acta ethol (2003) 6:2334DOI 10.1007/s10211-003-0080-y

O R I G I NA L ART I C L E

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 ofgeophagy) has been described, there are few behavioraldata on temporal patterns, social interactions, speciesassociations, or reactions to potential predators. Weexamined the behavior of nine species of macaws,parrots, and parakeets at the Machiguenga Ccolpa, a claylick on the Rio Manu, Peru in the dry season. Threedistinct mixed-species groups used the licks: in the earlymorning (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 timesof day as well. The first parrots to begin eating at the lickin the early morning were yellow-crowned parrots(Amazona ochrocephala) and dusky-headed parakeets(Aratinga weddellii), followed by blue-headed parrotsPionus sordidus, and then by mealy (Amazona farinosa)and orange-cheeked (Pionopsitta barrabandi) parrots, andchestnut-fronted macaws (Ara severa). Although blue-headed parrots fed in dense groups of over 50, the othersrarely exceeded 20 individuals. Scarlet macaws (A.macao) sometimes fed alone or joined the early morninggroups, but most associated with a large group of red andgreen macaws (A. chloroptera) that arrived, often scaringoff the smaller birds. On average, about 100 macaws andparrots fed in the early morning, macaw feeding groupsaveraging just over 40, and the parakeets averaged over70. Average time at the lick ranged from 28 min foryellow-crowned parrots to 47 min for tui parakeets. Of the

early morning group, blue-headed and mealy parrots werethe most aggressive and orange-cheeked parrots were theleast aggressive. Red and green macaws were moreaggressive than scarlet macaws; the parakeets wereequally aggressive. All species had more aggressiveinteractions with conspecifics than with other species.Responses to intruders and predators varied by species ofparrot/macaw and type of intruder. In response tointruders or loud calls, responses could be partial (someindividuals flew away, circled, and returned), temporary(all individuals flew away but returned within a fewminutes), or total (all flew away and abandoned feedingfor at least a half hour). The large macaws showed thelowest rate of total abandonment and the parakeetsshowed the highest. People passing up or down river inboats scared birds from the lick. The local residents(Machiguenga tribespeople in boats) elicited a muchgreater response than did the researchers. In the recentpast, macaws and parrots were hunted for food, feathers,and the pet trade, and the birds response, as well as thepresence of parrot and macaw feathers in local villageswe visited, suggests some continued exploitation, or along-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 tropicalregions, including invertebrates, reptiles, birds, andmammals, including humans (Sokol 1971; Arms et al.1974; Emmons and Stark 1979; Kreulen 1985; Abrahamsand Parsons 1996; Gilardi et al. 1999). There are manyhypotheses for why animals eat soil, including mechan-ical enhancement of digestion, mineral supplementation,acid buffering, adsorption of dietary toxins, and gastro-intestinal cytoprotection (Gilardi et al. 1999). Based on acomparison of the chemical composition of selected and

Communicated by R.F. Oliveira

J. Burger ())Division of Life Sciences,Rutgers University,604 Allison Road, Piscataway, NJ 08854-8082, USAe-mail: burger@biology.rutgers.eduTel.: +1-732-4454318Fax: +1-732-4455870

M. GochfeldEnvironmental and Community Medicine,Environmental and Occupational Health Sciences Institute,UMDNJRobert Wood Johnson Medical School,Piscataway, NJ 08854, USA

non-selected clays, and laboratory experiments withparrots, Gilardi et al. (1999) proposed that geophagyprotects the gastrointestinal lining from various biologicaland chemical insults, which allows for greater dietarybreadth during the dry season when foods are scarce.

The range of animals using clay licks and thefrequency of use by some species suggest that eatingclay or earth is very important. Yet, facing a cliff orcoming to a bare expanse of earth potentially exposesanimals to predators. Many animals approach clay licks ina manner that minimizes detection, such as feeding atnight, using licks deep in the forest or partly hidden byvegetation, and coming solitarily. In several parts ofSouth America, parrots and macaws, however, come toclay licks during the day, in large noisy groups, oftenfeeding at licks that are exposed on the banks of riversand streams (Munn 1994). They are thus fully exposed topredators and must interact with the other species comingto feed on the lick at the same time. Competition andpredation might be expected to affect behavior at claylicks, yet this aspect of parrot behavior has not beenexamined in detail.

In this article we examine the temporal patterns,feeding behavior, aggressive interactions, and behavioralresponses to intruders of macaws, parrots, and parakeetsfeeding at clay licks in the Manu National Park in Peru.

We test the following hypotheses:

1. There are no differences among species in the dailypatterns of use of the clay lick.

2. There are no differences in feeding behavior (lag timeto begin feeding, sequence in which species begin tofeed, feeding duration, species associations).

3. There are no species differences in aggression withinor among species.

4. There are no species differences in response tointruders and predators.

Although these are stated as null hypotheses, weexpected, based on prior research, that there would bedifferences in all four because of species differences insize and overall activity patterns (Munn 1992, 1994;Gilardi and Munn 1998; Gilardi et al. 1999). Detailed dataon these four hypotheses were gathered in August 2000.There are many other questions than can be asked aboutbehavior of parrots at clay licks, such as whether speciesdiffer in their competitive ability, whether some birds aredenied access to clay on any given day, and whether theyrequire clay. The objective of this article, however, was toexamine behavior during one season throughout whichpopulation numbers of each species and weather condi-tions were similar to provide basic data on behavior at thelick. Such quantitative data are not presently available,and this is a first step in understanding behavior andcompetition at a clay lick.

Parrots (Psittaciformes) comprise a diverse order ofbirds that occur primarily in Australia, the Neotropics,and in tropical Africa and Asia (Forshaw 1989). Manyparrot species are threatened by capture for local use and

the pet trade, and by widespread habitat destruction(Gochfeld 1974; Butler 1992; Beissinger and Snyder1992; Munn 1992; Casagrande and Beissinger 1997; Guixet al. 1999). The behavior and ecology of many species ofAfrican and Australian parrots have been studied becausethey inhabit open country, many species feed on theground in great numbers, and some are agricultural pests(McFarland 1991; Emison et al. 1994). However, rela-tively little is known about the behavior of most speciesof Neotropical parrots in the wild because they are forestdwelling, 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 conserva-tion of Neotropical parrots that are threatened or endan-gered (see papers in Beissinger and Snyder 1992;Christian et al. 1996a, 1996b; Munn 1998; Marsden etal. 2000), and to those few Neotropical parrots that arecrop pests (Bucher 1992). Gilardi and Munn (1998)studied activity, flocking, and habitat use of parrots in thesame area where we worked. By sitting on observationdecks 2530 m above the forest floor, they found thatparrot and macaw activity peaked just after sunrise, with asecond peak following the mid-day low, except forparakeets, which were active in the early afternoon.Flocks were exclusively monospecific except whenforaging 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 neotrop-ical Amazon parrots, macaws, and parakeets is in contrastto some of the Australian species that sometimes formlarge flocks in grasslands, grainfields, and fruit-growingareas (Westcott and Cockburn 1988). One situation inwhich Neotropical parrots congregate is at clay licks inthe Amazon basin (Munn 1992, 1994). Our studies of thebehavior of macaws, parrots, and parakeets at clay lickscomplement those of Gilardi and Munn (1998).

Methods

We studied the behavior of nine species of macaws, parakeets, andparrots feeding at clay licks, or ccolpas, on the Manu RiverMadre del Dios, Peru during August 2000. The main series oflicks (1148.930S, 7125.400W) is about 1 km upriver fromthe Machiguenga Ccolpa Biological Station (1150.2920S,7125.5460W; Fig. 1). We studied a second lick (1150.3900S,7125.2450W) in a nearby quebrada, or creek, about 500 mupstream from its mouth. The elevation is about 350 m, and the siteis about 12 h by boat (depending on water depth) upriver from thejunction of the Manu and the Alto Madre de Dios Rivers, near thetown of Boca Manu. The licks are the site of the main macawstudies conducted by Munn (1992), who founded the biologicalstation.

The study area is within the Manu National Park, created in1973 as part of the Manu Biosphere Reserve (designated in 1977) toinclude the Manu Reserve Zone and the National Park, covering anarea of 1.5 million hectares. Ecological features are extensivelydescribed in the book Manu (Wilson and Sandoval 1996) and inmany papers cited therein. Our study area was selected because it isabove the tourist zone, reducing the likelihood of human distur-bance and ensuring that the behavior we were observing was notunduly influenced by ecotourists (Munn 1992). Observation blinds

24

were constructed 2 weeks before our arrival to allow time forhabituation.

The main clay area along the river is on a cliff, which at thetime of our visit (low water) was about 912 m high. A skirt ofalmost flat river bank was exposed. The clay lick is thus exposed toa wide expanse of river and is visible from 1 km away. On theterrace above the cliff is mature rain forest dominated by figs(Ficus spp.). At this point the Manu River is about 80100 m wide.The far bank, from which we made some observations, consisted ofa broad sandy beach (inundated after 2 days of rain), backed by adense stand of Tessaria trees and giant cane (Gynerium), behindwhich is low-lying varzea forest dominated by Cecropia trees witha rich flora of palms (Palmaceae), flooded during the rainy season.This is similar to the vegetation studied in greater detail at CochaCashu Biological Station (18 km downriver, Terborgh 1985).

Parrots were observed on the river lick feeding on five exposedcliff faces; other presumably suitable faces were currently coveredwith dense vegetation. The five faces extended over a length ofabout 350 m. Distances between the faces on this lick varied from 8to 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 mwide. It was surrounded by vegetation. The lick was visible only

from about 30 m on either side. Our observation blind was about15 m from the lick.

The species that regularly fed at the clay lick included scarletmacaw (Ara macao), red and green macaw (A. chloroptera),chestnut-fronted macaw (A. severa), dusky-headed parakeet(Aratinga weddellii), tui parakeet (Brotogeris sanctithomia), andorange-cheeked (Pionopsitta barrabandi), blue-headed (Pionussordidus), 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 speciesknown to occur in the area were not observed at the licks during ourvisit. Blue and yellow macaws (Ara ararauna) were seen daily atthe quebrada, but not at the licks during our study, although largenumbers occur at other licks in southeastern Peru. Other speciesthat came to the lick included plumbeous pigeon (Columbaplumbea), speckled chachalaca (Ortalis guttata), and blue-throatedpiping guan (Pipile cumanensis).

Our overall protocol was to observe at the lick from beforedawn (0530 hours) until late afternoon (about 1700 hours). Wealways arrived at the blinds when it was still dark and before anyparrots were in the vicinity and left only after there were no birdsremaining in the area. Observations were made from blinds located

Fig. 1 Temporal patterns ininitiation of feeding bouts at theMachiguenga clay licks inManu National Park, Peru

25

(1) 812 m from the central section of the river lick on the samebank, (2) across the river from the river lick, and (3) across thestream from the quebrada lick. Three or four observers wererequired to watch both licks at the same time and record arrivalsand departures by species and interactions (about 3.5 personmonths). We coordinated our activities among ourselves and withour boatman using walkie-talkies to minimize disturbance to thebirds.

We made four kinds of observations: temporal patterns of lickuse, number of each species feeding at the lick, aggressiveencounters at the lick, and responses to predators and otherintruders. We also recorded when each species arrived in the treesabove the lick. From the close blind at the river, we could not seeall the tree tops, and arrival was noted by identifying vocalizations.

Temporal patterns were recorded by noting the time that thefirst individual of each species landed on the lick to begin feeding,and final departure of all individuals. We defined a feeding bout asthe time between when the first individual landed to feed and thelast one departed, with the lick used relatively continuously duringthat time. We classified departures into three types. In a partialdeparture, most birds left suddenly, but some birds remained andwere rejoined shortly, usually within 15 min. In a temporarydeparture, all birds flew and either circled or landed in nearby treesand returned, usually within 5 min. In a total departure orabandonment, all birds left and none returned to the lick within30 min. In the case of temporary departures, we did not identify theend of the bout until 30 min had elapsed.

We also recorded the number of each species present every 15 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 arbitrarilyanalyzed the data as follows. To examine the number ofheterospecifics present for each species we analyzed the data bynoting how many of each species were present when the number ofany species being examined was the highest for that bout. Forexample, if the maximum count for a given feeding bout foryellow-crowned parrots was 12, we used the number of each otherspecies present the first time 12 was reached as the heterospecificfeeding flock size. The maximum counts for the various speciesusually did not coincide.

Since the number of individuals feeding at the lick variedmarkedly from minute to minute, and it was difficult to record allaggressive interactions when the lick had over 35 individuals, werecorded the number of aggressive interactions observed and thenumber of birds we were observing. We compared aggressionamong species using both a conspecific and heterospecific aggres-sion index. We defined the conspecific index for species A as thetotal number of intraspecific aggression interactions of A/numberof feeding bouts with A presentmean maximum number of speciesA present for all the bouts. We defined the heterospecific index forspecies A as the total number of heterospecific aggressiveinteractions of A/number of feeding bouts of species Ameanmaximum number of all heterospecifics present while species Awas feeding. These two indices provide a comparison for aggres-sion rates among species.

We examined the responses of feeding birds to predators andintruders by recording whether there was no response, partial,temporary, or total departure, following certain visual or acousticstimuli. Many loud noises or sudden appearances of large birdstriggered a departure, often a total departure. By observingsimultaneously from different blinds we increased our likelihoodof identifying intruders. Raptorial birds (most of which are notpotential parrot predators) included hawk eagles (Spizaetus spp.),roadside hawk (Buteo magnitorstris), great black-hawk (Buteogal-lus urubitinga), king vulture (Sarcoramphus papa), black vulture(Coragyps atratus), greater yellow-headed vulture (Cathartesmelambrotus), and black caracara (Daptrius ater). Birds alsoresponded 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-lippedpeccaries (Tayassu pecari) and jaguar (Panthera onca).

The smaller parrots and parakeets responded to the alarm callsand arrivals of the large macaws. We combined the parrots,parakeets, and macaws into three species groups and present thepercentage of times that these three groups partially or temporarilyflew, or abandoned a feeding bout. The groups included very largebirds (scarlet and red and green macaws), intermediate-sized birds(chestnut-fronted macaws and the two amazon parrots, blue-headedand orange-cheeked parrots), and smaller birds (dusky-headed andtui parakeets).

Comparisons among groups were made with analysis ofvariance, followed by Duncan multiple range tests to examinedifferences between groups. We accept a level of significance asP

The pattern of feeding at the licks is illustrated inFig. 2 for parrots and chestnut-fronted macaw for 1 day.In most instances, yellow-crowned parrots landed on thelick first and began to feed before the others. Blue-headedparrots quickly joined them, and a few minutes later, theother species landed. While the number of most speciesrarely exceeded 20, blue-headed parrots fed in muchlarger groups. They usually fed in the same small section

of the lick, often piling on top of one another. Yellow-crowned parrots seemed intimidated by the appearance ofthe mass of blue-crowns and either left or moved to theedges of the lick to continue feeding.

Mean time to start feeding at the clay lick confirms therelationships shown in Fig. 2 (Table 1). Not all speciesstarted feeding at the beginning of the bout, although mostcame down to the lick within about 10 min. Meanduration 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 totaltimes that species visited. That is, each day, each specieswas given a ranking for its order of appearance.

The order of appearance was as follows: yellow-crowned parrots (with the lowest number) usually landedfirst, followed by blue-headed parrots, whereas orange-cheeked parrots were usually last. Since the birds came inthree groups (parrots, parakeets, macaws), the numbersreflect that pattern. Thus, yellow-crowned parrots camefirst for the parrots, the macaws came at about the sametime, and the parakeets alternated which species landedfirst (Table 1).

Species associations

Usually there were fewer than 20 individuals of eachspecies feeding in the early morning group, except forblue-headed parrots (Table 2). The average number ofred and green macaws feeding at the lick was about 35,while there were usually only about 6 scarlet macaws

Fig. 2 Schematic of arrival and feeding durations for parrots andchestnut-fronted macaws at the clay lick along the Manu River.Data based on five bouts where all five species were present andbegan feeding before 0600 hours. Time zero is about 0600

Table 1 Temporal patterns in use of a clay lick in MachiguengaCcolpa clay lick in Manu, Peru (meanSE). Species sharing thesame letter in a column do not differ significantly at P=0.05.

Comparisons are made with KruskalWallis one-way ANOVA,yielding a 2 statistic. Duncan multiple range groupings are givenbelow

Species Bouts(n)

Time of day tostart feeding

Lag time to initiatefeeding after firstspecies fed(min)

Duration offeeding(min)

Order ofappearance

Total numberof parrots andmacaws feeding

Yellow-crowned parrot 36 06:500:07 0.690.33 28.73.28 1.250.09 98.310.5C C B D A, B

Chestnut-fronted macaw 23 6:470:06 9.611.63 32.74.87 3.910.23 11211.5C A B A A

Blue-headed parrot 42 6:590:09 3.520.66 37.73.96 1.980.13 94.79.16C B A, B C A, B, C

Mealy parrot 29 7:010:09 9.341.73 35.04.40 3.410.18 11210.6C A B B A

Orange-cheeked parrot 21 7:040:14 10.52.13 31.54.11 3.710.29 11215.2C A B A, B A

Red and green macaw 45 10:460:22 0.470.13 33.13.48 1.510.09 44.84.23B C B D D

Scarlet macaw 58 10:2600:27 1.830.89 34.53.02 1.550.16 42.14.91B B, C B D D

Dusky-headed parakeet 45 10:310:47 0.580.25 38.53.44 1.380.09 77.27.14B C A, B D B, C

Tui parakeet 40 11:460:44 0.530.26 47.43.55 1.350.12 72.14.83A C A D C

KruskallWallis 2 comparison 176 (0.0001) 178 (0.0001) 17.9 (0.02) 172 (0.0001) 83.6 (0.0001)

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Table2Meannumberof

heterospecificsfeedingat

clay

licksin

Machiguenga

Ccolpa

clay

lick

inManu,

Peru.

Species

sharingthesameletter

inacolumndo

notdiffer

significantlyat

P=0.05.Com

parisons

aremadewithKruskalW

allisone-way

ANOVA,

yielding

a2statistic.Duncanmultiplerangegroupingsaregivenbelow

Species

feedingat

lick

Bouts

(n)

Meannumber

ofconspecifics

Other

species

KruskalW

al-

lis2compari-

son

Yellow

Chestnut

Blue

Mealy

Orange

Red

and

green

Scarlet

Dusky

Tui

Yellow-crownedparrot

3616.62.41

3.811.05

55.16.71

13.62.44

2.440.89

0.060.06

0.110.08

3.111.18

3.441.99

152(0.0001)

CA

BC

CC

CC

Chestnut-frontedmacaw

236.961.36

15.23.37

64.17.04

15.82.94

4.261.26

0.000.00

0.170.12

2.701.60

3.002.41

107(0.0001)

BA

BC

CC

CC

Blue-headed

parrot

4256.55.67

13.32.31

3.620.91

12.62.18

2.690.77

0.100.07

0.290.15

3.291.16

2.381.58

120(0.0001)

AB

AB

BB

BB

Mealy

parrot

2917.32.69

15.73.06

4.661.24

64.26.82

2.520.80

0.070.07

0.340.21

3.831.55

3.452.28

134(0.0001)

BC

AC

CC

CC

Orange-cheekedparrot

215.861.39

13.54.07

5.811.58

65.29.09

13.53.50

0.000.00

0.330.25

5.432.09

2.572.57

85.7

(0.0001)

BB,C

AB

CC

B,C

B,C

Red

andgreenmacaw

4535.83.59

0.130.13

0.130.13

1.271.03

0.930.85

0.040.04

6.420.81

0.000.00

0.000.00

248(0.0001)

BB

BB

BA

BB

Scarlet

macaw

585.790.64

0.660.53

0.600.40

0.600.40

0.980.68

0.100.06

26.73.46

0.000.00

0.000.00

196(0.0001)

CC

BC

CA

CC

Dusky

parakeet

4513.51.26

3.241.69

1.020.64

14.05.11

1.560.72

1.090.56

0.000.00

0.360.17

42.45.60

96.3

(0.0001)

CC

BC

CC

CA

Tui

parakeet

4058.94.13

0.600.47

0.150.15

1.001.00

0.580.58

0.080.08

0.000.00

0.300.17

10.51.53

172(0.0001)

BB

BB

BB

BA

28

with them. Dusky-headed parakeets usually fed in smallgroups of less than 20, whereas tui parakeets fed inlarger groups of nearly 60 (Table 2). Figure 3 shows thefrequency distribution of the maximum number presentfor each clay-feeding bout. Although the mean for themaximum number of individuals present gives anindication of central tendency, it does not adequatelydescribe the variation in the maximum number that fedeach day.

The heterospecifics feeding with each species areshown in Table 2. There are differences in the speciescomposition because of the temporal pattern of feeding at

clay licks. It is clear from this table that some species (tuiparakeet) rarely fed with other species, while the parrotsalways fed with other species.

Even at the river lick, they did not use the five facesequally (Table 3). Only the parakeets used the firstsection, and they mainly used the first and second sectionsand did not come to the central faces. Similarly only themacaws used the fifth section.

Fig. 3 Frequency distributionof the maximum number ofeach species feeding at the claylick. Shown are percentages foreach feeding group size

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Aggressive interactions

The feeding assemblages of macaws, parrots, and para-keets at clay licks are very dynamic, with frequent shiftsin the species composition, the number of birds present,and the relative proportion of different species. The largenumbers of birds at the lick resulted in displacements asbirds tried to land; there were also deliberate displace-ments, lunges, and fights with others on the lick. Ingeneral, birds landed near conspecifics and defendedspace against them, often supplanting them. The conspe-cific aggression index was higher for each species thanthe heterospecific aggression index (Table 4). There werealso differences in the index among species: (1) in theearly-morning feeding group, blue-headed parrots werethe most aggressive, followed by mealy parrots; (2) redand green macaws were more aggressive than scarletmacaws; and (3) the two parakeets had similar aggressionindices (Table 4). The heterospecific index mirrored the

conspecific index; blue-headed parrots and red and greenmacaws were also aggressive toward other species;yellow-crowned parrots and orange-cheeked parrots werenot very aggressive toward conspecifics or towardheterospecifics (Table 4).

Responses to intruders and predators

Because clay licks are visible, birds feeding at a clay lickare vulnerable to disturbances from intruders and preda-tors. The birds were generally very wary. The responsepattern varied among the species (Table 5). Possibleresponses included no change in behavior, flight of some

Table 4 Aggression indices for species of parrots, macaws, andparakeets feeding at a riverine clay lick in Manu, Peru. Index Totalaggressive encounters/number of boutsmean number present

Conspecificindex

Heterospecificindex

Early-morning group

Yellow-crowned parrot 0.065 0.006Blue-headed parrot 0.391 0.063Mealy parrot 0.204 0.021Chestnut-fronted macaw 0.037 0.003Orange-cheeked parrot 0.022 0.0009

Mid-morning group

Red and green macaw 0.516 0.317Scarlet macaw 0.19 0.028

Early-afternoon group

Dusky-headed parakeet 0.082 0.002Tui parakeet 0.11 0.003

Table 5 Response of macaws, parrots, and parakeets to intruders and disturbances at a clay lick in Manu, Peru. Given is percent of boutsthe birds partially or permanently abandoned the lick (the remaining time they stayed)

Disturbance Large macaws Intermediate macaws and parrots Parakeets

Bouts(n)

Partial ortemporary%

Abandoned%

Bouts(n)

Partial ortemporary%

Abandoned%

Bouts(n)

Partial ortemporary%

Abandoned%

Raptor

Large hawks/eagles 28 54 38 33 33 55 24 17 83Roadside hawk 13 0 0 22 0 0 12 58 25Black vulture 8 25 50 20 20 60 10 10 80King vulture 4 100 0 8 0 100 10 0 100Black caracara 14 14 14 23 26 70 26 19 79

Macaw/parrots

Large macaw call 79 66 28 65 54 46Large macaw land 89 21 79 53 13 87Small macaw call 50 26 18 Blue-headed landa 26 65 196 Oropendola callb 6 16 0 46 50 35 14 43 57Monkeys 55 60 25 56 45 55 27 18 82White-lipped peccaries 33 58 30 56 38 59 25 20 80Jaguar 6 33 66 21 5 95 6 0 100Machiguenga 28 36 64 49 12 88 18 6 94Researchers 16 13 0 18 22 0 19 26 11

a Over 25 landing at onceb Loud social calls and alarm calls

Table 3 Use of different faces of the river lick, given as percents ofbouts for each species on each face

River Licks

1 2 3 4 5

Yellow-crowned Parrot 29% 46% 25%Chestnut-fronted macaw 25% 50% 25%Blue-headed parrot 29% 50% 21%Mealy parrot 30% 50% 20%Orange-cheeked parrot 11% 67% 22%Scarlet macaw 7% 34% 37% 22%Red and green macaw 14% 27% 32% 27%Tui parakeet 47% 53%

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individuals from the lick temporarily (partial), flight of allindividuals from the lick temporarily (temporary), orpermanent flight of all the individuals from the lick,ending the feeding bout (total abandonment). At timeseach of these responses occurred when we could notdetect or find the apparent stimulus. Therefore, werecorded behavior when an intruder or potential predatorwas visible from the clay lick or when there was anaudible sound. Responses varied depending upon both thespecies of macaws, parrots, and parakeets, and the type ofintruder (Table 5). Overall, large macaws reacted theleast, and parakeets reactions were the strongest (Fig. 4),although they also returned most quickly. A jaguargrunting and the local inhabitants (Machiguenga tribe),in boats, elicited the strongest responses from all threegroups, 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) elicitedsome responses from the parrots and parakeets, and thecalls of large macaws elicited some responses from theother species, even if they were feeding at a lick 100 maway.

The response to people bears comment. Usually people(Machiguenga and researchers) went by the lick in boatsand did not stop. Although researchers mainly usedmotorized boats with a sun cover, they did not always doso, and sometimes they used local motorized boats similarto those used by the Machiguenga and other local peoplepassing up and down the river. The local tribespeople who

lived about 6 km upriver sometimes passed by in non-motorized canoes. The macaws, parrots, and parakeetsnonetheless responded differently regardless of the sim-ilar-looking boats. While the researchers usually movedalong the middle of the river, or were closer to the claylick, the Machiguenga usually went in the center ortoward the opposite side (near the sand bar where theycould look for turtle eggs). The greatest response, loudcalling and flying around, followed by complete aban-donment of the lick and all the trees in the vicinity,occurred when a boat of five Machiguenga stopped on amudflat across from the clay lick, and the peopledisembarked to hunt for turtle eggs. When a similarboatload of researchers landed, the birds were onlytemporarily disturbed and returned to feeding on the lick.Both groups of people were generally silent, and the noiselevel did not appear to vary between groups.

Discussion

Competition

The daily patterns in use of the clay licks were consistentfrom day to day during the observation period. Therewere three main groups feeding at the licks. Parrots andchestnut-fronted macaws fed in the early morning just atdaybreak, the large macaws (scarlet, red and green) fedmainly in mid and late morning, and the parakeets fedmainly in the early afternoon. In addition, the degree ofconsistency varied among these three groups. The speciesfeeding in the early morning did not come to the licks tofeed at other times of the day. The parakeets came and fedat the lick at nearly all times of the day but did not remainin the vicinity except when feeding. The large macawsnormally fed in the late morning but came at other timesof the day to feed at the lick and often remained in thetrees above the lick for much of the day.

We attribute these differences in behavior to differ-ences in overall activity patterns, interactions among thespecies, and antipredator behavior (see below). Gilardiand Munn (1998) studied the activity patterns andflocking behavior of this same group of macaws, parrots,and parakeets in the same region and found that parrotsand macaws were active just after sunrise, with anotherpeak after the mid-day lull, although the parakeets wereactive in the early afternoon. Activity, defined as flightover the forest, was highest from about 0630 until0900 hours. These patterns are consistent with thepatterns of feeding at clay licks observed in this dryseason study.

Gilardi and Munns (1998) observations, and ours,suggest that the parrots and chestnut-fronted macawscame to the lick at the early part of their activity and thenleft to forage for fruits and seeds. Similarly, the dusky-headed parakeets came to feed at the clay lick in the earlypart of their most active period and flew over the forest tosearch for food afterward. The large macaws, on the otherhand, came to the lick at least 1.5 h after dawn and were

Fig. 4 Percent of times each group totally abandoned the feedingbout because of interactions with different intruders and predators.Large macaws include scarlet, and red and green; parrots includechestnut-fronted macaw and the parrots; parakeets include tui anddusky-headed. *P

presumably foraging for food in the early part of theiractivity pattern, prior to coming to the lick. Some scarletmacaws were exceptions in that they fed in the early tomid morning, sometimes with the parrots and sometimesby themselves. They never came, however, right atsunrise.

The social nature of the lick was exemplified by theuse of only one of the five faces at any given time. Thebirds, particularly the large macaws, seemed to take timeto decide which face to use for a given bout. However,once one bird landed on a lick, others joined in. Almostnever were two faces in use at the same time. When twofaces were used, it was usually by two different speciesgroups (i.e. macaws at one, parakeets at the other).

Only the macaws seemed to use the clay lick area as asocial gathering place. Once they arrived, usually in pairs,they spent more time preening and calling before theycame down to feed on the clay, and they frequentlyremained in the treetops for much of the rest of the day.Pairs slept, preened, or simply remained vigilant untilthey departed in the late afternoon. This phase wasvariable in that on some days many remained near theclay lick, on others few remained, and on a very few daysthey all departed by early afternoon. Such departures,however, were often preceded by the appearance of eaglesor Machiguenga in boats. We usually waited to call ourboat to get us until there were few macaws in the treesoverhead. However, when the boat came for us, the fewremaining macaws would call loudly, sometimes circlingover the river, but usually did not abandon the area.

When present, the large macaws seemed to dominatethe clay lick by their size, as is evident by the percent oftimes the other species abandoned the clay lick for the dayif the large macaws landed at the lick. Abandonment byparrots often occurred when the macaws began to increasetheir calling rate from the trees over the lick as a preludeto descending. It usually occurred as soon as one of thelarge macaws landed on branches or vines above the lick,and always occurred if more then two macaws landed onthe clay cliffs.

Size was not the only factor affecting behavior at thelick. Aggression and numbers also influenced bothfeeding at the lick and location of feeding. The largestspecies was not always the most aggressive. For example,blue-headed parrots were smaller than several of the otherspecies that they fed with, yet they were the most freneticand aggressive. Within feeding associations (the threetypes of feeding groups), the most aggressive speciesusually had primary access to the best clay-eating places.

In the early-morning group, blue-headed parrots werethe most aggressive toward both conspecifics and het-erospecifics, 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 twolarge macaws, the larger red and green were moreaggressive than scarlet macaws, and they overwhelmedthem by numbers as well. The parakeets were similarlyaggressive, and there was no clear pattern in displace-ments. Individuals were primarily aggressive toward

conspecifics, which seemed to us to result from theirpattern of landing near conspecifics.

In addition to size and aggressiveness, density was afactor. Blue-headed parrots showed great tolerance forbeing in contact with conspecifics. Yellow-crownedparrots were often displaced from the preferred placesby the mass of landing blue-headed parrots and moved offto the side. Even when blue-headed parrots landed awayfrom the main group, they quickly moved over to themain group of blue-headed parrots, forcing others away.Sometimes they even climbed on top of one another, andboth the one on top and the one underneath continued tofeed. Yellow-crowns, mealys, and orange-cheeked parrotsquickly moved away from these dense groups of blue-headed parrots. Other factors, such as conspecific groupsize, could have played a role.

Moreover, where they landed was not only a functionof 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. Forexample, when other yellow-crowned parrots came to thelick, they joined conspecifics already there, even thoughthere were other unoccupied places on the lick. Thishappened with all the other species that fed with the blue-headed parrots. The blue-headed parrots, by virtue of theirnumbers and crowding, simply forced all other species tothe edge. The only exception to this pattern was when ascarlet macaw landed and moved toward the blue-headedparrots. Even then, however, one macaw seldom dis-placed the dense mass of blue-headed parrots. Thisphenomenon has also been shown for gulls feeding at agarbage dump, where the smaller laughing gull (Larusatricilla) 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 aplace to land and feed (Burger and Gochfeld 1984).

The much smaller parakeets dealt with competitionfrom the larger species by either abandoning feeding atthe lick when larger species arrived, moving to the edges(leaving a meter between them and the larger species), orusing a lick not preferred by the other species. Theymoved to the edges when confronted by parrots orchestnut-fronted macaws and left completely or used adifferent lick when confronted by the large macaws(scarlet, red and green). Avoiding interactions with largerspecies is not an unusual pattern, and having access todifferent food items (or in this case clay) is often achievedpartly on the basis of size and weight (Roth 1984).

Antipredator behavior

Macaws, parrots, and parakeets feeding at clay licks arevulnerable to disturbance and to predation because manyof the clay licks are on major rivers used for transporta-tion by people and the openness of the river makes themvisible for some distance. In addition, they are often quitenoisy while feeding on the lick. Birds waiting in the treesare particularly noisy. These characteristics ensure that

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they would be detected by predators or people seeking tocapture them. While feeding on the lick itself they arevulnerable to raptors, particularly birds that can capturethem in flight. One of the advantages of having birds inthe trees that are waiting to take their turn at the lick isthat these can be vigilant and warn of impending danger.While parrots regularly expose themselves to predators onthe bare branches of trees, these sites are not as wellknown, and usually far fewer gather at any one point. Theclay licks are presumably known to predators.

The response of the birds to intruders and potentialpredators varied by the species of macaw, parrot, orparakeet, and by the species of predator. Westcott andCockburn (1988) found that vigilance in Australianparrots increased with the potential risk from predators.In our study, antipredator responses also were strongest(total abandonment of the lick) to the predators presentingthe greatest risk. The strongest responses were to someraptors, jaguars, and Machiguenga. Some of the raptorsare 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 andsmall motorized boats. It was not merely the presence of aboat that disturbed them because the birds rarelyresponded severely to researchers in boats. Althoughcapture of the macaws, parrots, and parakeets is illegaland is discouraged by the park personnel, the nativepeoples are allowed to capture wild birds and other gamefor subsistence and cultural uses. We observedMachiguenga hunting for turtle eggs (also discouraged)and saw macaw and parrot feathers in local villages.Further, even if there was currently no exploitation by theMachiguenga and other local people, macaws and parrotsare long-lived and would likely remember encounters thatoccurred more than a decade ago. Munn (1992) hassuggested that parrot licks may well be protected byhaving the local communities deriving revenues fromproviding tourist opportunities.

The responses to intruders and predators varied amongthe macaws, parrots, and parakeets, mainly as a functionof body size. The larger macaws responded less severelyand rarely abandoned feeding at the clay lick completelywhen there was no clear and significant threat, whereasthe parakeets often abandoned a feeding bout when facedwith raptors and mammals. The parakeets respondedmore frequently to the warning calls of the oropendolasthan did the other species. The parrots were generallyintermediate in their response. The differences in re-sponses were no doubt due to the very real threat ofpredation; the smaller species were more vulnerable topredators, although they were probably less vulnerable tocapture by humans.

Conservation implications

Since macaws, parrots, and even parakeets are vulnerableto a wide range of exploitation by humans (see papers in

Beissinger and Snyder 1992), it is important to understandthe behavior and ecology of their entire life cycles to aidin conservation. The relative importance of feeding onclay for these species (Gilardi et al. 1999) forces the birdsto seek out licks even though they are exposed. Not alllicks are equally exposed, and the birds can go to a nearbylick when disturbed. Although we did not have markedbirds, we communicated with walkie-talkies and kepttrack of the exact time birds arrived and left both the riverand quebrada lick. On several occasions, birds thatabandoned the river lick because of the presence ofeagles, jaguars, or Machiguenga appeared at the creeklick (the same species and relative composition). Al-though not conclusive, this is suggestive of using severallicks within the same region.

The differential response to researchers and Machi-guenga suggests that these birds clearly distinguish differ-ent people and confirms that some observation by people ispossible without unduly disturbing the birds. Indeed, thereare several places where lodges provide viewing opportu-nities for tourists from blinds located on rivers across fromclay licks. Our observations, however, confirm that thebirds habituate and can distinguish different humanactivities. Ecotourism is an important conservation toolfor preserving parrots, particularly when such moniesenrich the local and regional inhabitants (Munn 1992).

Finally, our observation of the small clay lick along thecreek suggests that some habitat modification may bepossible to create additional licks so that there are optionsfor birds when they are disturbed from one lick. At theend of our field work we removed some vegetation fromin front of one section of the main riverine lick (forphotographic purposes) and found that the large macawsimmediately moved to this new area and fed there,suggesting some limitation in good clay lick faces. Ouractions opened an area where the preferred clay layer wasstill relatively soft and easy to break off, and where therewere sufficient vines for easy access to the lick. The vinesprovided places for macaws waiting their turn to cling. Insome regions, there may be few clay licks, and creatingother licks may prove useful.

Acknowledgments The authors wish to thank Wilfredo ArizabalArriaga (Willie) for serving as our guide and field assistant,Faustino Fernandez, Alberto Flores, and Miguel Palacio for fieldassistance, Kit Herring and the U.S. and Peruvian staffs ofInkanatura for logistical arrangements and provision of a well-trained field staff. We are particularly indebted to C.A. Munn forsetting us up in his field station and providing information on theparrots and local people. We thank the Peruvian government andthe Manu National Park for permits for work in the restricted areaof the park and for providing advice while at the station.

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