Download Parrot behavior at a Rio Manu (Peru) clay lick: temporal patterns

acta ethol (2003) 6:23–34
DOI 10.1007/s10211-003-0080-y
ORIGINAL ARTICLE
Joanna Burger · Michael Gochfeld
Parrot behavior at a Rio Manu (Peru) clay lick:
temporal patterns, associations, and antipredator responses
Received: 2 August 2002 / Revised: 6 June 2003 / Accepted: 2 August 2003 / Published online: 1 October 2003
Springer-Verlag and ISPA 2003
Abstract Although eating clay at “licks” (a form of
geophagy) has been described, there are few behavioral
data on temporal patterns, social interactions, species
associations, or reactions to potential predators. We
examined the behavior of nine species of macaws,
parrots, and parakeets at the Machiguenga Ccolpa, a clay
lick on the Rio Manu, Peru in the dry season. Three
distinct mixed-species groups used the licks: in the early
morning (parrots and small macaws), in mid-morning
(large macaws), and in the early afternoon (parakeets),
although the latter two groups used the licks at other times
of day as well. The first parrots to begin eating at the lick
in the early morning were yellow-crowned parrots
(Amazona ochrocephala) and dusky-headed parakeets
(Aratinga weddellii), followed by blue-headed parrots
Pionus sordidus, and then by mealy (Amazona farinosa)
and orange-cheeked (Pionopsitta barrabandi) parrots, and
chestnut-fronted macaws (Ara severa). Although blueheaded parrots fed in dense groups of over 50, the others
rarely exceeded 20 individuals. Scarlet macaws (A.
macao) sometimes fed alone or joined the early morning
groups, but most associated with a large group of red and
green macaws (A. chloroptera) that arrived, often scaring
off the smaller birds. On average, about 100 macaws and
parrots fed in the early morning, macaw feeding groups
averaging just over 40, and the parakeets averaged over
70. Average time at the lick ranged from 28 min for
yellow-crowned parrots to 47 min for tui parakeets. Of the
Communicated by R.F. Oliveira
J. Burger ())
Division of Life Sciences,
Rutgers University,
604 Allison Road, Piscataway, NJ 08854-8082, USA
e-mail: [email protected]
Tel.: +1-732-4454318
Fax: +1-732-4455870
M. Gochfeld
Environmental and Community Medicine,
Environmental and Occupational Health Sciences Institute,
UMDNJ–Robert Wood Johnson Medical School,
Piscataway, NJ 08854, USA
early morning group, blue-headed and mealy parrots were
the most aggressive and orange-cheeked parrots were the
least aggressive. Red and green macaws were more
aggressive than scarlet macaws; the parakeets were
equally aggressive. All species had more aggressive
interactions with conspecifics than with other species.
Responses to intruders and predators varied by species of
parrot/macaw and type of intruder. In response to
intruders or loud calls, responses could be partial (some
individuals flew away, circled, and returned), temporary
(all individuals flew away but returned within a few
minutes), or total (all flew away and abandoned feeding
for at least a half hour). The large macaws showed the
lowest rate of total abandonment and the parakeets
showed the highest. People passing up or down river in
boats scared birds from the lick. The local residents
(Machiguenga tribespeople in boats) elicited a much
greater response than did the researchers. In the recent
past, macaws and parrots were hunted for food, feathers,
and the pet trade, and the birds’ response, as well as the
presence of parrot and macaw feathers in local villages
we visited, suggests some continued exploitation, or a
long-term memory in the birds.
Keywords Clay lick · Temporal patterns · Macaws ·
Parrots · Parakeets
Introduction
Many animals deliberately eat clay or earth (geophagy).
This occurs in a wide range of animals living in tropical
regions, including invertebrates, reptiles, birds, and
mammals, including humans (Sokol 1971; Arms et al.
1974; Emmons and Stark 1979; Kreulen 1985; Abrahams
and Parsons 1996; Gilardi et al. 1999). There are many
hypotheses for why animals eat soil, including mechanical enhancement of digestion, mineral supplementation,
acid buffering, adsorption of dietary toxins, and gastrointestinal cytoprotection (Gilardi et al. 1999). Based on a
comparison of the chemical composition of selected and
24
non-selected clays, and laboratory experiments with
parrots, Gilardi et al. (1999) proposed that geophagy
protects the gastrointestinal lining from various biological
and chemical insults, which allows for greater dietary
breadth during the dry season when foods are scarce.
The range of animals using clay licks and the
frequency of use by some species suggest that eating
clay or earth is very important. Yet, facing a cliff or
coming to a bare expanse of earth potentially exposes
animals to predators. Many animals approach clay licks in
a manner that minimizes detection, such as feeding at
night, using licks deep in the forest or partly hidden by
vegetation, and coming solitarily. In several parts of
South America, parrots and macaws, however, come to
clay licks during the day, in large noisy groups, often
feeding at licks that are exposed on the banks of rivers
and streams (Munn 1994). They are thus fully exposed to
predators and must interact with the other species coming
to feed on the lick at the same time. Competition and
predation might be expected to affect behavior at clay
licks, yet this aspect of parrot behavior has not been
examined in detail.
In this article we examine the temporal patterns,
feeding behavior, aggressive interactions, and behavioral
responses to intruders of macaws, parrots, and parakeets
feeding at clay licks in the Manu National Park in Peru.
We test the following hypotheses:
1. There are no differences among species in the daily
patterns of use of the clay lick.
2. There are no differences in feeding behavior (lag time
to begin feeding, sequence in which species begin to
feed, feeding duration, species associations).
3. There are no species differences in aggression within
or among species.
4. There are no species differences in response to
intruders and predators.
Although these are stated as null hypotheses, we
expected, based on prior research, that there would be
differences in all four because of species differences in
size and overall activity patterns (Munn 1992, 1994;
Gilardi and Munn 1998; Gilardi et al. 1999). Detailed data
on these four hypotheses were gathered in August 2000.
There are many other questions than can be asked about
behavior of parrots at clay licks, such as whether species
differ in their competitive ability, whether some birds are
denied access to clay on any given day, and whether they
require clay. The objective of this article, however, was to
examine behavior during one season throughout which
population numbers of each species and weather conditions were similar to provide basic data on behavior at the
lick. Such quantitative data are not presently available,
and this is a first step in understanding behavior and
competition at a clay lick.
Parrots (Psittaciformes) comprise a diverse order of
birds that occur primarily in Australia, the Neotropics,
and in tropical Africa and Asia (Forshaw 1989). Many
parrot species are threatened by capture for local use and
the pet trade, and by widespread habitat destruction
(Gochfeld 1974; Butler 1992; Beissinger and Snyder
1992; Munn 1992; Casagrande and Beissinger 1997; Guix
et al. 1999). The behavior and ecology of many species of
African and Australian parrots have been studied because
they inhabit open country, many species feed on the
ground in great numbers, and some are agricultural pests
(McFarland 1991; Emison et al. 1994). However, relatively little is known about the behavior of most species
of Neotropical parrots in the wild because they are forest
dwelling, and most nest solitarily high in the trees.
Although some species form roosting aggregations
(Chapman et al. 1989), they disperse widely to feed.
Considerable attention has been devoted to conservation of Neotropical parrots that are threatened or endangered (see papers in Beissinger and Snyder 1992;
Christian et al. 1996a, 1996b; Munn 1998; Marsden et
al. 2000), and to those few Neotropical parrots that are
crop pests (Bucher 1992). Gilardi and Munn (1998)
studied activity, flocking, and habitat use of parrots in the
same area where we worked. By sitting on observation
decks 25–30 m above the forest floor, they found that
parrot and macaw activity peaked just after sunrise, with a
second peak following the mid-day low, except for
parakeets, which were active in the early afternoon.
Flocks were exclusively monospecific except when
foraging or eating clay (at the same licks we studied),
and for most species, averaged fewer than six individuals
(Gilardi and Munn 1998). The behavior of these neotropical Amazon parrots, macaws, and parakeets is in contrast
to some of the Australian species that sometimes form
large flocks in grasslands, grainfields, and fruit-growing
areas (Westcott and Cockburn 1988). One situation in
which Neotropical parrots congregate is at clay licks in
the Amazon basin (Munn 1992, 1994). Our studies of the
behavior of macaws, parrots, and parakeets at clay licks
complement those of Gilardi and Munn (1998).
Methods
We studied the behavior of nine species of macaws, parakeets, and
parrots feeding at clay licks, or “ccolpas,” on the Manu River
Madre del Dios, Peru during August 2000. The main series of
licks (1148.930 S, 7125.400 W) is about 1 km upriver from
the Machiguenga Ccolpa Biological Station (1150.2920 S,
7125.5460 W; Fig. 1). We studied a second lick (1150.3900 S,
7125.2450 W) in a nearby “quebrada,” or creek, about 500 m
upstream from its mouth. The elevation is about 350 m, and the site
is about 12 h by boat (depending on water depth) upriver from the
junction of the Manu and the Alto Madre de Dios Rivers, near the
town of Boca Manu. The licks are the site of the main macaw
studies conducted by Munn (1992), who founded the biological
station.
The study area is within the Manu National Park, created in
1973 as part of the Manu Biosphere Reserve (designated in 1977) to
include the Manu Reserve Zone and the National Park, covering an
area of 1.5 million hectares. Ecological features are extensively
described in the book Manu (Wilson and Sandoval 1996) and in
many papers cited therein. Our study area was selected because it is
above the tourist zone, reducing the likelihood of human disturbance and ensuring that the behavior we were observing was not
unduly influenced by ecotourists (Munn 1992). Observation blinds
25
Fig. 1 Temporal patterns in
initiation of feeding bouts at the
Machiguenga clay licks in
Manu National Park, Peru
were constructed 2 weeks before our arrival to allow time for
habituation.
The main clay area along the river is on a cliff, which at the
time of our visit (low water) was about 9–12 m high. A skirt of
almost flat river bank was exposed. The clay lick is thus exposed to
a wide expanse of river and is visible from 1 km away. On the
terrace above the cliff is mature rain forest dominated by figs
(Ficus spp.). At this point the Manu River is about 80–100 m wide.
The far bank, from which we made some observations, consisted of
a broad sandy beach (inundated after 2 days of rain), backed by a
dense stand of Tessaria trees and giant cane (Gynerium), behind
which is low-lying varzea forest dominated by Cecropia trees with
a rich flora of palms (Palmaceae), flooded during the rainy season.
This is similar to the vegetation studied in greater detail at Cocha
Cashu Biological Station (18 km downriver, Terborgh 1985).
Parrots were observed on the river lick feeding on five exposed
cliff faces; other presumably suitable faces were currently covered
with dense vegetation. The five faces extended over a length of
about 350 m. Distances between the faces on this lick varied from 8
to 150 m. The quebrada lick, about 1.5 km away, had only one face,
with a skirt of land beneath it sloping down to a stream about 20 m
wide. It was surrounded by vegetation. The lick was visible only
from about 30 m on either side. Our observation blind was about
15 m from the lick.
The species that regularly fed at the clay lick included scarlet
macaw (Ara macao), red and green macaw (A. chloroptera),
chestnut-fronted macaw (A. severa), dusky-headed parakeet
(Aratinga weddellii), tui parakeet (Brotogeris sanctithomia), and
orange-cheeked (Pionopsitta barrabandi), blue-headed (Pionus
sordidus), yellow-crowned (Amazona ochrocephala), and mealy
(A. farinosa) parrots. Cobalt-winged parakeets (B. cyanoptera)
rarely came to the lick with the other parakeets, and several species
known to occur in the area were not observed at the licks during our
visit. Blue and yellow macaws (Ara ararauna) were seen daily at
the quebrada, but not at the licks during our study, although large
numbers occur at other licks in southeastern Peru. Other species
that came to the lick included plumbeous pigeon (Columba
plumbea), speckled chachalaca (Ortalis guttata), and blue-throated
piping guan (Pipile cumanensis).
Our overall protocol was to observe at the lick from before
dawn (0530 hours) until late afternoon (about 1700 hours). We
always arrived at the blinds when it was still dark and before any
parrots were in the vicinity and left only after there were no birds
remaining in the area. Observations were made from blinds located
26
(1) 8–12 m from the central section of the river lick on the same
bank, (2) across the river from the river lick, and (3) across the
stream from the quebrada lick. Three or four observers were
required to watch both licks at the same time and record arrivals
and departures by species and interactions (about 3.5 person
months). We coordinated our activities among ourselves and with
our boatman using walkie-talkies to minimize disturbance to the
birds.
We made four kinds of observations: temporal patterns of lick
use, number of each species feeding at the lick, aggressive
encounters at the lick, and responses to predators and other
intruders. We also recorded when each species arrived in the trees
above the lick. From the close blind at the river, we could not see
all the tree tops, and arrival was noted by identifying vocalizations.
Temporal patterns were recorded by noting the time that the
first individual of each species landed on the lick to begin feeding,
and final departure of all individuals. We defined a feeding bout as
the time between when the first individual landed to feed and the
last one departed, with the lick used relatively continuously during
that time. We classified departures into three types. In a “partial”
departure, most birds left suddenly, but some birds remained and
were rejoined shortly, usually within 1–5 min. In a “temporary”
departure, all birds flew and either circled or landed in nearby trees
and returned, usually within 5 min. In a “total” departure or
abandonment, all birds left and none returned to the lick within
30 min. In the case of temporary departures, we did not identify the
end of the bout until 30 min had elapsed.
We also recorded the number of each species present every 1–
5 min, depending on the changing species composition at the lick.
Since the number of individuals (and species) feeding at the lick,
particularly in the early morning, was very dynamic, we arbitrarily
analyzed the data as follows. To examine the number of
heterospecifics present for each species we analyzed the data by
noting how many of each species were present when the number of
any species being examined was the highest for that bout. For
example, if the maximum count for a given feeding bout for
yellow-crowned parrots was 12, we used the number of each other
species present the first time 12 was reached as the heterospecific
feeding flock size. The maximum counts for the various species
usually did not coincide.
Since the number of individuals feeding at the lick varied
markedly from minute to minute, and it was difficult to record all
aggressive interactions when the lick had over 35 individuals, we
recorded the number of aggressive interactions observed and the
number of birds we were observing. We compared aggression
among species using both a conspecific and heterospecific aggression index. We defined the conspecific index for species A as the
total number of intraspecific aggression interactions of A/number
of feeding bouts with A presentmean maximum number of species
A present for all the bouts. We defined the heterospecific index for
species A as the total number of heterospecific aggressive
interactions of A/number of feeding bouts of species Amean
maximum number of all heterospecifics present while species A
was feeding. These two indices provide a comparison for aggression rates among species.
We examined the responses of feeding birds to predators and
intruders by recording whether there was no response, partial,
temporary, or total departure, following certain visual or acoustic
stimuli. Many loud noises or sudden appearances of large birds
triggered a departure, often a total departure. By observing
simultaneously from different blinds we increased our likelihood
of identifying intruders. Raptorial birds (most of which are not
potential parrot predators) included hawk eagles (Spizaetus spp.),
roadside hawk (Buteo magnitorstris), great black-hawk (Buteogallus urubitinga), king vulture (Sarcoramphus papa), black vulture
(Coragyps atratus), greater yellow-headed vulture (Cathartes
melambrotus), and black caracara (Daptrius ater). Birds also
responded to the warning cries of russet-backed oropendola
(Psarcolius angustifrons), red howler monkey (Alouatta seniculus),
and dusky titi monkey (Callicebus moloch), to the voices of people,
the sound of motorized canoes, and the presence of white-lipped
peccaries (Tayassu pecari) and jaguar (Panthera onca).
The smaller parrots and parakeets responded to the alarm calls
and arrivals of the large macaws. We combined the parrots,
parakeets, and macaws into three species groups and present the
percentage of times that these three groups partially or temporarily
flew, or abandoned a feeding bout. The groups included very large
birds (scarlet and red and green macaws), intermediate-sized birds
(chestnut-fronted macaws and the two amazon parrots, blue-headed
and orange-cheeked parrots), and smaller birds (dusky-headed and
tui parakeets).
Comparisons among groups were made with analysis of
variance, followed by Duncan multiple range tests to examine
differences between groups. We accept a level of significance as
P<0.05, and in the text we give means and standard errors.
Results
Daily temporal patterns
Observations on the daily patterns of feeding at two licks
were made in the dry season of August 2000. There were
three main temporal assemblages of species feeding at the
licks: (1) the parrots and chestnut-fronted macaws fed in
the early morning; (2) the large macaws fed from midmorning to early afternoon; and (3) parakeets fed
throughout the day, but peaked in the early afternoon
(Fig. 1). The clay licks served as a gathering place for
parrots and chestnut-fronted macaws in the early morning, and pairs flew to the trees above the lick from nearly
all directions. With first light (between 0530 and
0545 hours), chestnut-fronted macaws and parrots (mealy,
yellow-crowned) began to arrive in the treetops all along
the licks. Over a period of 5–20 min vocalizations
increased, and the birds coalesced in leafless trees above
the main central licks. Gradually, with increasing group
vocalizations, they began to move lower in the trees and
to land first in the shrubs above the lick, then on exposed
limbs hanging over the top of the lick; they then started
climbing down the vines toward the lick. Although the
noise of the flock increased, the first parrots to land on the
lick were usually silent. On most mornings, the first parrot
to land on the lick was a yellow-crowned parrot, followed
quickly by one or two conspecifics, and then usually by
blue-headed parrots.
Parrots (mealy, yellow-crowned) and chestnut-fronted
macaws always initiated feeding bouts in the early
morning, mainly between 0600 and 0700 hours (Fig. 1).
Most red and green macaws initiated feeding bouts
between 0900 and 1200 hours, although some bouts were
initiated as early as 0800 and as late as 1600 hours.
Although scarlet macaws usually fed with the red and
green macaws, some joined the early morning parrots and
some came to the lick alone. Of the 58 bouts of scarlet
macaws feeding, 19% were of one or two solitary
individuals, with no other parrots, macaws, or parakeets
around. In the quebrada, dusky-headed parakeets sometimes fed alone. The other species rarely fed alone, and
this only occurred when a whole group started to come
down on the vines and branches but were startled away by
the appearance of a predator or intruder.
27
Fig. 2 Schematic of arrival and feeding durations for parrots and
chestnut-fronted macaws at the clay lick along the Manu River.
Data based on five bouts where all five species were present and
began feeding before 0600 hours. Time zero is about 0600
The pattern of feeding at the licks is illustrated in
Fig. 2 for parrots and chestnut-fronted macaw for 1 day.
In most instances, yellow-crowned parrots landed on the
lick first and began to feed before the others. Blue-headed
parrots quickly joined them, and a few minutes later, the
other species landed. While the number of most species
rarely exceeded 20, blue-headed parrots fed in much
larger groups. They usually fed in the same small section
Table 1 Temporal patterns in use of a clay lick in Machiguenga
Ccolpa clay lick in Manu, Peru (mean€SE). Species sharing the
same letter in a column do not differ significantly at P=0.05.
Species
Bouts
(n)
Time of day to
start feeding
Yellow-crowned parrot
36
06:50€0:07
C
6:47€0:06
C
6:59€0:09
C
7:01€0:09
C
7:04€0:14
C
10:46€0:22
B
10:26€00:27
B
10:31€0:47
B
11:46€0:44
A
176 (0.0001)
Chestnut-fronted macaw
Blue-headed parrot
Mealy parrot
23
42
29
Orange-cheeked parrot
21
Red and green macaw
45
Scarlet macaw
58
Dusky-headed parakeet
45
Tui parakeet
40
Kruskall–Wallis 2 comparison
of the lick, often piling on top of one another. Yellowcrowned parrots seemed intimidated by the appearance of
the mass of blue-crowns and either left or moved to the
edges of the lick to continue feeding.
Mean time to start feeding at the clay lick confirms the
relationships shown in Fig. 2 (Table 1). Not all species
started feeding at the beginning of the bout, although most
came down to the lick within about 10 min. Mean
duration of feeding bouts varied significantly by species
(Table 1). Table 1 also shows the order of appearance,
which is the mean number of appearances of the total
times that species visited. That is, each day, each species
was given a ranking for its order of appearance.
The order of appearance was as follows: yellowcrowned parrots (with the lowest number) usually landed
first, followed by blue-headed parrots, whereas orangecheeked parrots were usually last. Since the birds came in
three groups (parrots, parakeets, macaws), the numbers
reflect that pattern. Thus, yellow-crowned parrots came
first for the parrots, the macaws came at about the same
time, and the parakeets alternated which species landed
first (Table 1).
Species associations
Usually there were fewer than 20 individuals of each
species feeding in the early morning group, except for
blue-headed parrots (Table 2). The average number of
red and green macaws feeding at the lick was about 35,
while there were usually only about 6 scarlet macaws
Comparisons are made with Kruskal–Wallis one-way ANOVA,
yielding a 2 statistic. Duncan multiple range groupings are given
below
Lag time to initiate
feeding after first
species fed
(min)
0.69€0.33
C
9.61€1.63
A
3.52€0.66
B
9.34€1.73
A
10.5€2.13
A
0.47€0.13
C
1.83€0.89
B, C
0.58€0.25
C
0.53€0.26
C
178 (0.0001)
Duration of
feeding
(min)
28.7€3.28
B
32.7€4.87
B
37.7€3.96
A, B
35.0€4.40
B
31.5€4.11
B
33.1€3.48
B
34.5€3.02
B
38.5€3.44
A, B
47.4€3.55
A
17.9 (0.02)
Order of
appearance
1.25€0.09
D
3.91€0.23
A
1.98€0.13
C
3.41€0.18
B
3.71€0.29
A, B
1.51€0.09
D
1.55€0.16
D
1.38€0.09
D
1.35€0.12
D
172 (0.0001)
Total number
of parrots and
macaws feeding
98.3€10.5
A, B
112€11.5
A
94.7€9.16
A, B, C
112€10.6
A
112€15.2
A
44.8€4.23
D
42.1€4.91
D
77.2€7.14
B, C
72.1€4.83
C
83.6 (0.0001)
Bouts
(n)
36
23
42
29
21
45
58
45
40
Species feeding at lick
Yellow-crowned parrot
Chestnut-fronted macaw
Blue-headed parrot
Mealy parrot
Orange-cheeked parrot
Red and green macaw
Scarlet macaw
Dusky parakeet
Tui parakeet
58.9€4.13
13.5€1.26
5.79€0.64
35.8€3.59
5.86€1.39
17.3€2.69
56.5€5.67
6.96€1.36
16.6€2.41
Mean number
of conspecifics
5.81€1.58
B, C
4.66€1.24
C
3.62€0.91
B
3.81€1.05
C
Chestnut
0.60€0.47 0.15€0.15
B
B
3.24€1.69 1.02€0.64
C
C
0.66€0.53 0.60€0.40
C
C
0.13€0.13 0.13€0.13
B
B
13.5€4.07
B
15.7€3.06
B
13.3€2.31
A
15.2€3.37
B
Yellow
Other species
13.5€3.50
B
12.6€2.18
A
15.8€2.94
B
13.6€2.44
B
Mealy
2.52€0.80
C
2.69€0.77
B
4.26€1.26
C
2.44€0.89
C
Orange
1.56€0.72 1.09€0.56
C
C
1.00€1.00 0.58€0.58 0.08€0.08
B
B
B
14.0€5.11
B
0.60€0.40 0.98€0.68 0.10€0.06
B
C
C
0.00€0.00
B
0.00€0.00
C
26.7€3.46
A
0.00€0.00
C
0.07€0.07
C
0.10€0.07
B
0.00€0.00
C
0.06€0.06
C
Red and
green
0.30€0.17
B
0.36€0.17
C
6.42€0.81
A
0.33€0.25
C
0.34€0.21
C
0.29€0.15
B
0.17€0.12
C
0.11€0.08
C
Scarlet
Tui
10.5€1.53
A
42.4€5.60
A
0.00€0.00 0.00€0.00
C
C
0.00€0.00 0.00€0.00
B
B
5.43€2.09 2.57€2.57
B, C
B, C
3.83€1.55 3.45€2.28
C
C
3.29€1.16 2.38€1.58
B
B
2.70€1.60 3.00€2.41
C
C
3.11€1.18 3.44€1.99
C
C
Dusky
172 (0.0001)
96.3 (0.0001)
196 (0.0001)
248 (0.0001)
85.7 (0.0001)
134 (0.0001)
120 (0.0001)
107 (0.0001)
152 (0.0001)
Kruskal–Wallis 2 comparison
significantly at P=0.05. Comparisons are made with Kruskal–Wallis one-way ANOVA,
yielding a 2 statistic. Duncan multiple range groupings are given below
1.27€1.03 0.93€0.85 0.04€0.04
B
B
B
65.2€9.09
A
64.2€6.82
A
64.1€7.04
A
55.1€6.71
A
Blue
Table 2 Mean number of heterospecifics feeding at clay licks in Machiguenga Ccolpa
clay lick in Manu, Peru. Species sharing the same letter in a column do not differ
28
29
Fig. 3 Frequency distribution
of the maximum number of
each species feeding at the clay
lick. Shown are percentages for
each feeding group size
with them. Dusky-headed parakeets usually fed in small
groups of less than 20, whereas tui parakeets fed in
larger groups of nearly 60 (Table 2). Figure 3 shows the
frequency distribution of the maximum number present
for each clay-feeding bout. Although the mean for the
maximum number of individuals present gives an
indication of central tendency, it does not adequately
describe the variation in the maximum number that fed
each day.
The heterospecifics feeding with each species are
shown in Table 2. There are differences in the species
composition because of the temporal pattern of feeding at
clay licks. It is clear from this table that some species (tui
parakeet) rarely fed with other species, while the parrots
always fed with other species.
Even at the river lick, they did not use the five faces
equally (Table 3). Only the parakeets used the first
section, and they mainly used the first and second sections
and did not come to the central faces. Similarly only the
macaws used the fifth section.
30
Table 3 Use of different faces of the river lick, given as percents of
bouts for each species on each face
River Licks
Yellow-crowned Parrot
Chestnut-fronted macaw
Blue-headed parrot
Mealy parrot
Orange-cheeked parrot
Scarlet macaw
Red and green macaw
Tui parakeet
1
2
3
4
46%
50%
50%
50%
67%
34%
27%
25%
25%
21%
20%
22%
37%
32%
47%
29%
25%
29%
30%
11%
7%
14%
53%
Table 4 Aggression indices for species of parrots, macaws, and
parakeets feeding at a riverine clay lick in Manu, Peru. Index Total
aggressive encounters/number of boutsmean number present
5
22%
27%
Aggressive interactions
The feeding assemblages of macaws, parrots, and parakeets at clay licks are very dynamic, with frequent shifts
in the species composition, the number of birds present,
and the relative proportion of different species. The large
numbers of birds at the lick resulted in displacements as
birds tried to land; there were also deliberate displacements, lunges, and fights with others on the lick. In
general, birds landed near conspecifics and defended
space against them, often supplanting them. The conspecific aggression index was higher for each species than
the heterospecific aggression index (Table 4). There were
also differences in the index among species: (1) in the
early-morning feeding group, blue-headed parrots were
the most aggressive, followed by mealy parrots; (2) red
and green macaws were more aggressive than scarlet
macaws; and (3) the two parakeets had similar aggression
indices (Table 4). The heterospecific index mirrored the
Early-morning group
Yellow-crowned parrot
Blue-headed parrot
Mealy parrot
Chestnut-fronted macaw
Orange-cheeked parrot
Mid-morning group
Red and green macaw
Scarlet macaw
Early-afternoon group
Dusky-headed parakeet
Tui parakeet
Conspecific
index
Heterospecific
index
0.065
0.391
0.204
0.037
0.022
0.006
0.063
0.021
0.003
0.0009
0.516
0.19
0.317
0.028
0.082
0.11
0.002
0.003
conspecific index; blue-headed parrots and red and green
macaws were also aggressive toward other species;
yellow-crowned parrots and orange-cheeked parrots were
not very aggressive toward conspecifics or toward
heterospecifics (Table 4).
Responses to intruders and predators
Because clay licks are visible, birds feeding at a clay lick
are vulnerable to disturbances from intruders and predators. The birds were generally very wary. The response
pattern varied among the species (Table 5). Possible
responses included no change in behavior, flight of some
Table 5 Response of macaws, parrots, and parakeets to intruders and disturbances at a clay lick in Manu, Peru. Given is percent of bouts
the birds partially or permanently abandoned the lick (the remaining time they stayed)
Disturbance
Raptor
Large hawks/eagles
Roadside hawk
Black vulture
King vulture
Black caracara
Macaw/parrots
Large macaw call
Large macaw land
Small macaw call
Blue-headed landa
Oropendola callb
Monkeys
White-lipped peccaries
Jaguar
Machiguenga
Researchers
a
Over
b
Large macaws
Intermediate macaws and parrots
Parakeets
Bouts
(n)
Partial or
temporary
%
Abandoned
%
Bouts
(n)
Partial or
temporary
%
Abandoned
%
Bouts
(n)
Partial or
temporary
%
Abandoned
%
28
13
8
4
14
54
0
25
100
14
38
0
50
0
14
33
22
20
8
23
33
0
20
0
26
55
0
60
100
70
24
12
10
10
26
17
58
10
0
19
83
25
80
100
79
66
21
26
65
50
45
38
5
12
22
28
79
18
196
35
55
59
95
88
0
54
13
–
–
43
18
20
0
6
26
46
87
0
25
30
66
64
0
79
89
50
26
46
56
56
21
49
18
65
53
6
55
33
6
28
16
–
–
–
–
16
60
58
33
36
13
25 landing at once
Loud social calls and alarm calls
14
27
25
6
18
19
57
82
80
100
94
11
31
lived about 6 km upriver sometimes passed by in nonmotorized canoes. The macaws, parrots, and parakeets
nonetheless responded differently regardless of the similar-looking boats. While the researchers usually moved
along the middle of the river, or were closer to the clay
lick, the Machiguenga usually went in the center or
toward the opposite side (near the sand bar where they
could look for turtle eggs). The greatest response, loud
calling and flying around, followed by complete abandonment of the lick and all the trees in the vicinity,
occurred when a boat of five Machiguenga stopped on a
mudflat across from the clay lick, and the people
disembarked to hunt for turtle eggs. When a similar
boatload of researchers landed, the birds were only
temporarily disturbed and returned to feeding on the lick.
Both groups of people were generally silent, and the noise
level did not appear to vary between groups.
Discussion
Competition
Fig. 4 Percent of times each group totally abandoned the feeding
bout because of interactions with different intruders and predators.
Large macaws include scarlet, and red and green; parrots include
chestnut-fronted macaw and the parrots; parakeets include tui and
dusky-headed. *P<0.01; **P<0.001
individuals from the lick temporarily (partial), flight of all
individuals from the lick temporarily (temporary), or
permanent flight of all the individuals from the lick,
ending the feeding bout (total abandonment). At times
each of these responses occurred when we could not
detect or find the apparent stimulus. Therefore, we
recorded behavior when an intruder or potential predator
was visible from the clay lick or when there was an
audible sound. Responses varied depending upon both the
species of macaws, parrots, and parakeets, and the type of
intruder (Table 5). Overall, large macaws reacted the
least, and parakeets’ reactions were the strongest (Fig. 4),
although they also returned most quickly. A jaguar
grunting and the local inhabitants (Machiguenga tribe),
in boats, elicited the strongest responses from all three
groups, and researchers elicited the weakest responses
(Fig. 4, Table 5). The warning calls of oropendolas
(which nested in a tree close to the quebrada lick) elicited
some responses from the parrots and parakeets, and the
calls of large macaws elicited some responses from the
other species, even if they were feeding at a lick 100 m
away.
The response to people bears comment. Usually people
(Machiguenga and researchers) went by the lick in boats
and did not stop. Although researchers mainly used
motorized boats with a sun cover, they did not always do
so, and sometimes they used local motorized boats similar
to those used by the Machiguenga and other local people
passing up and down the river. The local tribespeople who
The daily patterns in use of the clay licks were consistent
from day to day during the observation period. There
were three main groups feeding at the licks. Parrots and
chestnut-fronted macaws fed in the early morning just at
daybreak, the large macaws (scarlet, red and green) fed
mainly in mid and late morning, and the parakeets fed
mainly in the early afternoon. In addition, the degree of
consistency varied among these three groups. The species
feeding in the early morning did not come to the licks to
feed at other times of the day. The parakeets came and fed
at the lick at nearly all times of the day but did not remain
in the vicinity except when feeding. The large macaws
normally fed in the late morning but came at other times
of the day to feed at the lick and often remained in the
trees above the lick for much of the day.
We attribute these differences in behavior to differences in overall activity patterns, interactions among the
species, and antipredator behavior (see below). Gilardi
and Munn (1998) studied the activity patterns and
flocking behavior of this same group of macaws, parrots,
and parakeets in the same region and found that parrots
and macaws were active just after sunrise, with another
peak after the mid-day lull, although the parakeets were
active in the early afternoon. Activity, defined as flight
over the forest, was highest from about 0630 until
0900 hours. These patterns are consistent with the
patterns of feeding at clay licks observed in this dry
season study.
Gilardi and Munn’s (1998) observations, and ours,
suggest that the parrots and chestnut-fronted macaws
came to the lick at the early part of their activity and then
left to forage for fruits and seeds. Similarly, the duskyheaded parakeets came to feed at the clay lick in the early
part of their most active period and flew over the forest to
search for food afterward. The large macaws, on the other
hand, came to the lick at least 1.5 h after dawn and were
32
presumably foraging for food in the early part of their
activity pattern, prior to coming to the lick. Some scarlet
macaws were exceptions in that they fed in the early to
mid morning, sometimes with the parrots and sometimes
by themselves. They never came, however, right at
sunrise.
The social nature of the lick was exemplified by the
use of only one of the five faces at any given time. The
birds, particularly the large macaws, seemed to take time
to decide which face to use for a given bout. However,
once one bird landed on a lick, others joined in. Almost
never were two faces in use at the same time. When two
faces were used, it was usually by two different species
groups (i.e. macaws at one, parakeets at the other).
Only the macaws seemed to use the clay lick area as a
social gathering place. Once they arrived, usually in pairs,
they spent more time preening and calling before they
came down to feed on the clay, and they frequently
remained in the treetops for much of the rest of the day.
Pairs slept, preened, or simply remained vigilant until
they departed in the late afternoon. This phase was
variable in that on some days many remained near the
clay lick, on others few remained, and on a very few days
they all departed by early afternoon. Such departures,
however, were often preceded by the appearance of eagles
or Machiguenga in boats. We usually waited to call our
boat to get us until there were few macaws in the trees
overhead. However, when the boat came for us, the few
remaining macaws would call loudly, sometimes circling
over the river, but usually did not abandon the area.
When present, the large macaws seemed to dominate
the clay lick by their size, as is evident by the percent of
times the other species abandoned the clay lick for the day
if the large macaws landed at the lick. Abandonment by
parrots often occurred when the macaws began to increase
their calling rate from the trees over the lick as a prelude
to descending. It usually occurred as soon as one of the
large macaws landed on branches or vines above the lick,
and always occurred if more then two macaws landed on
the clay cliffs.
Size was not the only factor affecting behavior at the
lick. Aggression and numbers also influenced both
feeding at the lick and location of feeding. The largest
species was not always the most aggressive. For example,
blue-headed parrots were smaller than several of the other
species that they fed with, yet they were the most frenetic
and aggressive. Within feeding associations (the three
types of feeding groups), the most aggressive species
usually had primary access to the best clay-eating places.
In the early-morning group, blue-headed parrots were
the most aggressive toward both conspecifics and heterospecifics, and they usually displaced the other species,
piling into the niche cut deeply into the cliff face,
evidence of generations of parrot favoritism. Of the two
large macaws, the larger red and green were more
aggressive than scarlet macaws, and they overwhelmed
them by numbers as well. The parakeets were similarly
aggressive, and there was no clear pattern in displacements. Individuals were primarily aggressive toward
conspecifics, which seemed to us to result from their
pattern of landing near conspecifics.
In addition to size and aggressiveness, density was a
factor. Blue-headed parrots showed great tolerance for
being in contact with conspecifics. Yellow-crowned
parrots were often displaced from the preferred places
by the mass of landing blue-headed parrots and moved off
to the side. Even when blue-headed parrots landed away
from the main group, they quickly moved over to the
main group of blue-headed parrots, forcing others away.
Sometimes they even climbed on top of one another, and
both the one on top and the one underneath continued to
feed. Yellow-crowns, mealys, and orange-cheeked parrots
quickly moved away from these dense groups of blueheaded parrots. Other factors, such as conspecific group
size, could have played a role.
Moreover, where they landed was not only a function
of the preferred feeding place (a line of pale reddish clay,
where indentations indicated months and years of eating).
They usually landed very close to conspecifics. For
example, when other yellow-crowned parrots came to the
lick, they joined conspecifics already there, even though
there were other unoccupied places on the lick. This
happened with all the other species that fed with the blueheaded parrots. The blue-headed parrots, by virtue of their
numbers and crowding, simply forced all other species to
the edge. The only exception to this pattern was when a
scarlet macaw landed and moved toward the blue-headed
parrots. Even then, however, one macaw seldom displaced the dense mass of blue-headed parrots. This
phenomenon has also been shown for gulls feeding at a
garbage dump, where the smaller laughing gull (Larus
atricilla) was able to displace the much larger herring gull
(L. argentatus) simply by feeding in groups so large,
dense, and frenetic, that the herring gulls could not find a
place to land and feed (Burger and Gochfeld 1984).
The much smaller parakeets dealt with competition
from the larger species by either abandoning feeding at
the lick when larger species arrived, moving to the edges
(leaving a meter between them and the larger species), or
using a lick not preferred by the other species. They
moved to the edges when confronted by parrots or
chestnut-fronted macaws and left completely or used a
different lick when confronted by the large macaws
(scarlet, red and green). Avoiding interactions with larger
species is not an unusual pattern, and having access to
different food items (or in this case clay) is often achieved
partly on the basis of size and weight (Roth 1984).
Antipredator behavior
Macaws, parrots, and parakeets feeding at clay licks are
vulnerable to disturbance and to predation because many
of the clay licks are on major rivers used for transportation by people and the openness of the river makes them
visible for some distance. In addition, they are often quite
noisy while feeding on the lick. Birds waiting in the trees
are particularly noisy. These characteristics ensure that
33
they would be detected by predators or people seeking to
capture them. While feeding on the lick itself they are
vulnerable to raptors, particularly birds that can capture
them in flight. One of the advantages of having birds in
the trees that are waiting to take their turn at the lick is
that these can be vigilant and warn of impending danger.
While parrots regularly expose themselves to predators on
the bare branches of trees, these sites are not as well
known, and usually far fewer gather at any one point. The
clay licks are presumably known to predators.
The response of the birds to intruders and potential
predators varied by the species of macaw, parrot, or
parakeet, and by the species of predator. Westcott and
Cockburn (1988) found that vigilance in Australian
parrots increased with the potential risk from predators.
In our study, antipredator responses also were strongest
(total abandonment of the lick) to the predators presenting
the greatest risk. The strongest responses were to some
raptors, jaguars, and Machiguenga. Some of the raptors
are undoubtedly predators on the parrots and parakeets,
and large cats would take them if they had a chance.
The Machiguenga also engendered a strong response,
mainly when they went down the river in their canoes and
small motorized boats. It was not merely the presence of a
boat that disturbed them because the birds rarely
responded severely to researchers in boats. Although
capture of the macaws, parrots, and parakeets is illegal
and is discouraged by the park personnel, the native
peoples are allowed to capture wild birds and other game
for subsistence and cultural uses. We observed
Machiguenga hunting for turtle eggs (also discouraged)
and saw macaw and parrot feathers in local villages.
Further, even if there was currently no exploitation by the
Machiguenga and other local people, macaws and parrots
are long-lived and would likely remember encounters that
occurred more than a decade ago. Munn (1992) has
suggested that parrot licks may well be protected by
having the local communities deriving revenues from
providing tourist opportunities.
The responses to intruders and predators varied among
the macaws, parrots, and parakeets, mainly as a function
of body size. The larger macaws responded less severely
and rarely abandoned feeding at the clay lick completely
when there was no clear and significant threat, whereas
the parakeets often abandoned a feeding bout when faced
with raptors and mammals. The parakeets responded
more frequently to the warning calls of the oropendolas
than did the other species. The parrots were generally
intermediate in their response. The differences in responses were no doubt due to the very real threat of
predation; the smaller species were more vulnerable to
predators, although they were probably less vulnerable to
capture by humans.
Conservation implications
Since macaws, parrots, and even parakeets are vulnerable
to a wide range of exploitation by humans (see papers in
Beissinger and Snyder 1992), it is important to understand
the behavior and ecology of their entire life cycles to aid
in conservation. The relative importance of feeding on
clay for these species (Gilardi et al. 1999) forces the birds
to seek out licks even though they are exposed. Not all
licks are equally exposed, and the birds can go to a nearby
lick when disturbed. Although we did not have marked
birds, we communicated with walkie-talkies and kept
track of the exact time birds arrived and left both the river
and quebrada lick. On several occasions, birds that
abandoned the river lick because of the presence of
eagles, jaguars, or Machiguenga appeared at the creek
lick (the same species and relative composition). Although not conclusive, this is suggestive of using several
licks within the same region.
The differential response to researchers and Machiguenga suggests that these birds clearly distinguish different people and confirms that some observation by people is
possible without unduly disturbing the birds. Indeed, there
are several places where lodges provide viewing opportunities for tourists from blinds located on rivers across from
clay licks. Our observations, however, confirm that the
birds habituate and can distinguish different human
activities. Ecotourism is an important conservation tool
for preserving parrots, particularly when such monies
enrich the local and regional inhabitants (Munn 1992).
Finally, our observation of the small clay lick along the
creek suggests that some habitat modification may be
possible to create additional licks so that there are options
for birds when they are disturbed from one lick. At the
end of our field work we removed some vegetation from
in front of one section of the main riverine lick (for
photographic purposes) and found that the large macaws
immediately moved to this new area and fed there,
suggesting some limitation in “good” clay lick faces. Our
actions opened an area where the preferred clay layer was
still relatively soft and easy to break off, and where there
were sufficient vines for easy access to the lick. The vines
provided places for macaws waiting their turn to cling. In
some regions, there may be few clay licks, and creating
other licks may prove useful.
Acknowledgments The authors wish to thank Wilfredo Arizabal
Arriaga (Willie) for serving as our guide and field assistant,
Faustino Fernandez, Alberto Flores, and Miguel Palacio for field
assistance, Kit Herring and the U.S. and Peruvian staffs of
Inkanatura for logistical arrangements and provision of a welltrained field staff. We are particularly indebted to C.A. Munn for
setting us up in his field station and providing information on the
parrots and local people. We thank the Peruvian government and
the Manu National Park for permits for work in the restricted area
of the park and for providing advice while at the station.
References
Abrahams PW, Parsons JA (1996) Geophagy in the tropics: a
literature review. Geogr J 162:63–72
Arms K, Fenney P, Lederhouse RC (1974) Sodium: stimulus for
puddling behavior by tiger swallowtail butterflies, Papilio
glaucus. Science 185:372–374
34
Beissinger SR, Snyder NFR (eds) (1992) New World parrots in
crisis: solutions from conservation biology. Smithsonian Institution Press, Washington, D.C.
Bucher EH (1992) Neotropical parrots as agricultural pests. In:
Beissinger SR, Snyder NFR (eds) New World parrots in crisis:
solutions from conservation biology. Smithsonian Institution
Press, Washington, D.C., pp 201–220
Burger J, Gochfeld M (1984) Foraging efficiency: the cost of being
outnumbered. Bird Behav 5:81–89
Butler PJ (1992) Parrots, pressures, people, and pride. In:
Beissinger SR, Snyder NFR (eds) New World parrots in crisis:
solutions from conservation biology. Smithsonian Institution
Press, Washington, D.C., pp 25–46
Casagrande DG, Beissinger SR (1997) Evaluation of four methods
for estimating parrot population size. Condor 99:445–457
Chapman CA, Chapman LJ, Lefebvre L (1989) Variability in parrot
flock size: possible functions of communal roosts. Condor
91:842–847
Christian CS, Potts TD, Burnett W, Lacher TE (1996a) Parrot
conservation and ecotourism in the Windward Islands. J
Biogeogr 23:387–393
Christian CS, Lacher TE Jr, Zamore MP, Potts TD, Burnett GW
(1996b) Parrot conservation in the Lesser Antilles with some
comparison to the Puerto Rican efforts. Biol Conserv 77:159–
167
Emison WB, Beardsell CM, Temby ID (1994) The biology and
status of the long-billed corella in Australia. Proc West Found
Vertebr Zool 5:211–247
Emmons LH, Stark NM (1979) Elemental composition of a natural
mineral lick in Amazonia. Biotropica 11:311–313
Forshaw JM (1989) Parrots of the world. Blandford, London
Gilardi JD, Munn CA (1998) Patterns of activity, flocking, and
habitat use in parrots of the Peruvian Amazon. Condor
100:641–653
Gilardi JD, Duffey SS, Munn CA, Tell LA (1999) Biochemical
functions of geophagy in parrots: detoxification of dietary
toxins and cytoprotection effects. J Chem Ecol 25:897–922
Gochfeld M (1974) Current status and threats to some parrots of the
Lesser Antilles. Biol Conserv 6:184–187
Guix JC, Martin M, Manosa S (1999) Conservation status of parrot
populations in an Atlantic rainforest area of southeastern Brazil.
Biodivers Conserv 8:1079–1088
Kreulen DA (1985) Lick use by large herbivores: a review of
benefits and banes of soil consumption. Mammal Rev 15:107–
123
Marsden SJ, Whiffin M, Sadgrove L (2000) Parrot populations and
habitat use in and around two lowland Atlantic forest reserves,
Brazil. Biol Conserv 96:208–217
McFarland DC (1991) The biology of the ground parrot, Pezoporus
wallicus, in Queensland. Wildl Res 18:168–184
Munn CA (1992) Macaw biology and ecotourism, or “when a bird
in the bush is worth two in the hand.” In: Beissinger SR, Snyder
NFR (eds) New World parrots in crisis: solutions from
conservation biology. Smithsonian Institution Press, Washington, D.C., pp 47–72
Munn CA (1994) Macaws: winged rainbows. Natl Geogr 185:118–
140
Munn CA (1998) Adding value to nature through macaw-oriented
ecotourism. J Am Vet Med Assoc 212:1246–1249
Roth P (1984) Reparticao do habitat entre psitacideros simpaticos
no sul da Amazonia. Acta Amazon 14:175–221
Sokol OM (1971) Lithophagy and geophagy in reptiles. J Herpetol
5:69–71
Terborgh J (1985) Habitat selection in Amazonian birds. In: Cody
ML (ed) Habitat selection in birds. Academic Press, New York,
pp 311–338
Westcott DA, Cockburn A (1988) Flock size and vigilance in
parrots. Aust J Zool 36:335–355
Wilson DE, Sandoval A (1996) Manu: the biodiversity of
Southeastern Peru. Smithsonian Institution, Washington D.C.