Content uploaded by Yvonne Roelofs
Author content
All content in this area was uploaded by Yvonne Roelofs on Jan 11, 2015
Content may be subject to copyright.
TOOL USE IN BIRDS
An overview of reported cases, ontogeny and underlying cognitive abilities
Yvonne Christina Roelofs
Supervisor: Dr. Cor Dijkstra
yroelofs@gmail.com, s1714376, Behavioural Biology, University of Groningen,
Biological Centre, PO Box 14, 9750 AA Haren, The Netherlands, January 2010
2
ABSTRACT
Tool use (manipulating an external object to achieve a certain goal) has been observed in
different species of birds. Birds display a rich variety of different tool use behaviours; most
aimed at the acquisition of food, others for maintenance, defence or courtship purposes. Tool
using bird species are found in different taxonomic classes, many in the order of
psittaciformes, passerids and corvids. Surprisingly, rooks spontaneously manipulate tools in
captivity, however this species has never been reported using tools in the wild. This may
indicate that tool use is not always advantageous.
Here I give an overview of reported cases and recent research on tool use behaviour. Among
others, researchers are trying to unravel the mechanisms involved in the development and
transmission of this behaviour, as well as the underlying cognitive processes. Tool use
ontogeny involves genetic components, sometimes accompanied by individual learning and/or
social learning.
It is thought that tool use is a form of intelligent behaviour reflected in relative brain size. By
including the latest data on tool use reports in birds, I was able to confirm a relationship
between tool use and relative brain size. Additionally, I found that birds that make or modify
their tools also have a larger relative brain size than birds that do not manufacture their tools.
Therefore, tool use and tool manufacture appear to require advanced intelligence.
Furthermore, a higher mean relative brain size in nest building raptors compared to non-nest
builders may indicate that nest construction requires higher cognition as well.
3
TABLE OF CONTENTS
ABSTRACT 2
TABLE OF CONTENTS 3
INTRODUCTION 4
CHAPTER 1: Tool use behaviour 5-6
1.1 Drumming 5
1.2 Baiting fish 5
1.3 Weapon use 5
1.4 Object preening 6
1.5 Anting 6
CHAPTER 2: Tool related behaviour 7-8
2.1 Prey manipulation 7
2.2 Nest construction 7-8
2.3 Play behaviour 8
CHAPTER 3: Development and transmission of tool use 8-9
CHAPTER 4: Tool selection 9-10
CHAPTER 5: Sequential tool use 10
CHAPTER 6: Tool manufacture ___11
CHAPTER 7: Cognition 11-14
7.1 Testing avian cognition 12-13
7.2 Correlations with brain size? 14
DISCUSSION 15-17
CONCLUSION 17
REFERENCES 18-23
APPENDICES 24-31
Table 1: True tool use 24-25
Table 2: Bait-fishing 26
Table 3: Weapon use 26
Table 4: Object preening 26
Table 5: Anting 27
Table 6: Proto-tool use 28-30
Table 7: Raptor nest building and brain sizes 30-31
4
INTRODUCTION
The use of tools has long been viewed as typically human behaviour. But many animals are
known to use tools too (Beck, 1980). The use of objects has been observed in more than 105
species of birds (Iwaniuk et al., 2009). Although many cases are aimed at the acquisition of food
or water, other functions of tool use have also been observed. Many parrots for example use
moulted feathers or other objects as preening aids. Also the use of ants, millipedes or even
mothballs for preening has been observed in several passerine birds, which could act as a
deterrent against fungi or bacteria (Potter, 1970; Clark, 1990), although a food-preparatory
function has also been suggested (Eisner & Aneshansley, 2008). Even the use of weapons by crows
has been observed (Caffrey, 2001; Balda, 2007). But perhaps one of the most remarkable examples
of tool use and modification is drumming by palm cockatoos. These birds use nuts and
manufacture sticks to produce loud knocking sounds, which is thought to serve territorial and
courtship purposes (Wood, 1984; 1988).
To determine which behaviours can be classified as ‘true’ tool use, a general definition is
crucial. St. Amant & Horton (2008) defined tool use as ‘the exertion of control over a freely
manipulable external object (the tool) with the goal of (1) altering the physical properties of
another object, substance, surface or medium (the target, which may be the tool user or
another organism) via a dynamic mechanical interaction, or (2) mediating the flow of
information between the tool user and the environment or other organisms in the
environment’. Proto-tool or borderline tool use is the use of objects that are part of a
substrate, for example battering on anvils and the use of wedges with which food is held
(Parker & Gibson, 1977; in Lefebvre et al., 2002). We speak of multiple or sequential tool use if more
than one object is used in a sequence; the first to gain or modify a second tool, which is
eventually used on the final goal (Clayton, 2007; Wimpenny et al., 2009). Tool manufacture has
been defined as the fashioning or modification of objects in the environment to improve their
suitability as tools (St. Amant & Horton, 2008).
The species that stands out most among tool-using birds is the New Caledonian crow. These
birds use and manufacture a number of different tools in the wild, as well as in captivity. So
far, all populations studied show high levels of tool use (Kacelnik et al., 2006) and differences in
tool shapes produced by individuals from different populations suggest possible cultural
transmission of this behaviour (Bluff et al., 2007).
Tool use is thought to require higher cognitive abilities (Cnotka et al., 2008) although successful
tool use does not necessarily imply causal understanding (Tebbich & Bshary, 2004). Tool users
could have formed a concept about functionality or have learned to perform procedures based
on superficial associations. Seemingly intelligent behaviour can be achieved by applying
simple rules, thus the behaviour could be explained by more parsimonious explanations
instead of having insight in the situation. Experimental designs could investigate whether or
not tool-using birds really understand the problem and are able to effectively use tools to
solve that problem. Several comparative studies have shown a correlation between brain size
and enhanced cognition (Lefebvre et al., 2004; Sol et al., 2005; Cnotka et al., 2008). And even a link
between brain size and tool use has been found (Lefebvre et al., 2002), suggesting that tool users
possess advanced intelligence.
In this thesis I aim to give a complete overview of tool use in birds. Further, I will try to
confirm if there is a relationship between relative brain size and tool use including the latest
data available and I want to examine if there is a correlation between relative brain size and
tool manufacture. In addition I will discuss how tool using behaviour may spread through a
population and generations. I will also consider a possible relationship between nest building
behaviour and brain size in raptors.
5
CHAPTER 1: Tool use behaviour
Using St. Amant & Horton’s definition of tool use the following behaviours can be classified
as ‘true’ tool use (Table 1).
1.1 Drumming
Palm cockatoos (Probosciger aterrimus) have been observed manipulating and using sticks as
drum-tools. They remove fresh twigs of about 10-12 centimetres in length, adapt them by
removing foliage and use them to knock on trunks. It is thought that the males perform this
ritual to attract females to an appropriate nesting site and possibly to define their territory. The
drumsticks are often shredded and added to the nest after successful courtship. Also nuts can
be used to produce the same sound (Wood, 1984; 1988).
1.2 Baiting fish
Bait-fishing is a foraging tactic during which the bird uses bait, such as fish pellets, pieces of
bread, leaves, twigs, feathers, insects, and even plastic foam, to attract fish (Sazima, 2007). This
behaviour has been observed in several species of birds, including herons (Figure 1), corvids
and raptors (Table 2). Some of these birds are omnivores, so they could have chosen to eat the
bread or insects themselves. But instead they resist the immediate motivation to eat the bait to
gain a bigger, more palatable or more nutritional food item (the fish) while risking to lose the
bait. This suggests that these birds have ‘self control’ and are able to foresee the consequences
of their actions.
Figure 1. Green-backed heron bait-fishing. On the left the heron throws a piece of bread into the water as bait.
On the right the heron has successfully caught a guppy (figure taken from Sazima, 2007).
1.3 Weapon use
There have been some observations of birds using objects as weapons against other
individuals or species, either to obtain prey or to defend themselves or their young. So far, all
of these cases were in the corvid family (Table 3). Fish crows (Corvus ossifragus) and
common ravens (C. corax) dropped dried grass on incubating gulls, apparently in attempts to
displace them from their nests and get hold of their eggs (Montevecchi 1978). Hooded crows (C.
corone cornix), common ravens and Eastern American crows (C. brachyrhynchos
brachyrhynchos) have been reported dropping objects (twigs, rocks and pine cones) on
humans to protect their offspring (Rolando and Zunino 1992, Janes 1976; Caffrey, 2001). Similarly,
gulls are known to protect the colony by defecating on intruders, however, since they do not
use an external object, this behaviour is not considered tool use. One remarkable anecdote is
that of a Steller’s jay (Cyanocitta stelleri) which broke off a stick and lunged it at an
American crow to scare it away from a feeding platform. Nonetheless, the crow managed to
take the stick and used it in turn to drive the jay away (Balda, 2007). The advantage of using a
stick to attack, instead of the beak, could be to increase the distance between the bird itself
and its opponent, thus reducing the chance of getting hurt.
6
1.4 Object preening
Object preening (the use of an unattached, freely manipulable object as a preening aid; Figure
2) seems to be a widespread behaviour among psittacines, although there are few scientific
articles about this behaviour. Even though there are some observations of object preening in
the wild (double-crested cormorant: Meyerriecks, 1972; black oystercatcher: Helbing, 1977) the majority of
these cases have been observed in captive birds (Table 4). There are even so-called ‘preening
toys’ available. Some birds even manipulate the object possibly to make it more suitable as a
preening aid. Object preening may have a function (e.g. to access hard to reach places) and/or
may be caused by stress. Captive parrots which are kept solitary often develop behavioural
problems and object preening may be an example of this. Yet it is much easier to observe
certain behaviours in captivity than in the wild, simply because captive birds are observed
more often. Perhaps wild birds use objects as preening aids equally often as their captive
congeners but these cases remain undocumented. However, if the behaviour has a function, in
the wild allopreening may remove the need for object preening by an individual.
Figure 2. Captive yellow-headed amazon preening with a moulted feather.
1.5 Anting
Anting refers to the rubbing of ants or other organic objects onto the plumage. Several
invertebrates (ants, caterpillars, millipedes, moths, snails) are used, but also the use of plant
parts (flowers and fruits) has been reported (Wee, 2008). A presumed function of anting is
obtaining chemicals (such as formic acid) to remove ectoparasites from the bird’s plumage
(Osborn, 1998). Alternatively, or in addition, this behaviour could function as food preparation
(Eisner & Aneshansley, 2008) since most, but not all, birds consume the ants after anting. Also the
chemicals produced by the invertebrates may soothe skin irritation during moult (Potter, 1970).
Anting is mainly practised by passerines (28 out of 35 species; Table 5).
7
CHAPTER 2: Tool related behaviour
2.1 Prey manipulation
Environmental changes may lead to the development of new foraging techniques. The
frequency of these new behaviours, also known as innovation rate, differs between species
and can be used as a measure to compare cognitive differences (Lefebvre et al., 2004). Here I will
discuss prey manipulative techniques closely related to tool use (proto-tool use; Table 6).
Batter on anvil
Birds may batter prey on a hard surface to make it more suitable for consumption. For
example song thrushes (Turdus philomelos) smash snails’ shells open on rocks (Boswall, 1977).
Red-tailed hawks (Buteo jamaicensis) slam snakes against rocks to kill them (Ellis & Brunson,
1993). And tawny frogmouths (Podargus strigoides) sometimes eat small birds which they
first batter against branches to remove the feathers (Lefebvre et al., 2002). Battering behaviour
does not classify as ‘true’ tool use because the target (prey) is directly being manipulated
whereas the substrate (anvil) remains unchanged.
Prey dropping behaviour
Many species of birds (e.g. corvids, gulls and raptors) open hard-shelled prey such as eggs,
molluscs and nuts by dropping them repeatedly onto the ground from considerable heights
(Cristol & Switzer, 1999). Also pushing and rolling eggs against rocks has been observed in the
sharp-beaked ground-finch (Geospiza difficilis) probably because this species is not big and
strong enough to lift the large booby eggs from the ground (Lefebvre et al., 2002). Like battering,
prey dropping is not considered as tool use because there is no separate object between the
target and the user.
Wedge or skewer
Another technique for making food-items more easily to consume is to hold them with a
wedge or skewer. Wedging is defined as the placing of an item in the fork of a substrate, for
example the placing of nuts in crevices by magpies. Skewering is the impaling of prey on a
sharp substrate such as barbed wire or thorns. Shrikes (Laniidae spp.) are known to impale
their prey, a behaviour possibly originating from wedging. Skewering behaviour may be an
adaptation to the lack of strong claws (Yosef & Pinshow, 2005).
2.2 Nest construction
By St. Amant & Horton’s definition nest-building is not true tool use. However, Hansell &
Ruxton (2008) argue that nest construction should not be overlooked because bird nests can
show much complexity and flexibility. There is much variation in nest complexity; compare
for example the nest of a weaverbird with that of a kestrel. Part of this variation may be
explained by environmental differences which may require certain adaptations which in turn
may stimulate the evolution of higher cognitive abilities in certain species. Therefore nest
complexity and brain size may be causally linked.
When high cognitive requirements are involved, it is often necessary to learn the behaviour to
be able to perform the task in a proper way. In some species there seems to be a learning
component to nest construction. This certainly seems to be true for weaver birds (Ploceus
spp.) (Collias & Collias, 1964). Similarly, there are indications that juvenile male bowerbirds
(Ptilonorhynchus spp.) learn bower construction by observing adult males and practise
building their own (Hansell & Ruxton, 2008). Male bowerbirds use bark wads to paint their bower
(Chaffer, 1945) and use several other decorations, such as berries (Madden, 2003); colourful
feathers and leaves (Borgia, 1985), to attract females to their bower.
8
Raptors show much variation in nest complexity, therefore this taxa is suitable for comparing
nest construction behaviour between species and evaluate a possible link with brain volume.
To my knowledge, no other studies have yet examined a correlation between brain size and
nest building. Table 7 shows relative brain sizes and nest building behaviour for 70 species.
Species are listed as nest builders when they actively transport nesting material to the nesting
site. Relative brain size was calculated as the unstandardized residuals of a linear regression
analysis with body mass as the independent and brain volume as the dependent factor. On
average nest builders have a larger residual brain size (0.300 ±2.303 SEM, n=26) than non-
nest builders (-1.236 ±0.787 SEM, n=11) and these means differ significantly from each other
(Independent T-test: p=0.001, n=37). Only genera with data of at least 5 species were
included in this analysis, to minimize the effect of outliers. It is noteworthy that all falcons
(Falco spp.) are non-nest builders since they only make a shallow scrape or use abandoned
nests from other birds. This in contrast with eagles (Aquila spp.) that build large nests using
various materials.
2.3 Play behaviour
Many young animals play. Play has been interpreted as behaviour with limited immediate
function; an activity that is different from the nonplay version of that activity (in terms of
form, sequence or the stage of life in which it occurs), is something the animal engages in
voluntarily and repeatedly, and occurs in a setting in which the animal is adequately fed,
healthy and free from stress (Burghardt, 2005).
In mammals there seems to be a correlation between brain size and play behaviour (Iwaniuk et
al., 2001). Also among birds play is most prevalent in species that have large brains, such as
corvids and parrots (Diamond & Bond, 2003). Especially corvids seem to have a rich set of play
behaviours, such as flight play, object play, vocal play, hanging upside down from branches,
sliding down inclines and rolling through the snow (Ficken, 1977; Brazil, 2002).
Playing seems to have an important function in learning. For example many seabirds and
raptors practise hunting and manipulating prey with inanimate objects such as twigs, sticks,
and bits of moss (Sazima, 2008). Also juveniles from food-caching species have been observed
caching non-food items (Ficken, 1977). Manipulating objects without reaching a certain goal
(i.e. play) may well be the precursor of tool use in animals.
CHAPTER 3: Development and transmission of tool use
There are three components that could play a part in the development and transmission of tool
use: (1) inherited traits, (2) individual learning (e.g. ‘trial and error’) and (3) social learning.
Experiments on hand-reared juveniles could shed some light on the ontogeny of tool use.
Tebbich et al. (2001) showed that young, naive woodpecker finches (Cactospiza pallida) can
learn to use tools even without a tutor. This shows that social learning is not essential for the
development of tool use in this species. Also Egyptian vultures (Neophron percnopterus) are
able to learn stone throwing in isolation (Thouless et al., 1989). But experiments on hand-reared
juvenile New Caledonian crows (Corvus moneduloides) did show an effect of social learning.
Birds that had received demonstrations of tool use by a human tutor showed more handling
and twig insertion than un-tutored birds, although these untutored birds also spontaneously
used and manufactured tools (Kenward et al., 2005). In Northern blue jays (Cyanocitta cristata)
there also seems to be a role for social learning (Jones & Kamil, 1973). Even the large cactus
ground finch (Geospiza conirostris), a non-tool using species, was able to learn twig-probing
from tool-using woodpecker finches. Other species of finches however were not able to learn
tool use in the same experimental set-up (Millikan & Bowman, 1967). This suggests that there
9
should be a genetic disposition for tool use. Furthermore it shows that social learning is not
limited within species but can also occur between individuals of different species.
Not all woodpecker finches use tools. In dry habitats prey is harder to reach and the use of
tools is therefore theoretically more advantageous than in humid habitats. Consequently tool
use occurs mainly in the dry zone and seldom in humid areas (Tebbich et al., 2001). Do these
non-tool using individuals differ genetically from their tool-using conspecifics or were they
deprived from tool-learning during a sensitive phase in their development? The results from
Tebbich et al. (2001) suggest the latter, since they used two complete families in their
experiment: the four parents were non-tool users, however all of their young (n=4) developed
tool use behaviour.
In the New Caledonian crow tool use is present in all populations. Interestingly there is
geographic diversity in tool shape among these populations, although their habitats do not
differ, which suggests that tool manufacturing is transmitted culturally (Hunt & Gray, 2003;
Kacelnik et al., 2006).
CHAPTER 4: Tool selection
Choice of the correct tools in novel situations may indicate causal understanding of tool
dimensions and task demands. If tool use is based on rigid rules, one would expect that
animals will continue their default behaviour or choose at random in novel tasks. Therefore
experiments have been developed to test for tool selectivity; defined as the use of tools
conditional in size or shape on the task being faced (Bluff et al., 2007).
Tool length
When food was placed further away woodpecker finches did not choose longer tools.
However, 3 out of 5 birds did learn to choose a longer tool when the food remained out of
reach of the shorter tools (Tebbich & Bshary, 2004). In contrast, New Caledonian crows did
choose tools of the correct length on their first trials more often than expected by chance,
suggesting that they were able to accurately assess the distance to the food and select the
appropriate tool length necessary to reach it (Chappell & Kacelnik, 2002). In another experiment
New Caledonian crows also chose longer tools when the food was placed further away, but
the chosen tools were often still too short to successfully solve the task. They also showed a
tendency to exchange short sticks for longer tools if the first attempt failed to retrieve the
food, suggesting that they were aware of the limited reach of their first chosen tool (Wimpenny
et al., 2009). The same results were found by Hunt et al. (2006); where crows initially seemed
to use a tool with a default length but changed the length if the first attempt was unsuccessful.
Tool diameter
A New Caledonian crow showed a clear preference for the thinnest tool, which fits in every
hole. Even when the thin tool was tied in a bundle while other tools were freely available
which were also suitable for the task, the crow still chose to obtain the thinnest rod (Chappell &
Kacelnik, 2004). Choosing a smaller tool than necessary for the given task does not mean that
the crows were unable to accurately assess the required tool diameter, because the smaller
tools are successful too. In the wild birds have been observed taking the same tool with them
during foraging (Hunt, 1996). It may be a good strategy to always pick the “safe option” which
is to choose the thinnest tool which can be used to probe in many different sized holes. In
natural conditions there is no extra cost in choosing a thinner tool, however in this experiment
there was the cost of dismantling the bundle. In a follow-up experiment the crows were able
to make their own tools. Now the subjects did take the diameter of the holes into account;
manufacturing wider tools when hole diameter increased. Thin tools bend and break more
10
easily than wider tools especially in a pushing task, however in the wild these birds do not use
tools for pushing, only for pulling food towards themselves (Chappell & Kacelnik, 2004).
In a recent experiment rooks (Corvus frugilegus) had to use stones to raise the water level
causing a floating worm to get into reach (Bird & Emery, 2009b). Soon these birds learned to
select the larger stones, which made the water level rise quicker and consequently less actions
were needed to obtain the reward.
CHAPTER 5: Sequential tool use
The term sequential tool use refers to the use of one tool to retrieve another object to be used
as a tool. Rooks (Bird & Emery, 2009b) and New Caledonian crows (Tayler et al., 2007; Wimpenny et
al., 2009) have been reported as sequential tool users in experimental settings.
The rooks were provided with a large stone, which could be used as a tool to reach another
large stone or a smaller stone. Only the small stone could be used to access out of reach food.
The birds were highly successful at their first trials, rarely trying to access the food with the
initial large stone and choosing to obtain the small stone significantly more often than the
other large stone (Bird & Emery, 2009b). The experimental set up for the New Caledonian crows
consisted of one transparent ‘food-tube’ and four transparent ‘tool-tubes’ while a short tool
was available. The short tool was not long enough to retrieve the food reward, but was able to
extract one of the longer tools. All subjects showed spontaneous sequential tool use on their
first trials (Wimpenny et al., 2009).
It has been suggested that sequential tool use may easily be learned by animals through
‘chaining’: adding previously learned behaviours together in a sequence. Therefore subjects
with different training experience were tested. Interestingly, one of the untrained birds did
manage to retrieve food through sequential tool use, demonstrating that chaining not always
explains this behaviour (Wimpenny et al., 2009).
Figure 3. New Caledonian crow (Betty) retrieving a bucket using a hook tool during an experiment
(Picture provided by Prof. A. Kacelnik, Oxford University).
11
CHAPTER 6: Tool manufacture
Tool manufacture has been defined as the fashioning or modification of objects in the
environment to improve their suitability as tools (St. Amant & Horton, 2008). Tool manufacture
has been shown in only few of the tool-using species (see Table 1) and is thought to require
sophisticated cognitive skills.
In the wild New Caledonian crows are known to use and manufacture different kind of tools:
straight or hooked stick-tools made from twigs or vines are used to probe for insects hiding in
holes and stepped-cut Pandanus leaves to extract small prey hiding under tree bark or crevices
(Kacelnik et al., 2006; Emery, 2006). Regional variation in the shape of these tools may be the
result of cultural transmission, since there are no clear ecological differences between the
populations (Hunt & Grey, 2003).
In an experiment two captive crows were provided with a fresh oak branch. The birds had
prior experience with tool use, but had not been observed manufacturing new tools. Still both
crows managed to spontaneously make useful stick-tools from the right length and diameter to
extract food out of holes (Chappell & Kacelnik, 2004).
A captive New Caledonian crow named Betty was able to bend a piece of straight wire into a
hook to extract a bucket from a vertical tube (Weir et al. 2002; see figure 3). Since the bird had
no prior experience with bending of wire-like material (only with pre-made hooks) the authors
proposed this as an exceptional novel skill for a specific task. In the wild these birds are
known to bend twigs into a hook (Hunt 1996), however Betty used a different method on
unfamiliar material which would have been unlikely to be effective when using natural
materials.
In another experiment woodpecker finches were confronted with H-shaped tools unsuitable
for insertion. To solve the task the birds had to remove one of the transverse pieces and use
the modified tool for the retrieval of food. Here the birds seemed to be unable to assess the
task the first time, but tried to insert the unmodified tool. They were, however, able to adapt
their behaviour when the first attempt failed (Tebbich & Bshary, 2004).
In a similar task, hand-raised rooks were provided with sticks that had 1 to 4 side branches
which had to be removed. The success rate at the first trial was remarkably high (97,5%). The
same subjects spontaneously manufactured hooks from straight wire to extract a bucket from
a vertical tube (Bird & Emery, 2009a).
CHAPTER 7: Cognition
Tool use may require higher cognitive abilities (Cnotka et al., 2008) yet animals can also show
seemingly intelligent behaviour by applying simple rules. For example spiders make and
modify their web depending on environmental conditions, although it seems unlikely to
classify these animals as ones possessing high cognition (Hansell & Ruxton, 2008). The example
of bait-fishing by crows, however, suggests that these birds are capable of self-control and
planning. The crow does not immediately eat the bread, but instead transports it to water to be
used as bait. Therefore some tool use by animals may indicate that the subject is capable of
short- or long-term planning. An example of short-term planning could be the transportation
of a suitable tool to the site of usage. Long-term planning could be the keeping of tools for
future use or food-caching. Planning requires some insight in the situation. Insight is the
sudden production of new adaptive responses, not the result of trial-and-error learning, or the
solution of a problem by the sudden adaptive reorganization of experience. The animal must
form a mental representation of the goal to understand what kind of tool and which actions are
required to reach this goal (Emery & Clayton, 2009a).
12
7.1 Testing avian cognition
The trap-tube test (Visalberghi & Limongelli, 1994) is the most applied test for causal
understanding in a variety of animals. In the traditional setting it consists of a transparent
horizontal tube with a trap in the middle and food placed next to the trap (Figure 4). The
subject has to insert a stick into the correct side of the tube to push the food out without
causing it to fall into the trap. The control configuration has the trap oriented upwards; if the
subject understands gravity it should show no bias to either side of the tube when the tube is
in this inactive state. Several modifications on this design have been made to make the test
more suitable for non-tool using species and to rule out the use of simple cues for solving the
task (Figure 5). Only one out of six woodpecker finches was able to solve the trap-tube test,
probably by trial and error learning (Tebbich & Bshary, 2004). Rooks also seemed to learn the
task by trial and error, although follow-up experiments showed that causal understanding may
have been involved too (Seed et al., 2006).
Figure 4. Traditional design of the trap-tube test (figure taken from Seed et al., 2006).
Figure 5. A modified trap-tube for non-tool using rooks. Instead of inserting a tool, the bird simply needs to pull
at the stick to make the reward fall out of the open trap. Pulling the other way will cause the reward to fall into
the active trap and therefore stay inaccessible to the bird (taken from Chappell, 2006).
13
Another test to examine insight in animals is the string-pulling task. In this task food is
attached at the end of a string (either in a small container or directly connected to the string)
and the goal is to pull the food into reach (Figure 6). When testing birds the reward is usually
attached to a vertical string instead of a horizontal one, whereas the latter is often used to test
mammals. For a correct execution of this task the animal needs to perform at least five
different steps (reach down, grab, pull up, hold with foot, release with beak; see Figure 7)
repeated in the same sequence several times to reach the food (Heinrich & Bugnyar, 2005). If an
individual is able to solve this task, it is thought to have some insight or understanding of the
properties of the string. Yet it has been argued that animals could learn to complete this task
through reinforcement or simply acting on instinct. Therefore this test also has several
modifications, such as presenting several strings (some with a reward, others with a stone
attached), crossing the strings (eliminating the effect of direct physical relations), or changing
the design to a pull-down task (here the reward is placed outside of the cage, only accessible
through the wire mesh if the bird pulls down the piece of string in the cage). Bird species of
which at least one individual was successful at the string-pulling task include ravens (Heinrich
& Bugnyar, 2005), keas (Werdenich & Huber, 2006), grey parrots (Pepperberg, 2004), goldfinches and
siskins (Seibt & Wickler, 2006), budgerigars, Indian starlings and jackdaws (Dücker & Rensch,
1977).
Figure 6. String-pulling task (figure taken from Seibt & Wickler, 2006).
Figure 7. Two string-pulling methods performed by common crows (figure taken from Heinrich, 1995).
The top panel shows lateral step behaviour, where the bird reaches down and pulls up the string and steps to the
side holding the string in place while reaching down for the next pull. The bottom panel shows the straight pull-
up technique, where the bird reaches down and brings up successive loops of string, then holds down these loops
with its foot before reaching again.
14
7.2 Correlations with brain size?
Species shown to be capable of ‘true tool use’ have larger brains than ‘proto-tool users’
(Lefebvre et al., 2002). This may be due to the higher cognitive abilities necessary for the
planning of actions.
The avian brain is very different from the brains of mammals. Birds have to stay light to be
able to fly, therefore there is a constraint on brain size. There are, however, possible
adaptations, such as increasing the numbers of neurons in certain brain areas. But the exact
functions of avian brain structures and the underlying neurochemistry and motor connectivity
are still poorly understood (Emery & Clayton, 2009). Consequently it is difficult to choose the
correct brain structures associated with tool use, therefore I decided to compare total relative
brain size of true tool and proto-tool users. Relative brain size values were taken from
Lefebvre et al. (2002), who used data from 737 species to obtain the residuals of a log brain
size against log body weight regression. Six new cases of true tool use and two new cases of
proto-tool use were added to the table published by Lefebvre et al. (2002) and I chose to
include bait-fishing in the true tool use category (following the new definition for tool use by
St. Amant & Horton, 2008). Mean relative brain size of true tool users (0.8939 ±0.118 SEM,
n=45) is larger than that of proto-tool users (0.4332 ±0.101 SEM, n=61) and these mean
values differ significantly (Mann-Whitney U test: Z= -2.867, p=0.004, n=106). Within the
true tool users group some species are known to modify the tool before using it (tool
manufacturers) whereas others do not change their tools. This is the first study exploring a
correlation between tool manufacture and relative brain size. When comparing mean relative
brain size of tool manufacturers (1.6160 ±0.267 SEM, n=8) and non-manufacturers (0.7378
±0.124 SEM, n=37) I found a significant difference (Mann-Whitney U test: Z= -2.553,
p=0.009, n=45). These results may indicate that tool use and manufacture require advanced
intelligence. However, since we cannot manipulate brain size, we have no choice but to look
at correlations, but we should keep in mind that we can not be sure about causation.
15
DISCUSSION
Tool use behaviour
Drumming, baiting fish, weapon use, object preening and anting are all examples of
behaviours that qualify as true tool use according to the definition by St. Amant & Horton
(2008). Drumming occurs only in palm cockatoos, where it seems to function as a courtship
and/or territorial ritual. Bait-fishing is an example of a remarkable feeding technique where
the bird uses an item to attract and catch fish. Interestingly, weapon use has so far only been
observed in corvids and the number of reports is low. Object preening is most prevalent in
captive parrots, whereas anting occurs mainly in passerines. Anting could be viewed as a form
of object preening, but presumably the chemicals obtained from invertebrates or plant parts
during anting is an important distinctive aspect compared to other forms of object preening.
The exact function of anting and object preening remains unclear, as well as why anting
behaviour seems to be mostly practised by passerines.
Tool related behaviour
Birds have been found to be very inventive when it comes to feeding innovations. Several
kinds of prey manipulation techniques, such as prey dropping or battering behaviour, are
performed by different species. Even when these examples can not be classified as true tool
use, they are no doubt remarkable. Also, some of these techniques may have been precursors
for tool use. For example battering a prey item on a rock is possibly preceding the act of
battering a rock (tool) on prey.
Nest construction is generally not viewed as tool use, although different objects are used to
build a long-lasting structure functioning as a safe place to incubate eggs, raise young, or
sleep. Does nest building require advanced cognition? I compared relative brain sizes of
raptors and found that non-nest builders on average have smaller brains than nest building
species. However, when comparing brain sizes and nest building behaviour we should keep in
mind that birds that do not build a nest may simply have no need for a nest. And birds with
larger brains may need these big brains for other purposes not related to nest building. This is
a problem in all comparative studies. Still it would be worthwhile to examine a possible link
between nest construction and brain size in other species.
Play behaviour is more prevalent in highly intelligent bird species, such as crows (Diamond &
Bond, 2003). Play probably has a function in learning the physical properties of the individual
itself and its environment, and practising certain behaviours for adulthood.
Development and transmission of tool use
Tool use may have evolved in species due to certain ecological conditions. Non-tool using
species may be as intelligent, or maybe even more intelligent, than tool-using species, if their
environment poses no need for the use of tools. Unsuccessful performances on tasks testing
animal cognition do not automatically prove an incompetence of these animals, but may be
due to motivational, inhibitory or perceptual factors. Also experiments on tool use and
cognitive abilities have shown substantial individual differences between subjects of the same
species. These may be caused by a different genetic disposition or experience. Perhaps bird
personalities can also explain some of these differences. Shy birds (slow explorers) may have
a divergent chance to invent a new method through trial and error than bold birds (fast
explorers), whereas the latter have been found to be more likely to acquire novel methods
through social learning (Marchetti & Drent, 2000).
Some non-tool using species can learn to use tools (rooks; large cactus ground finches). This
suggests social learning may be important in the development of tool use behaviour.
However, hand-raised naive New Caledonian crows, woodpecker finches and Egyptian
16
vultures spontaneously started using tools, which shows that there is no social learning
required in these species. However, in New Caledonian crows there seems to be an effect of
social learning on the frequency of tool use. Social learning may aid the transmission of tool
use behaviour, but is not essential for the development in all tool using species. In the case of
the New Caledonian crow this conclusion is further strengthened by the observation of
cultural differences in tool shape. The lack of environmental differences between populations
using different tool shapes provides a strong clue for social learning. If social learning has
been important in the development of tool use among different bird species, maybe they
learned how to use tools by imitating other tool-users, possibly even humans.
The spontaneous handling and sometimes manufacturing of tools by naive juveniles may
indicate that there is a genetic disposition for tool use. This idea is supported by the finding
that some non-tool using bird species have not been successful in learning to use tools in
captivity. It has been suggested that there is a sensitive phase for tool use during ontogeny; if
the behaviour is not sufficiently reinforced during this sensitive phase an individual will never
be able to learn how to use tools (Tebbich et al., 2001). However this could well differ between
species.
Probably all three components (inherited traits, individual and social learning) play a part in
the development and transmission of tool use. It would be interesting to examine the effect of
personalities on the development of tool use by social and individual learning in future
research. More knowledge about the time and length of the sensitive phase for tool use in
different species would also be interesting.
Tool selection and tool manufacture
Both the selection and manufacturing of tools raises the following questions: Are the birds
able to assess the required tool size at the first trial? And are the birds able to adapt their
behaviour when the first trials are ineffective? Rooks seem to be able to make a correct
assessment of the required tool at the first trial, whereas New Caledonian crows were
successful in some experiments, but failed in others. Adapting after failure has been shown in
both woodpecker finches and New Caledonian crows. These results may point towards the
use of a ‘two-stage heuristic strategy’, meaning that the birds initially adopt a default
behaviour which they can modify appropriately if the first attempt fails (Hunt et al., 2006).
Perhaps some corvids are capable of immediate inference, as the performances of rooks and
some New Caledonian crows imply. Differences in experimental arrangements could explain
the different outcomes, however individual diversity may be involved too.
Cognition and insight
Sequential tool use implies planning, the animal must anticipate the multiple actions required
to reach a single goal. But also other forms of tool use may involve planning. Especially bait-
fishing is an example which indicates that these birds can plan ahead. The lack of a direct
physical link between the tool (in this case bait) and the goal (food) may infer insight. Insight
is difficult to test in animals, because we can never be sure about the underlying cognitive
mechanisms involved. Yet experimental tests are developed in such a way that subjects using
simple procedural rules will behave differently than those that apply causal understanding.
The probability of solving the task by chance alone should also be minimized. Testing
animals in many different set-ups will raise the credibility of the conclusions.
17
Correlations with brain size
Comparative studies have shown a correlation between brain size and advanced cognitive
abilities (Lefebvre et al., 2002; 2004; Sol et al., 2005, Cnotka et al., 2008) and my results support this
finding. True tool users have larger relative brain sizes than proto-tool users. Furthermore,
birds that manufacture their own tools have bigger relative brain sizes than non-tool
manufacturers. Large brains are generally associated with higher intelligence. Evolution may
have favoured the most inventive individuals, leading to a gradual increase of brain mass in
those species.
CONCLUSION
The performances of rooks, a species that has not been observed using tools in the wild but is
able to spontaneously develop tool use in captivity, show that these birds are very inventive
and skilled in manipulating objects. The lack of tool use observations in the wild may indicate
that tool use poses no advantages for this species, however it may have been advantageous in
the past or in ancestors. Alternatively, rooks may also use tools in the wild but were never
reported doing so. It seems that, to be able to use tools, a bird should possess a certain
inherited component and the behaviour should be sufficiently reinforced during ontogeny.
Social learning (i.e. observing and imitating other individuals of the same, or of different
species) may play a role in some species, but appears to be unnecessary in others. Play
behaviour by juveniles seems to be an important method to learn about object properties and
how to manipulate tools.
The selection and manufacture of appropriately sized tools has been observed in some species
of corvids, yet an ‘adapt after failure strategy’ appears to be more widely applied. It is
difficult to assess if an animal is capable of planning or has insight, but it is evident that these
tool using birds have the ability to rapidly solve problems in novel situations. The uncovered
relationship between relative brain size, tool use and tool manufacture suggest that these
behaviours are cognitively more demanding.
18
REFERENCES
Balda, R.P. 2007, "Corvids in Combat: With a Weapon?", The Wilson Journal of Ornithology,
vol. 119, no. 1, pp. 100-102.
Beck, B.B. 1980, Animal tool behavior: the use and manufacture of tools by animals, Garland
STPM Press New York, New York.
Bird, C.D. & Emery, N.J. 2009 a, "Insightful problem solving and creative tool modification
by captive nontool-using rooks", Proceedings of the National Academy of Sciences, vol.
106, no. 25, pp. 10370.
Bird, C.D. & Emery, N.J. 2009 b, "Rooks Use Stones to Raise the Water Level to Reach a
Floating Worm", Current Biology, vol. 19, no. 16, pp. 1410-1414.
Bluff, L.A., Weir, A.A.S., Rutz, C., Wimpenny, J.H. & Kacelnik, A. 2007, "Tool-related
cognition in New Caledonian crows", Comparative cognition and behavior reviews, vol.
2, pp. 1-25.
Borgia, G. 1985, "Bower destruction and sexual competition in the satin bowerbird
(Ptilonorhynchus violaceus)", Behavioral Ecology and Sociobiology, vol. 18, no. 2, pp.
91-100.
Borsari, A. & Ottoni, E.B. 2005, "Preliminary observations of tool use in captive hyacinth
macaws (Anodorhynchus hyacinthinus)", Animal Cognition, vol. 8, no. 1, pp. 48-52.
Boswall, J. 1977, "Tool-using by birds and related behaviour", Avicult Mag, vol. 83, pp. 88-
97, 146-159, 220-228.
Brazil, M. 2002, "Common Raven Corvus corax at play; records from Japan", Ornithological
Science, vol. 1, no. 2, pp. 150-152.
Burghardt, G.M. 2005, The genesis of animal play: Testing the limits, The MIT Press.
Caffrey, C. 2001, "Goal-directed use of objects by American crows", The Wilson Bulletin,
vol. 113, no. 1, pp. 114-115.
Chaffer, N. 1945, "The spotted and satin bower-birds: a comparison", Emu, vol. 45, pp. 161-
181.
Chappell, J. 2006, "Avian cognition: understanding tool use", Current Biology, vol. 16, no. 7,
pp. 244-245.
Chappell, J. & Kacelnik, A. 2004, "Selection of tool diameter by New Caledonian crows
Corvus moneduloides", Animal Cognition, vol. 7, no. 2, pp. 121-127.
Chappell, J. & Kacelnik, A. 2002, "Tool selectivity in a non-primate, the New Caledonian
crow (Corvus moneduloides)", Animal Cognition, vol. 5, no. 2, pp. 71-78.
19
Clark, C.C., Clark, L. & Clark, L. 1990, "”Anting” behavior by common grackles and
European starlings", The Wilson Bulletin, vol. 102, no. 1, pp. 167-169.
Clayton, N. 2007, "Animal Cognition: Crows spontaneously solve a metatool task", Current
Biology, vol. 17, no. 20, pp. 894-895.
Cnotka, J., Güntürkün, O., Rehkämper, G., Gray, R.D. & Hunt, G.R. 2008, "Extraordinary
large brains in tool-using New Caledonian crows (Corvus moneduloides)", Neuroscience
letters, vol. 433, pp. 241-245.
Collias, E.C. & Collias, N.E. 1964, "The development of nest-building behavior in a
weaverbird", The Auk, vol. 81, no. 1, pp. 42-52.
Cristol, D.A. & Switzer, P.V. 1999, "Avian prey-dropping behavior. II. American crows and
walnuts", Behavioral Ecology, vol. 10, no. 3, pp. 220.
Diamond, J. & Bond, A.B. 2003, "A comparative analysis of social play in birds", Behaviour,
vol. 140, no. 8, pp. 1091-1115.
Dubois, C.A. 1969, "Grackle anting with a mothball", The Auk, vol. 86, pp. 131.
Dücker, G. & Rensch, B. 1977, "The solution of patterned string problems by birds",
Behaviour, vol. 62, no. 1, pp. 164-173.
Eisner, T. & Aneshansley, D. 2008, "“Anting” in Blue Jays: evidence in support of a food-
preparatory function", Chemoecology, vol. 18, no. 4, pp. 197-203.
Ellis, D.H. & Brunson, S. 1993, "”Tool” use by the red-tailed hawk (Buteo jamaicensis)",
Journal of Raptor Research, vol. 27, no. 2, pp. 128.
Emery, N.J. 2006, "Cognitive ornithology: the evolution of avian intelligence", Philosophical
Transactions B, vol. 361, no. 1465, pp. 23.
Emery, N.J. & Clayton, N.S. 2009, "Tool use and physical cognition in birds and mammals",
Current opinion in neurobiology, vol. 19, no. 1, pp. 27-33.
Ficken, M.S. 1977, "Avian play", The Auk, vol. 94, no. 3, pp. 573-582.
Groff, M.E. & Brackbill, H. 1946, "Purple Grackles 'Anting' with Walnut Juice", The Auk,
vol. 63, no. 2, pp. 246-247.
Hansell, M. & Ruxton, G.D. 2008, "Setting tool use within the context of animal construction
behaviour", Trends in Ecology & Evolution, vol. 23, no. 2, pp. 73-78.
Heinrich, B. & Bugnyar, T. 2005, "Testing problem solving in ravens: string-pulling to reach
food", Ethology, vol. 111, no. 10, pp. 962.
Helbing, G.L. 1977, Maintenance activities of the black oystercatcher, Haematopus bachmani
Audubon, in Northwestern California, Humboldt State University.
20
Hunt, G.R. 1996, "Manufacture and use of hook-tools by New Caledonian crows", Nature,
vol. 379, no. 6562, pp. 249-251.
Hunt, G.R. & Gray, R.D. 2003, "Diversification and cumulative evolution in New Caledonian
crow tool manufacture.", Proceedings of the Royal Society B: Biological Sciences, vol.
270, no. 1517, pp. 867.
Hunt, G.R., Rutledge, R.B. & Gray, R.D. 2006, "The right tool for the job: what strategies do
wild New Caledonian crows use?", Animal Cognition, vol. 9, no. 4, pp. 307-316.
Iwaniuk, A.N., Lefebvre, L. & Wylie, D.R. 2009, "The comparative approach and brain–
behaviour relationships: A tool for understanding tool use.", Canadian Journal of
Experimental Psychology, vol. 63, no. 2, pp. 150-159.
Iwaniuk, A.N., Nelson, J.E. & Pellis, S.M. 2001, "Do big-brained animals play more?
Comparative analyses of play and relative brain size in mammals", Journal of
Comparative Psychology, vol. 115, no. 1, pp. 29-41.
Janes, S.W. 1976, "The apparent use of rocks by a raven in nest defense", The Condor, vol.
78, no. 3, pp. 409-409.
Jones, T.B. & Kamil, A.C. 1973, "Tool-Making and Tool-Using in the Northern Blue Jay",
Science (New York, N.Y.), vol. 180, no. 4090, pp. 1076-1078.
Kacelnik, A., Chappell, J., Weir, A.A.S. & Kenward, B. 2006, "Cognitive adaptations for
tool-related behaviour in New Caledonian crows" in Comparative cognition:
Experimental explorations of animal intelligence, eds. Wasserman E.A. & Zentall T.R.,
Oxford University Press, Oxford, pp. 515-528.
Kenward, B., Weir, A.A.S., Rutz, C. & Kacelnik, A. 2005, "Tool manufacture by naive
juvenile crows", Nature, vol. 433, pp. 121.
King, W.B. & Kepler, C.B. 1970, "Active Anting in the Puerto Rican Tanager", The Auk, vol.
87, pp. 376-378.
Laskey, A.R. 1948, "Bronzed grackle anointing plumage with orange-skin", The Wilson
Bulletin, vol. 60, no. 4, pp. 244-245.
Lefebvre, L., Nicolakakis, N. & Boire, D. 2002, "Tools and brains in birds", Behaviour, vol.
139, no. 7, pp. 939-973.
Lefebvre, L., Reader, S.M. & Sol, D. 2004, "Brains, innovations and evolution in birds and
primates", Brain, Behav Evol, vol. 63, no. 4, pp. 233-246.
Lunt, N., Hulley, P.E. & Craig, A.J.F.K. 2004, "Active anting in captive Cape White-eyes
Zosterops pallidus", Ibis, vol. 146, no. 2, pp. 360-362.
Madden, J.R. 2003, "Bower decorations are good predictors of mating success in the spotted
bowerbird", Behavioral Ecology and Sociobiology, vol. 53, no. 5, pp. 269-277.
21
Marchetti, C. & Drent, P.J. 2000, "Individual differences in the use of social information in
foraging by captive great tits", Animal Behaviour, vol. 60, no. 1, pp. 131-140.
Meyerriecks, A.J. 1972, "Tool-Using by a Double-Crested Cormorant", The Wilson Bulletin, ,
pp. 482-483.
Millikan, G.C. & Bowman, R.I. 1967, "Observations on Galápagos tool-using finches in
captivity", Living Bird, vol. 6, pp. 23-41.
Mlikovsky, J. 1989, "Brain size in birds: 2. Falconiformes through Gaviiformes", Vestnik
Ceskoslovenska Spolecnosti Zoologicka, vol. 53, pp. 200–213.
Montevecchi, W.A. 1978, "Corvids using objects to displace gulls from nests", The Condor,
vol. 80, no. 3, pp. 349-349.
Moreau, R.E. & Moreau, W.M. 1944, "Do young birds play?", Ibis, vol. 86, pp. 93-94.
Osborn, S.A.H. 1998, "Anting by an American dipper (Cinclus mexicanus)", The Wilson
Bulletin, vol. 110, no. 3, pp. 423-425.
Parker, S.T. & Gibson, K.R. 1977, "Object manipulation, tool use and sensorimotor
intelligence as feeding adaptations in cebus monkeys and great apes", Journal of human
evolution, vol. 6, pp. 623-641.
Parkes, K.C., Weldon, P.J. & Hoffman, R.L. 2003, "Polydesmidan millipede used in self-
anointing by a strong-billed woodcreeper (Xiphocolaptes promeropirhyncus) from
Belize", Ornitol.Neotrop, vol. 14, pp. 285-286.
Pepperberg, I.M. 2004, "“Insightful” string-pulling in Grey parrots (Psittacus erithacus) is
affected by vocal competence", Animal Cognition, vol. 7, no. 4, pp. 263-266.
Post, W. & Browne, M.M. 1982, "Active anting by the Yellow-shouldered Blackbird", The
Wilson Bulletin, vol. 94, pp. 89-90.
Potter, E.F. 1970, "Anting in wild birds, its frequency and probable purpose", The Auk, vol.
87, pp. 692-713.
Rolando, A. & Zunino, M. 1992, "Observations of tool use in corvids", Ornis Scandinavica,
vol. 23, no. 2, pp. 201-202.
Sazima, I. 2009, "Anting behaviour with millipedes by the dendrocolaptid bird Xiphocolaptes
albicollis in southeastern Brazil", Biota Neotropica, vol. 9, no. 1, pp. 249-252.
Sazima, I. 2008, "Playful birds: cormorants and herons play with objects and practice their
skills", Biota Neotropica, vol. 8, no. 2, pp. 259-264.
Sazima, I. 2007, "Frustrated fisher: geese and tilapias spoil bait-fishing by the Green Heron
(Butorides striata) in an urban park in Southeastern Brazil", Rev.Bras.Ornitol, vol. 15,
no. 4, pp. 611-614.
22
Schmid, R. 2004, The influence of the breeding method on the behaviour of adult African grey
parrots.
Schneider, L., Serbena, A.L. & Guedes, E.N.M.R. 2006, "Behavioral categories of hyacinth
macaws (Anodorhynchus hyacinthinus) during the reproductive period, at South
Pantanal, Brazil", Revista de Etologia, vol. 8, no. 2, pp. 71-80.
Seed, A.M., Tebbich, S., Emery, N.J. & Clayton, N.S. 2006, "Investigating physical cognition
in rooks, Corvus frugilegus", Current Biology, vol. 16, no. 7, pp. 697-701.
Seibt, U. & Wickler, W. 2006, "Individuality in problem solving: string pulling in two
Carduelis species (Aves: Passeriformes)", Ethology, vol. 112, no. 5, pp. 493-502.
Sol, D., Duncan, R.P., Blackburn, T.M., Cassey, P. & Lefebvre, L. 2005, "Big brains,
enhanced cognition, and response of birds to novel environments", Proceedings of the
National Academy of Sciences, vol. 102, no. 15, pp. 5460.
St. Amant, R. & Horton, T.E. 2008, "Revisiting the definition of animal tool use", Animal
Behaviour, vol. 75, no. 4, pp. 1199-1208.
Taylor, A.H., Hunt, G.R., Holzhaider, J.C. & Gray, R.D. 2007, "Spontaneous metatool use by
New Caledonian crows", Current Biology, vol. 17, no. 17, pp. 1504-1507.
Tebbich, S. & Bshary, R. 2004, "Cognitive abilities related to tool use in the woodpecker
finch, Cactospiza pallida", Animal Behaviour, vol. 67, no. 4, pp. 689-697.
Tebbich, S., Taborsky, M., Fessl, B. & Blomqvist, D. 2001, "Do woodpecker finches acquire
tool-use by social learning?", Proceedings of the Royal Society B: Biological Sciences,
vol. 268, pp. 1482-2189.
Thouless, C.R., Fanshawe, J.H. & Bertram, B.C.R. 1989, "Egyptian Vultures Neophron
percnopterus and Ostrich Struthio camelus eggs: the origins of stone-throwing
behaviour", Ibis, vol. 131, no. 1, pp. 9-15.
VanderWerf, E.A. 2005, "Elepaio “anting” with a garlic snail and a Schinus fruit", Journal of
Field Ornithology, vol. 76, no. 2, pp. 134-137.
Visalberghi, E. & Limongelli, L. 1994, "Lack of comprehension of cause-effect relations in
tool-using capuchin monkeys (Cebus apella)", Journal of Comparative Psychology, vol.
108, pp. 15-15.
Wee, Y.C. 2008, "Anting in Singapore birds", Nature in Singapore, vol. 1, pp. 23-25.
Weir, A.A.S., Chappell, J. & Kacelnik, A. 2002, "Shaping of hooks in New Caledonian
crows", Science, vol. 297, no. 5583, pp. 981.
Wenny, D. 1998, "Three-striped warbler (Basileuterus tristriatus) "anting" with a caterpillar",
The Wilson Bulletin, vol. 110, no. 1, pp. 128-131.
23
Werdenich, D. & Huber, L. 2006, "A case of quick problem solving in birds: string pulling in
keas, Nestor notabilis", Animal Behaviour, vol. 71, no. 4, pp. 855-863.
Whitaker, L.M. 1957, "A resume of anting, with particular reference to a captive Orchard
Oriole", The Wilson Bulletin, vol. 69, no. 3, pp. 194-262.
Wimpenny, J.H., Weir, A.A.S., Clayton, L., Rutz, C. & Kacelnik, A. 2009, "Cognitive
Processes Associated with Sequential Tool Use in New Caledonian Crows", vol. 4, no. 8,
pp. 1-16.
Wood, G.A. 1988, "Further field observations of the palm cockatoo Probosciger aterrimus in
the Cape York Peninsula, Queensland", Corella, vol. 12, pp. 48-52.
Wood, G.A. 1984, "Tool use by the palm cockatoo Probosciger aterrimus during display",
Corella, vol. 8, no. 4, pp. 94-95.
Yosef, R. & Pinshow, B. 2005, "Impaling in true shrikes (Laniidae): A behavioral and
ontogenetic perspective", Behavioural processes, vol. 69, no. 3, pp. 363-367.
24
APPENDICES
Table 1. True tool use
True tool use observations in several bird species sorted by taxa. Brain size is given as
residual deviation from log-log regression against body weight (Lefebvre et al. 2002).
W/C=Wild or Captive; R=References; B=Brain size; M=Tool Manufacture
Taxon
Species
W/C
Technique
R
B
M
Accipitrida
Hamirostra
melanosternon
Captive
Throw stones at eggs
1
0.543*
no
Accipitrida
Neophron
percnopterus
Wild
Stones to hammer
ostrich eggs, smash
lizard
1
0.264
no
Charadriida
Haematopus
ostralegus
Captive
Stick to dislodge
invertebrates
1
-0.598
no
Ciconiida
Ciconia ciconia
Wild
Wring moss in beak to
give chicks water
1
0.287
no
Ciconiida
Leptoptilos
crumeniferus
Wild
Stick to get prey in
hole
1
1.393
no
Corvida
Colluricincla
harmonica
Wild
Twigs for probing
1
1.554*
no
Corvida
Corcorax
melanorhamphos
Wild
Empty shells to
hammer open closed
mussels
1
1.554*
no
Corvida
Corvus
brachyrhynchos
Captive
Cup to carry water to
dry mash
1
2.121
no
Corvida
Corvus
brachyrhynchos
Wild
Stone to smash acorn;
sharpen wood to
probe
1
2.121
yes
Corvida
Corvus caurinus
Captive
Stick to pry peanut
from bamboo
1
1.694*
no
Corvida
Corvus corax
Wild
Pull fishing lines to get
fish under ice
1
1.973
no
Corvida
Corvus corone
Wild
Pull fishing lines to get
fish under ice
1
1.530
no
Corvida
Corvus frugilegus
Captive
raise waterlevel with
stones, hook-bending
2, 3
1.554
yes
Corvida
Corvus
moneduloides
Wild
Twigs, leaves as
probes, hooks
1
1.694*
yes
Corvida
Corvus rhipidurus
Wild
Hammer ‘egg’ with
rock
1
1.694*
no
Corvida
Corvus splendens
Wild
Leaf to get ants from
hole
1
1.694*
no
Corvida
Cyanocitta cristata
Captive
Tear paper, use as
rake and sponge
1
1.621
yes
Corvida
Cyanocorax yncas
Wild
Twig under bark
1
1.181
no
Corvida
Daphoenositta
chrysoptera
Wild
Use and carry twigs to
open wood-borer grub
1
1.554*
no
Corvida
Falcunculus frontatus
Wild
Twigs for probing
1
1.554*
no
25
Table 1 (continued)
Taxon
Species
W/C
Technique
R
B
M
Passerida
Bradornis
microrhynchus
Wild
Grass stem in hole to
fish for termites
1
-0.045*
no
Passerida
Camarhynchus
heliobates
Wild
Twigs for probing
1
0.230*
no
Passerida
Camarhynchus
pallidus
Wild
Wood chips scrapers;
twig probes and levers
1, 4
0.230*
yes
Passerida
Certhidea olivacea
Wild
Twig probes
1
0.230*
no
Passerida
Euphagus
cyanocephalus
Wild
Dunked prey as sponge
to bring nestlings water
1
0.230*
no
Passerida
Geospiza conirostris
Captive
Twigs for probing
4
0.230*
no
Passerida
Parus caeruleus
Wild
Twig to push nuts
1
0.510
no
Passerida
Parus gambeli
Wild
Splinter in crack
1
0.680*
no
Passerida
Parus major
Wild
Pine needles in crevices
1
0.626
no
Passerida
Parus palustris
Captive
Sponge up food powder,
wrap to store
1
0.430
no
Passerida
Sitta carolinensis
Wild
Bark lever
1
0.929*
no
Passerida
Sitta pusilla
Wild
Bark scale levers
1
0.929*
no
Passerida
Turdus merula
Wild
Twig broom to search
for food in snow
1
-0.110
no
Piciformes
Melanerpes
uropygialis
Wild
Gouges bark chips to
bring honey to young
1
1.189*
yes
Psittaciformes
Amazona
ochrocephala
Captive
Bell to scoop seed
1
1.900
no
Psittaciformes
Anodorhynchus
hyacinthinus
Captive
Leaf to steady
nutcracking; pieces of
wood for nutcracking
5
2.913
yes
Psittaciformes
Anodorhynchus
hyacinthinus
Wild
Pieces of wood, leaves
for nutcracking
6
2.913
yes
Psittaciformes
Cacatua galerita
Captive
Bottle top to scoop water
1
1.310
no
Psittaciformes
Nandayus nenday
Captive
Spoon to scoop food
9
1.606*
no
Psittaciformes
Probosciger aterrimus
Wild
Drumtools for display
7, 8
1.606*
yes
Psittaciformes
Psittacus erithacus
Captive
Pipe to bail water
1
1.606*
no
Scolopacida
Numenius tahitiensis
Wild
Throw stones at eggs
1
0.236
no
*Data unavailable for this species; value is mean residual for the genus, family or suborder.
References: 1=Lefebvre et al. 2002; 2=Seed 2006; 3=Bird & Emery 2009; 4=Millikan & Bowman 1967;
5=Borsari & Ottoni 2005; 6=Schneider 2006; 7=Wood 1984; 8=Wood 1988;
9=http://www.youtube.com/watch?v=-RRI9NTzWJA
26
Table 2. Bait-fishing
Species reported baiting fish. Brain size is given as residual deviation from log-log regression
against body weight (Lefebvre et al. 2002)
W/C=Wild or Captive; R=References; B=Brain size; M=Tool Manufacture
Taxon
Species
W/C
Technique
R
B
M
Accipitrida
Milvus migrans
Wild
Bait fish with bread
1
0.33
no
Charadriida
Larus fuscus
Captive
Bait fish with bread
1
0.16
no
Ciconiida
Ardeola ralloides
Wild
Bait fish with insects
1
-0.76
no
Ciconiida
Butorides striatus
Wild
Bait fish with bread, insects,
twigs, feathers
1
-0.31
no
Coraciiformes
Ceryle rudis
Wild
Bait fish with bread
1
0.16
no
Corvida
Corvus corone cornix
Wild
Bait fish with bread
2
1.53
no
Grui
Eurypyga helias
Wild
Bait fish with maggots
3
-0.07
no
*Data unavailable for this species; value is mean residual for the genus, family or suborder.
References: 1=Lefebvre et al. 2002; 2=http://www.orenhasson.com/EN/bait-fishing.htm;
3=Boswall 1977; 4=Cristol & Switzer 1999
Table 3. Weapon use
W/C=Wild or Captive; R=References; M=Tool Manufacture
Taxon
Species
W/C
Technique
R
M
Corvida
Corvus albicollis
Wild
Throw twig at opponent
1
no
Corvida
Corvus brachyrhynchos
Wild
Drop objects
2
no
Corvida
Corvus corax
Wild
Drop objects
3, 4
no
Corvida
Corvus corone cornix
Wild
Drop objects
5
no
Corvida
Corvus ossifragus
Wild
Drop objects on incubating birds
4
no
Corvida
Cyanocitta stelleri
Wild
Use stick as weapon
6
yes
References: 1=Moreau & Moreau 1944; 2=Caffrey 2001; 3=Janes 1976; 4=Montevecchi 1978;
5=Rolando & Zunino 1992; 6=Balda 2007
Table 4. Object preening
W/C=Wild or Captive; R=References; M=Tool Manufacture
Taxon
Species
W/C
Technique
R
M
Charadriida
Haematopus bachmani
Wild
Limpet shell as preening tool
1
no
Psittaciformes
Amazona amazonica
Captive
Objects for preening
2
no
Psittaciformes
Amazona oratrix
Captive
Moulted feather for preening
3
yes
Psittaciformes
Ara nobilis nobilis
Captive
Objects for preening
4
yes
Psittaciformes
Cacatuidae spp
Captive
Moulted feather for preening
2
no
Psittaciformes
Psittacus erithacus
Captive
Twigs for preening
5
yes
Psittaciformes
Pyrrhura molinae
Captive
Moulted feather for preening
6
no
Sulida
Phalacrocorax auritus
Wild
Moulted feather for preening
7
no
References: 1=Helbing 1977; 2=personal communications;
3=http://www.youtube.com/watch?v=bTZqMZuBC1U;
4=http://www.youtube.com/watch?v=tSJ3-46r62w; 5=Schmid, 2004;
6=http://www.youtube.com/watch?v=xuzsNA5ADWk; 7=Meyerriecks 1972
27
Table 5. Anting
Bird species known to perform anting behaviour.
W/C=Wild or Captive; R=References
Taxon
Species
English name
W/C
R
Corvida
Chasiempis sandwichensis
Elepaio
Wild
1
Corvida
Cyanocitta cristata
Blue Jay
Wild
2
Furnariida
Xiphocolaptes albicollis
White-collared Woodcreeper
Wild
3
Furnariida
Xiphocolaptes promeropirhynchus
Strong-billed Woodcreeper
Wild
4
Galliformes
Callipepla squamata
Scaled Quail
Wild
2
Passerida
Acridotheres fuscus
Jungle Myna
Wild
5
Passerida
Acridotheres javanicus
Javan Myna
Wild
5
Passerida
Agelaius phoeniceus
Red-winged Blackbird
Wild
2
Passerida
Agelaius xanthomus
Yellow-shouldered Blackbird
Wild
6
Passerida
Basileuterus tristriatus
Three-striped Warbler
Wild
7
Passerida
Cardinalis cardinalis
Northern Cardinal
Wild
2
Passerida
Cinclus mexicanus
American dipper
Wild
8
Passerida
Dumetella carolinensis
Grey Catbird
Wild
2
Passerida
Hylocichla mustelina
Wood Thrush
Wild
2
Passerida
Icterus spurius
Orchard Oriole
Captive
9
Passerida
Junco hyemalis
Slate-colored Junco
Wild
2
Passerida
Melospiza melodia
Song Sparrow
Wild
2
Passerida
Molothrus ater
Brown-headed Cowbird
Wild
2
Passerida
Nesospingus speculiferus
Puerto Rican Tanager
Wild
10
Passerida
Passer domesticus
House Sparrow
Wild
2
Passerida
Passerina cyanea
Indigo Bunting
Wild
2
Passerida
Pipilo erythrophthalmus
Rufous-sided Towhee
Wild
2
Passerida
Piranga olivacea
Scarlet Tanager
Wild
2
Passerida
Piranga rubra
Summer Tanager
Wild
2
Passerida
Protonotaria citrea
Prothonotary Warbler
Wild
2
Passerida
Quiscalus quiscula
Common Grackle
Wild
11, 12
Passerida
Quiscalus quiscula stonei
Purple Grackle
Wild
13
Passerida
Quiscalus quiscula versicolor
Bronzed Grackle
Wild
14
Passerida
Sturnus vulgaris
European Starling
Wild
2, 12
Passerida
Toxostoma rujum
Brown Thrasher
Wild
2
Passerida
Turdus migratorius
American Robin
Wild
2
Passerida
Vermivora pinus
Blue-winged Warbler
Wild
2
Passerida
Zosterops pallidus
Cape White-eye
Captive
15
Piciformes
Colaptes auratus
Yellow-shafted Flicker
Wild
2
Psittaciformes
Psittinus cyanurus
Blue-rumped Parrot
Wild
5
References: 1=VanderWerf 2005; 2=Potter 1970; 3=Sazima 2009; 4=Parkes et al. 2003
5=Wee 2008; 6=Post & Browne 1982; 7=Wenny 1998; 8=Osborn 1998
9=Whitaker 1957; 10=King & Kepler 1970; 11=Dubois 1969; 12=Clark 1990
13=Groff & Brackbill 1946; 14=Laskey 1948; 15=Lunt 2004
28
Table 6. Proto-tool use
Species of birds demonstrating tool related behaviours. Brain size is given as residual
deviation from log-log regression against body weight (Lefebvre et al. 2002).
W/C=Wild or Captive; R=References
Taxon
Species
W/C
Technique
R
Brain size
Batter on anvil
Accipitrida
Buteo jamaicensis
Wild
Slam snake on rock in
flight
1
0.843
Accipitrida
Gypaetus barbatus
Wild
Batter bones on rocks
1
0.860
Caprimulgi
Podargus strigoides
Wild
Batter feathers off prey
against dead bough
1
0.716
Ciconiida
Threskiornis molucca
Wild
Batter mussels on anvils
1
-0.021
Coraciiformes
Ceryle rudis
Wild
Batter crab on rocks
1
0.161
Coraciiformes
Dacelo novaeguineae
Wild
Batter rat and bone
1
0.790
Coraciiformes
Halcyon smyrnensis
Wild
Batter frog on branch
1
0.193
Corvida
Ailuroedus
dentirostris
Wild
Batter snails on stones
1
1.313*
Corvida
Colluricincla
harmonica
Wild
Batter mouse on stump,
wren and robin on rock
1
1.554*
Corvida
Corcorax
melanorhamphos
Wild
Batter mussels
1
1.554*
Corvida
Corvus
brachyrhynchos
Wild
Batter fish on sand, wipe
on sand (to scale?)
1
2.121
Corvida
Daphoenositta
chrysoptera
Wild
Bash insects on branch
1
1.554*
Corvida
Falcunculus frontatus
Wild
Bash insects on branch
1
1.554*
Corvida
Lanius collaris
Wild
Batter grasshopper on
post then skewer on
thorn
1
0.318
Cuculiformes
Geococcyx
californianus
Wild
Batter reptiles on rocks
1
-0.246
Passerida
Acridotheres fuscus
Wild
Batter mouse
1
0.496*
Passerida
Anthus petrosus
Wild
Batter snails
1
-0.846*
Passerida
Ficedula hypoleuca
Wild
Batter snails
1
-0.045*
Passerida
Myiophonus
caeruleus
Wild
Batter shells on rocks
1
-0.045*
Passerida
Oenanthe leucura
Wild
Batter lizard on stone
1
-0.045*
Passerida
Oenanthe oenanthe
Wild
Batter caterpillars
1
-0.045*
Passerida
Passer domesticus
Wild
Batter wings off
damselflies
1
0.402
Passerida
Ploceus philippinus
Wild
Batter frogs on electrical
wire
1
-0.347*
Passerida
Pycnonotus cafer
Wild
Batter gecko on wall
1
0.455*
Passerida
Saxicola rubetra
Wild
Batter caterpillars
1
-0.234*
Passerida
Saxicola torquata
Wild
Batter snails
1
-0.234*
Passerida
Saxicoloides fulicata
Wild
Batter frog and gecko
1
-0.045*
Passerida
Turdus iliacus
Wild
Batter snails
1
0.364
Passerida
Turdus pelios
Wild
Batter snails on rocks
1
0.379
Passerida
Turdus philomelos
Wild
Batter snails on rocks
2
0.088
Ralli
Eulabeornis
castaneoventris
Wild
Batter shells on anvils
1
-0.577*
Scolopacida
Numenius tahitiensis
Wild
Batter crabs on rocks
1
0.236
Sulida
Anhinga anhinga
Wild
Batter fish on branch
1
-1.342
29
Table 6 (continued)
Taxon
Species
W/C
Technique
R
Brain size
Tyranni
Pitta erythrogaster
Wild
Batter hard-shelled prey
1
0.771*
Tyranni
Pitta guajana
Wild
Batter hard-shelled prey
1
0.771*
Tyranni
Pitta moluccensis
Wild
Batter hard-shelled prey
1
0.771*
Tyranni
Pitta sordida
Wild
Batter hard-shelled prey
1
0.771*
Tyranni
Pitta versicolor
Wild
Batter hard-shelled prey
1
0.771*
Tyranni
Xenicus gilviventris
Wild
Batter grasshopper on
corrugated iron
1
0.771*
Drop on substrate
Accipitrida
Aquila chrysaetos
Wild
Drop tortoises
1
0.164
Accipitrida
Gypaetus barbatus
Wild
Drop bones and tortoise
2
0.860
Accipitrida
Haliaeetus
leucocephalus
Wild
Drop tortoises
1
0.403
Accipitrida
Neophron
percnopterus
Wild
Drop tortoise and lizards
1
0.264
Accipitrida
Pandion haliaetus
Wild
Drop conches on
concrete-filled drums
1
0.810
Charadriida
Catharacta skua
Wild
Drop penguin eggs
2
-0.198*
Charadriida
Larus argentatus
Wild
Drop rabbits on rocks
1
-1.179
Charadriida
Larus canus
Wild
Drop molluscs
3
0.142
Charadriida
Larus delawarensis
Wild
Drop molluscs
3
-0.198*
Charadriida
Larus dominicanus
Wild
Drop egg on water
1
-0.098
Charadriida
Larus glaucescens
Wild
Drop molluscs
3
-0.198*
Charadriida
Larus marinus
Wild
Drop crabs on hard sand;
drop rat
1
-0.287
Charadriida
Larus
melanocephalus
Wild
Drop molluscs
3
-0.198*
Charadriida
Larus occidentalis
Wild
Drop molluscs
3
-0.198*
Charadriida
Larus pacificus
Wild
Drop mussels on road
1
-0.198*
Corvida
Corvus albicollis
Wild
Drop tortoises
1
1.780
Corvida
Corvus
brachyrhynchos
Wild
Drop nuts on freeway
1
2.121
Corvida
Corvus caurinus
Wild
Drop shells
1
1.694*
Corvida
Corvus corax
Wild
Drop bones
1
1.973
Corvida
Corvus corone cornix
Wild
Drop molluscs, nuts,
crustaceans
3
1.530
Corvida
Corvus corone
corone
Wild
Drop shells on roads,
place nuts at traffic lights
1
1.530
Corvida
Corvus frugilegus
Wild
Drop mussels
1
1.554
Corvida
Corvus monedula
Wild
Drop horse chestnuts
1
1.278
Corvida
Corvus moneduloides
Wild
Drop nuts
1
1.694*
Corvida
Corvus rhipidurus
Wild
Drop ‘egg’ on soil
1
1.694*
Corvida
Corvus splendens
Wild
Drop gerbil
1
1.694*
Grui
Cariama cristata
Wild
Drop eggs on stones
1
-0.013*
Passerida
Geospiza difficilis
Wild
Push, lever, bill brace,
eggs down on rocks
1
0.230*
Scolopacida
Numenius tahitiensis
Wild
Drop eggs
1
0.236
Hold wedge or skewer
Corvida
Cracticus spp
Wild
Thorns to impale prey
2
1.554*
30
Table 6 (continued)
Taxon
Species
W/C
Technique
R
Brain size
Corvida
Cracticus torquatus
Wild
Wedge in forks, crevices;
skewer on branch
1
1.554*
Corvida
Lanius spp
Wild
Thorns to impale prey
2
0.381
Corvida
Pica pica
Wild
Wedge nuts in crevice
1
1.916
Passerida
Sitta carolinensis
Wild
Knotholes as vice
1
0.929*
Passerida
Thryothorus
ludovicianus
Wild
Wedge sunflower seeds
between bricks
1
0.187*
Piciformes
Dendrocopos major
Wild
Wedge in enlarged hole
2
1.435
Piciformes
Dendrocopos syriacus
Wild
Crack in wall as wedge
and anvil
1
1.352*
Piciformes
Melanerpes
carolinensis
Wild
Wedge seed in crevice
1
1.189*
Piciformes
Melanerpes lewis
Wild
Wedge in enlarged hole
1
1.189*
Piciformes
Picoides pubescens
Wild
Knothole as vice
1
2.215*
Piciformes
Picoides villosus
Wild
Wedge seed in crevice
1
2.215*
Piciformes
Sphyrapicus varius
Wild
Wedge seeds in bark
1
1.427*
*Data unavailable for this species; value is mean residual for the genus, family or suborder.
References: 1=Lefebvre et al. 2002; 2=Boswall 1977; 3=Cristol & Switzer 1999
Table 7. Raptor nest building and brain sizes
Nest building (NB) ranges from 0-1 (0=no nest building; 1=nest building).
Relative brain mass is calculated as the unstandardized residuals of body size x brain mass
(data used from: Mlikovsky, 1989).
Family
Species
English name
NB
Brain size
Accipitridae
Accipiter brevipes
Levant Sparrowhawk
1
-1.586
Accipitridae
Accipiter gentilis
Goshawk
1
0.723
Accipitridae
Accipiter nisus
Northern Sparrowhawk
1
-1.913
Accipitridae
Accipiter striatus
Sharp-shinned Hawk
1
-0.078
Accipitridae
Accipiter tachiro
African Goshawk
1
-1.208
Accipitridae
Aegypius monachus
European Black Vulture
1
-2.774
Accipitridae
Aquila audax
Wedge-tailed Eagle
1
1.630
Accipitridae
Aquila chrysaetos
Golden Eagle
1
1.054
Accipitridae
Aquila clanga
Greater Spotted Eagle
1
1.476
Accipitridae
Aquila heliaca
Imperial Eagle
1
3.688
Accipitridae
Aquila pomarina
Lesser Spotted Eagle
1
2.600
Accipitridae
Aquila rapax
Tawny Eagle
1
2.053
Accipitridae
Aquila verreauxii
African Black Eagle
1
1.265
Accipitridae
Aquila pennata
Booted Eagle
1
-1.090
Accipitridae
Aviceda leuphotes
Black Baza
1
-1.459
Accipitridae
Butastur liventer
Rufous-winged Buzzard
1
-0.670
Accipitridae
Butastur teesa
White-eyed buzzard
1
-0.770
Accipitridae
Buteo auguralis
Red-necked Buzzard
1
-0.780
Accipitridae
Buteo buteo
Common Buzzard
1
1.123
Accipitridae
Buteo jamaicensis
Red-tailed Hawk
1
2.553
Accipitridae
Buteo lagopus
Rough-legged Buzzard
1
2.023
Accipitridae
Buteo lineatus
Red-shouldered Hawk
1
0.464
Accipitridae
Buteo magnirostris
Roadside Hawk
1
-0.770
31
Table 7 (continued)
Family
Species
English name
NB
Brain size
Accipitridae
Buteo rufinus
Long-legged Buzzard
1
2.693
Accipitridae
Buteo rufofuscus
Jackal Buzzard
1
2.423
Accipitridae
Circaetus cinereus
Brown Snake-Eagle
1
-0.423
Accipitridae
Circus aeruginosus
Marsh Harrier
1
-0.195
Accipitridae
Circus cyaneus
Northern Harrier
1
-0.989
Accipitridae
Gypaetus barbatus
Bearded Vulture
1
3.496
Accipitridae
Gypohierax angolensis
Palm-nut Vulture
1
1.029
Accipitridae
Gyps africanus
African White-backed Vulture
1
-1.987
Accipitridae
Gyps bengalensis
Indian White-backed Vulture
1
0.560
Accipitridae
Gyps coprotheres
Cape Vulture
1
-7.015
Accipitridae
Gyps fulvus
Eurasian Griffon Vulture
1
1.337
Accipitridae
Gyps himalayensis
Himalayan Griffon Vulture
1
-3.426
Accipitridae
Haliaeetus albicilla
White-tailed Eagle
1
1.101
Accipitridae
Haliaeetus leucocephalus
Bald Eagle
1
0.401
Accipitridae
Halieetus vocifer
African Fish Eagle
1
0.241
Accipitridae
Kaupifalco
monogrammicus
Lizard Buzzard
1
-1.518
Accipitridae
Lophaetus occipitalis
Long-crested Eagle
1
0.705
Accipitridae
Melierax canorus
Pale-chanting Goshawk
1
-0.007
Accipitridae
Milvus migrans
Black Kite
1
-0.071
Accipitridae
Milvus milvus
Red Kite
1
0.652
Accipitridae
Neophron percnopterus
Egyptian Vulture
1
0.676
Accipitridae
Nisaetus cirrhatus
Changeable Hawk-eagle
1
-0.594
Accipitridae
Pernis apivorus
Honey Buzzard
1
0.799
Accipitridae
Polyboroides radiatus
Madagascar Harrier-hawk
1
1.434
Accipitridae
Spizaetus ornatus
Ornate Hawk-eagle
1
2.341
Falconidae
Falco biarmicus
Lanner Falcon
0
0.035
Falconidae
Falco columbarius
Merlin
0
-1.886
Falconidae
Falco moluccensis
Spotted Kestrel
0
-1.359
Falconidae
Falco naumanni
Lesser Kestrel
0
-1.891
Falconidae
Falco peregrinus
Peregrine Falcon
0
-0.336
Falconidae
Falco rupicoloides
Greater Kestrel
0
-1.121
Falconidae
Falco rusticolus
Gyr Falcon
0
-0.159
Falconidae
Falco sparverius
American Kestrel
0
-1.942
Falconidae
Falco subbuteo
Eurasian Hobby
0
-1.521
Falconidae
Falco tinnunculus
Common Kestrel
0
-1.113
Falconidae
Falco vespertinus
Red-footed Falcon
0
-2.304
Falconidae
Herpetotheres cachinnans
Laughing Falcon
0
-0.265
Falconidae
Microhierax fringillarius
Black-thighed Falconet
0
-3.258
Falconidae
Milvago chimango
Chimango Caracara
1
-1.018
Falconidae
Phalcoboenus albogularis
White-throated Caracara
1
-1.777
Falconidae
Polyborus plancus
Crested Caracara
1
0.341
Pandionidae
Pandion haliaetus
Osprey
1
0.900
Sagittariidae
Sagittarius serpentarius
Secretary Bird
1
1.159
Cathartidae
Cathartes aura
Turkey Vulture
0
0.488
Cathartidae
Coragyps atratus
Black Vulture
0
0.488
Cathartidae
Sarcoramphus papa
King Vulture
0
4.154
Cathartidae
Vultur gryphus
Andean Condor
0
1.168
