as is true tool use. Wedg-
ing is seen in large-brained woodpeckers (Piciformes), while skewering is
a specialized technique used by two types of Corvida, shrikes (genus La-
nius) and butcherbirds (genus Cracticus). Such concentrations of particular
techniques in particular genera are seen for other types of tools. The genus
Pitta, for example, includes several species that batter prey on anvils, as does
the genus Turdus. Dropping prey on a hard surface is seen in several Larus
and Corvus species (see Cristol & Switzer, 1999 for a detailed discussion of
dropping). Several species of Galapagos nches use twig probes for remov-
ing insects from crevices. Common ancestry is an obvious explanation for
the concentration of particular techniques in particular genera. This concen-
tration could be caused by independent selection for each technique in each
genus or by a general set of cognitive processes present in all tool-using taxa,
which only takes a particular form when exploitatio n of a particular food type
is required. In the latter view, the cognitive basis for hammering with a stone
and poking with a twig is similar, i.e. changing the function of an object and
manipulating it to reach hidden food. Differences between the techniques
would be driven instead by the particular defence mechanisms of the prey
(hiding in a shell vs hiding in acrevice). The two possibilities , independent
selection for each technique vs common cognitive basis shaped by particular
food handling constraints, cannot be distinguishe d for the moment, but are
in any case not mutually exclusive.
Despite the fact that some techniques are prevalent in particular taxa, most
of our evidence suggests that phyletic confounds are not responsible for the
overall trends in the data. In all cases, eliminating multiple entries per genus
yielded identical results to the analyses conducted on the full data set. For
telencephalic areas, the regressions on independent contrasts and phyletically
uncorrected taxa both point to the neostriatum as the best predictor of true
tool use reports. It is only at the level of the whole brain that common
ancestry poses a statistical problem at the node that joins suborders Passeri
and Tyranni (Fig. 4). The contrast produced by CAIC at the Passeriforme
node is so large that it leads to a violation of the normality asssumption of
linear regressions. Eliminating the outlier solves the statistical problem, but
obscures the fact that the two Passeriforme suborders differ sharply in the
number of true tool use cases. Conversely, keeping the outlier accounts for
the Passeri-Tyranni difference, but may cause the results of the regression
to be statistically meaningless. Since both solutions pose problems, we have
included the two versions in our results.
In agreement with Boswall (1977, 1978, 1983a, b), our study suggests
that tool use in birds is more common than is often assumed. Over 120 cases
were found in birds, but this is still much smaller than the 607 cases collected
by Reader & Laland (2002; Reader, 1999) in the order Primates. The
current avian total may underestimate actual frequencies because biologists
do not expect as many cases in birds as they do in primates. Primates
(apes in particular) could still be more frequent tool users than are birds,
however, be it for reasons of cognition, dexterity or dietary specialisation
on embedded foods (Gibson, 1986; Parker, 1996). The important point is
that the association between larger telencephalic structures and tool use in
several groups of birds provides independent support for the joint evolution
of these traits in widely divergent taxa. Comparing primates to humans is
instructive, but raises the possibility of a phyletic confound, since the highest
number of tool use reports occurs in Pan, the genus most closely related to
Homo (Reader & Laland, 2002; van Lawick Goodall, 1970; Whiten et al.,
1999; McGrew, 1992). In their study, Reader & Laland (2002) were careful
to exclude common ancestry through the use of independent contrasts, but
our results on birds further strengthen the case for independent evolution in
two ways: not only are birds as a whole very distantly related to primates,
but in addition, most large-brained, tool using groups of birds are distantly
related to each other. As is evident in Figs. 4 and 6, Passeri, Accipitrida,
Charadriida, Psittaciformes, Coraciiformes and Piciformes, six groups that
show positive residuals, come from widely-divergen t branches of the avian

phyletic tree.
Caution must be exercised in interpreting anecdotal observations (see
the open peer commentary that follows Whiten & Byrne, 1988). In some
cases, detailed work (Hunt, 1996) has con rmed a single chance observation
(Orenstein, 1972). In other cases, however, initial claims have not been
supported. The dropping of nuts (Maple, 1974) and palm fruit (Grobecker
& Pietsch, 1978) on roads by C. brachyrhynchos, for example, has been
validated by experimental work (Cristol & Switzer, 1999), but the suggestion
that vehicles are used as nut-crackers in these cases has not (Cristol et al.,
1997; Shettleworth, 1998; see however Caffrey, 2001 and similar work by
Nihei, 1995 on C. corone). Captivity can also introduce some biases (e.g.
training effects; Powell & Kelly, 1977), althought close proximity between
humans and captive animals may make detection of tool using ability easier
than it is in the eld. Beyond these cautionary remarks, however, it is still
reasonable to assume that complex cognitive processes are often operating
when a vertebrate uses a tool. Parallel ndings on primates (Reader &
Laland, 2002) and widely-divergent groups of birds (this study) suggest
that these cognitive processes may have independently co-evolved with large
brains a number of times, allowing several species to pro t from otherwise
inaccessible food (Parker & Gibson, 1977; Gibson, 1986).
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TOOLS AND BRAINS IN BIRDS

LOUIS LEFEBVRE1) , NEKTARIA NICOLAKAKIS and DENIS BOIRE 2,3,4)

In birds, there is large taxonomic variation in the relative size (regressed

to 1800 cases of new, unusual or rare foraging techniques or food types

Regressions, phylogeny and independent contrasts

residual deviation from log-log regression against body weight

Oenanthe oenanthe Batter caterpillars King 1978 ¡0:045*

Larus paci cus Drop mussels on road Wheeler 1946 ¡0:198*

wedge and anvil

rake and sponge, captive

Sitta carolinensis Bark lever Mitchell 1993 0.929*

True tools and telencephalic areas

that variable at the end of the multiple regressions. As predicted, size of

True tools and whole brains

Without multiple entries/genus

 nal multiple regression model for phyletically-uncorrecte d frequencies, for

Without multiple entries/genus

tahitiensis, Neophron percnopterus, Corcorax melanorhamphos, Corvus

show positive residuals, come from widely-divergen t branches of the avian

Marshall, A.J. (1954). Bower birds. — Clarendon Press, Oxford.

Sedgwick, E.H. (1947). Feeding of butcherbirds. — Emu 47, p. 68-69.

Webster, S. & Lefebvre, L. (2001). Problem-solving and neophobia in a Columbiforme-

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Larus paci cus Drop mussels on road Wheeler 1946 ¡0:198*

nal multiple regression model for phyletically-uncorrecte d frequencies, for