Table Of ContentWilson Bulletin, 1 16(2), 2004, pp. 134-145
EFFECTS OF WEATHER ON PARROT GEOPHAGY IN
TAMBOPATA, PERU
DONALD BRIGHTSMITH'
J.
—
ABSTRACT. Geophagy is widespread and well documented for mammals, but avian geophagy has only
recently become the subjectofserious scientific investigation. I analyzeddatafrom606morningsofobservations
at a large avian geophagy site or “clay lick” in the southwestern Amazon Basin to examine the effects of
weather on bird lick use. Birds used the clay lick on 94% ofthe mornings without precipitation or fog. Parrots
dominated the site in both numbers of species (17) and individuals (>99%). Weather conditions were signifi-
cantly correlated with total lick use: there was greater use on sunny mornings and less on rainy mornings. Fog
and overnight rain were correlated with low lick use. Sun, rain, fog, and overnight rain were recorded on 47,
25, 20, and 8% ofthe mornings, respectively. I estimatedthat inclement weathercausedan annual 29% reduction
in geophagy forall bird species combined. When early morning rain prevented species from using the lick, they
did not return later in the day nor did they compensate for rainy mornings by increasing lick use on subsequent
days. The timing of lick use and the lack ofcompensation suggest that neutralization oftoxins could be driving
lick use in this system. Received 25 August 2003, accepted 26 May 2004.
Geophagy, the intentional consumption of parrots (Psittaciformes), which gather by the
soil, is widespread among vertebrate and in- hundreds to consume clay-rich soils from riv-
vertebrate taxa including mammals, birds, rep- erbank sites in South America (Emmons and
tiles, and insects (Sokol 1971, Arms et al. Stark 1979, Gilardi et al. 1999, Burger and
1974, Davies and Baillie 1988, Benkman Gochfeld 2003, Brightsmith and Aramburu in
1992, Smedley and Eisner 1996). Geophagy press). The soils from these “clay licks” ap-
occurs on all continents (except Antarctica) parently provide an important source of so-
and is particularly well documented for mam- dium and protection against dietary toxins
mals, including humans and other primates (Diamond et al. 1999, Gilardi et al. 1999,
(Jones and Hanson 1985, Abrahams and Par- Brightsmith and Aramburu in press). These
sons 1996, Klaus and Schmidt 1998, Wiley soils likely permit geophagous species to ex-
and Katz 1998, Krishnamani and Mahaney ploit a wider range of plant resources and al-
2000). Recent studies of avian geophagy in low the high diversity and density of parrots
tropical areas have focused on soil chemistry, found in the western Amazon basin (Diamond
physiology, or short-term observations of be- et al. 1999). However, geophagy is not prac-
havior (Diamond et al. 1999, Gilardi et al. ticed by all psittacids. This variation in geo-
1999, Burger and Gochfeld 2003, Brightsmith phagous behavior within locations over time
and Aramburu in press). Long-term studies of and between locations provides an opportunity
geophagy sites are lacking and this hinders to explore the ecological role of geophagy.
our ability to understand the ecological role Weather is known to have strong effects on
and relative importance of this phenomenon. bird survival and behavior (Sillett et al. 2000,
Here, I document the effects of weather on Takagi 2001, Winkler et al. 2002, Cougill and
avian geophagy in a lowland tropical forest Marsden 2004). Rain and lower temperatures
over a 3-year period.
cause short-term increases in nutritional stress
Geophagy is known for members ofthe avi- for birds and often reduce the frequency of
an orders Anseriformes, Columbiformes, Pas-
behaviors not critical to immediate survival,
seriformes, Casuariiformes, Galliformes, and
including song, migration, communal roost-
Psittaciformes (Jones and Hanson 1985,
Benkman 1992, Wink et al. 1993, Diamond et Linegn,gaangdneflaynidngS(lPaytelre 2e0t0a2l,. L1o9p9e3,z-KCealalsetja19a9n4d,
al. 1999, Keppie and Braun 2000). Of these, Bozinovic 2003, Cougill and Marsden 2004).
the most conspicuous and well studied are the
However, rain and lower temperatures often
cause an increase in foraging, a behavior
' Duke Univ., Dept, ofBiology, Durham, NC 27708, needed for short-term survival (Einney et al.
USA; e-mail: [email protected] 1999, Fischer and Griffin 2000, Dewasmes et
134
Brightsmith • WEATHER EEFECTS ON AVIAN GEOPHAGY 135
al. 2001). I hypothesized that inclement the data >2 days (63 of93 months). The mean
weather (rain and fog) would decrease lick use rainfall for each month of each year was used
and that birds would compensate for this de- to calculate the overall monthly mean and
crease by using the lick more afterthe weather standard deviation (e.g., the data from January
cleared. of each year was averaged to provide a com-
posite rainfall for January). Data collected
METHODS
during the El Nino Southern Oscillation of
—
Study area. I studied avian geophagy at a December 1997 to June 1998 were omitted
clay lick near the Tambopata Research Center due to the highly irregular patterns of rainfall
(13° 08' S, 69° 37' W) in southeastern Peru. that typically occur during such events. The
The center is on the border of the Tambopata average annual rainfall total was calculated by
National Reserve (275,000 ha) and the Ba- summing the means for each month. Data on
huaja-Sonene National Park (537,000 ha) in the timing and duration, but not intensity of
the department of Madre de Dios. The center rain, fog, and insolation, were collected during
lies at the boundary between tropical moist observations of the clay lick (see Bird data
and subtropical wet forest at an elevation of below).
250 m and receives 3,200 mm ofrain per year Bird data.—Observers recorded bird use at
(Tosi 1960; this paper). The research center is the clay lick on 606 mornings from 12 Janu-
located in a small (<1 ha) clearing surrounded ary 2000 to 16 November 2002. Observers be-
by mature floodplain forest, successional gan watching the lick before the birds arrived
floodplain forest, Mauritia fiexuosa (Areca- (approximately at sunrise) until the birds hn-
ceae) palm swamp, and upland forest (Foster ished their early morning lick use (usually be-
et al. 1994). A large patch of bamboo {Guad- fore 07:30 EST). On 280 occasions, observers
Lia sarcocarpa', Poaceae) covered the area im- conducted full-day observations (sunrise until
mediately adjacent to the clay lick, but this 16:00—17:30), but only early morning data are
patch flowered and died in 2001-2002 (Foster reported here. Every 5 min, observers record-
et al. 1994, Griscom and Ashton 2003, DJB ed the weather as rain (rain falling on the ob-
pers. obs.). The clay lick is a 500-m long, 25- server), sun (sun hitting the ground anywhere
to 30-m high bank along the western edge of in the vicinity of the clay lick), or cloud (if
the upper Tambopata River, approximately neither of the others applied). We also noted
300 m from the research center. The cliff is the presence or absence of fog. Observers re-
I formed by the Tambopata River’s erosion of corded the time, number, and species of the
uplifted. Tertiary-age alluvial sediments (Ras- first birds that landed on the lick. Starting
iinen and wSalo 1990, Foster et al. 1994, Ras- from this point, observers counted all birds on
iinen and Linna 1995). The soils of the lick the lick every 5 min using binoculars and a
are rich in clay with high cation exchange ca- spotting scope (20-60X zoom). Ob.servers
pacity and high sodium levels (Gilardi et al. could readily distinguish all of the common
1999, D.IB Linpubl. data). bird species on the lick except the two, small,
—
Weather data. From June 1995 through green macaws: Chestnut-frontetl Macaw {Am
February 2003, researchers at the site record- severa) and Red-bellied Macaw {Orthopsitta-
ed weather data. Daily maximum and mini- ca luandata). For this study, these tv\o species
mum temperatures were taken from a mercury are lumped together and analyzed as “green
max-min thermometer located in the understo- macaws.” —
ry of primary floodplain forest approximately Data anidysis. I analyzed the correlation
20 111 from the forest edge. Rain data were between weather variables, month, and lick
collected using a standard rain gauge in a use using a t|uasi-likelihood general linear re-
II clearing approximately 30 in from the forest gression (e.g., a Poisson regression with ov-
edge. Observers recorded the approximate ertlispersion; Agresti 2002). This type ofmod-
^
time of rainfall on all days, even when not el was needed because the binls traveled in
observing the clay lick. We did not collect flocks and descended to the lick en masse,
weather data every day and gaps of day to causing the \ariancc in daily lick use to be
I
>1 month occurred. calculatetl mean rainfall greater than the mean. The main elfects in-
I
for all months in which there were no gaps in cluiled in the analysis were year, month.
136 THE WILSON BULLETIN • Vol. 116, No. 2, June 2004
weather index, rain the night before, fog, daily minimum temperature was highly correlated
minimum temperature, daily maximum tem- with the coefficient of fog (Pearson product-
perature, lick use the day before, the number moment correlation = 0.998) and the inclu-
of days since the lick was used, and two-way sion of the interaction term caused both fog
interaction terms. The dependent variable was and the interaction to become nonsignificant,
lick use measured in bird minutes. Bird min- so this interaction term was removed from the
utes were dehned as the number of birds on analysis. This procedure was repeated using
the lick multiplied by the number of minutes lick use for each individual species as the de-
they stayed on the lick (i.e., 4 birds for 15 pendent variable. Means are reported ± SD.
min each = 60 bird min). The weather index To measure potential lick use, for each
was a composite variable based on the obser- month I calculated daily average lick use for
vations of sun, cloud, and rain recorded every each species using data only from “fair
5 min during observations. It was calculated weather” mornings (i.e., mornings with no
as the average for each morning with sun = fog, rain, or rain the night before). To measure
1, cloud = 2, and rain = 3. Rain the night actual lick use, for each month I calculated
before was recorded as present if rain fell be- daily average lick use for each species using
tween 20:00 and 04:00. The variable “fog” data from all days regardless of weather. For
used in the model was the sum of the number actual lick use, 1 included mornings with con-
of 5-min intervals in which fog was recorded tinuous heavy rain when the observers did not
during each morning observation. “Lick use go to the lick and assumed that total lick use
the day before” was the number of bird min- was zero. The total reduction in lick use due
utes oflick use recorded on the preceding day. to weather was estimated by the following for-
The “number ofdays since the lick was used” mula: (potential lick use — actual lick use)/
was the number of days since birds used the potential lick use.
lick. I considered the lick used by birds on a
RESULTS
given morning ifthe total numberofbird min-
utes recorded was >10% of the average for A total of 28 species of birds ate soil from
that month. For the calculation of lick use the the lick (Table 1). Parrots dominated the site,
day before and number of days since the lick both in number of species (n = 17) and num-
was used, I assumed that total lick use was ber of observations (>99%). Thirteen species
zero for days when heavy rain all morning used the lick regularly in the early mornings
prevented the observers from going to the (before 07:30) and are included in the analy-
lick. This assumption is justified because on ses presented here. The remaining species
12 mornings, where rain was recorded >80% were either too uncommon to include in the
of the time, total lick use averaged only 39 ± analysis (n = 1 1) or did not use the lick in
107 bird min (SD) or 1.3% of the lick use for the early morning (n = 4). Of the 13 species
fair weather days (mean/,,,,,,,,,,;,,,,/,,,, = 3051 ± that used the lick in the early morning, 4 also
2465 SD, nf^,irnea,herJays = 386). used the lick in the late morning and afternoon
The hrst regression analysis included all (Table 1): Blue-throated Piping-Guan {Pipile
variables. Then I excluded all variables that cumanensis), Blue-and-yellow Macaw {Ara
did not contribute significantly to the model araraima). Scarlet Macaw (A. macao), and
and reran the analysis. Finally, I ran a separate Red-and-gre—en Macaw (A. chloroptera).
analysis on each of the excluded variables to Weather. The average annual rainfall at
determine whether any of them contributed Tambopata Research Center was 3,236 mm.
significantly to the model (Pyle et al. 1993). Monthly mean rainfall ranged from 95 ± 57.7
The daily maximum temperature was corre- mm in August (n — 6 years) to 528 ± 172.4
lated with both the daily minimum tempera- mm in January (n = 7 years). The months of
ture (Pearson product-moment correlation = July and August were the only two in which
0.45) and the weather index (Pearson product- mean rainfall fell below the estimated poten-
moment correlation = —0.35), and it ex- tial evapotranspiration (Fig. 1). Rain events of
plained less variation than either of the other >1 mm were recorded on 42% of the days
two, so it was eliminated from the analysis. (709 of 1,679 days). The number ofdays with
The interaction coefficient of fog by daily rain was greatest in January (mean = 18 ±
Brightsmith • WEATHER EEEECTS ON AVIAN GEOPHAGY 137
TABLE 1. Species recorded eating soil from the clay lick at Tambopata Research Center in southeastern
Peru, 12 January 2000-16 November 2002. Abundances are given as C (common, seen during >15% of the
observations), U (uncommon, seen <75% and >25%), R (rare, seen <25% and ^5%), or O (occasional, seen
during <5% of the observations). Eor species listed as occasional, the number of times seen is reported in
parentheses.
Timeofday
Abundance
Before07:30 07:30-12:00 After 12:00 atlick
Species analyzed in this paper
Blue-and-yellow Macaw {Ara araraima) X X X c
Scarlet Macaw {Ara macao) X X X c
Red-and-green Macaw {Ara chloroptera) X X X c
Chestnut-fronted Macaw {Ara severa) X c
Red-bellied Macaw {Orthopsittaca manilata) X c
White-bellied Parakeet {Aratinga leucophthalmus) X u
Dusky-headed Parakeet {Aratinga weddellii) X u
White-bellied Parrot {Pioiiites leucogaster) X X u
Orange-cheeked Parrot {Pionopsitta barrabandi) X u
Blue-headed Parrot {Pionus menstriiiis) X c
Yellow-crowned Parrot {Aniazona ochrocephala) X u
Mealy Parrot {Amazonafarinosa) X c
Blue-throated Piping-Guan {Pipile cumanensis) X X X u
Additional species recorded at the lick
Speckled Chachalaca {Ortalis guttata) X X X R
Spix’s Guan {Penelopejacquacu) X X X R
Orange-breasted Falcon {Falco deiroleucus) X o (1)
Plumbeous Pigeon {Patagioenasplumbea) X X u
Pale-vented Pigeon {Patagioenas cayennensis) X X u
Ruddy Pigeon {Patagioenas subvinacea) X X u
Blue-headed Macaw {Primolius couloni) X R
Dusky-billed Parrotlet {Forpus sclateri) X X R
Amazonian Parrotlet {Nannopsittaca dachilleae) X X O (9)
Tui Parakeet {Brotogeris sanctithomae) X X 0(1)
Cobalt-winged Parakeet {Brotogeris cyanoptera) X X U
GPrurapyl-ifsrhonJtaeyd{DCoyvaeno{cLoerpatoxticlyaanroufmaexliallsa)) XX XX Oo ((24))
Blue-gray Tanager {Thraiipis episcopiis) X X O (4)
Crested Oropendola {Psarocolius decumanus) X O (2)
4.1 days, n = 1 years) and least in August The variables month, weather index, fog, and
(mean = 5.5 ± 2.6 days, n = 6 years). The rain the night before explained 47% {P <
mean temperature was 24.3 ± 1.4° C. Early O.OOl) of the variation in total lick use lablc
(
morning fog was recorded on 20% of the days 2). As weather progressed from sunny to
(// = 606). Rain was recorded during 12% of cloudy to rainy, and fog duration increased,
the observations (// = 606). It rained the pre- total lick use decreased, explaining 7% of the
vious night during 8% of the observations (// variation in the data (/^ < O.OOl; Table 2).
= 510); there was no rain or fog of any sort Birds used the lick less on early mornings fol-
for 76% of the ob.servations (// = 510). On 80 lowing rain the j')re\ious night (P < 0.05; Pa-
days there was heavy rain during the early ble 2). Month exidained yPA of the variation
I
I morning (and observers did not go to the lick in total lick use (P 0.001; fable 2): mean
on these days). daily lick use rangeil from 4.784 2,387 bird
—
Weather effects on geophagy. Birds used min in August to 257 378 biril min in May
the clay lick on 04% of the fair weather morn- d ig. 2).
ings (i.e., without rain or fog during the ob- When each taxon was analyzed separately,
servatiofi or rain the night before, // 386). liek use was negatively eorrelated uith ueath-
138 THE WILSON BULLETIN • Voi IJ6, No. 2. June 2004
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Month
FIG. I. Mean monthly temperature, rainfall, andestimatedevapotranspiration atTambopataResearchCenter,
Peru, June 1995 through February 2003. Evapotranspiration was estimated following Holdridge (1967).
TABLE 2. Quasi-likelihood general linear regression model (Poisson regression with overdispersion) of
weatherand month affecting lick use by birds in Tambopata. Peru, 12 January 2000-16 November2002. Values
are presented forcombined lick use by 13 species and as the percent deviance explained (regressioncoefficient).
Coefficients with negative values indicate that birds used the lick less as the value ofthe independent variable
increased. A single coefficient cannot be calculated for the categorical variable month, and so is not reported.
The model uses the chi-squared-based analysis-of-deviance test. The overall model is significant at P < 0.001.
Variable Deviance(regressioncoefficient)
Month 39%-*****
Weather index 4% (-0.36) ***
Fog 3% (-0.038)***
Rained night before 1% (-0.32)*
Year NS*’
Birds yesterday NS
Days since used*-' NS
Daily minimum temperature NS
Month:weather^ NS
Monthifog*' NS
Daily minimumiweather index*' NS
Total df 509
Total deviance 229,190
Deviance explained 47%
“*P<0.05.**p<0.01.***P<0.001.
'’NS = notsignificant(P>0.05).
Dayssinceusedisameasureofhowmanymorningshadelapsedsincethelickhadbeenusedbybirds.
Variablesseparatedbyacolonindicateinteractions.
Brightsmith • WEATHER EEEECTS ON AVIAN GEOPHAGY 139
9000
Allobservations
8000 Fairweatheronly
7000
6000
c0/)
D 5000
c
E
-D 4000
1—
CD
3000
2000
1000
0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Month
EIG. 2. Mean daily lick use (bird min) by month for all mornings (white bars) and fair weather mornings
(black bars) at a clay lick in Tambopata, Peru, 12 January 2000-16 November 2002. Pair weather mornings are
defined as those without rain, fog, or rain the night before. Error bars indicate ±1 SD. The data for fairweather
mornings measure potential lick use while data for all days measure actual lick use. The difference between
lick use forfairweather mornings and lick use forall mornings is an estimate ofthe reduction in lick usecaused
by inclement weather = 307, = 643).
er index for 7 of 12 taxa analyzed (all P < the changes were mixed: Red-and-green and
0.05) indicating that decreased sun and in- Blue-and-yellow macaws increased with year
creased rain correlated with reduced lick use {P < O.OOl and P < 0.05, respectively) while
(Table 3). Weather index explained 0.4-6.0% Yellow-crowned Parrots (Amazonti ochrocc-
of the variation in lick u.se for these species phcilci) and White-eyed Parakeets (Arafinga
(Table 3). As fog increased, lick use decreased leiicophthcilmus) decreased (/^ < 0.05 both
significantly for 8 of 12 taxa, explaining 0.4- species; Table 3). For Red-and-green Macaw
3.0% ofthe variation in lick use for these spe- and Orange-cheeked Parrot {Pionopsina har-
cies (all P < 0.05; Table 3). Four species used raham/i), lick use increased with daily mini-
the lick less on mornings following overnight mum temperature {P < 0.05 both species). All
rains (all P < 0.05; Table 3) while the White- species showed a highly signilicant month ef-
bellied Parrot {Pionitcs lencogaster) used the fect, indicating strong .seasonality in lick u.se
lick more on mornings following rain (P < (P < 0.001; fable 3). Month explained 17-
0.05). Mealy Parrots {Aniazotm farinosa) 60% of the variation in the tiata. for Mealy
showed a positive interaction between weather Parrots, there were signilicant effects of
index and the daily minimum temperature, month by fog aiul daily minimum temperature
suggesting that sun and rain had less effect on by weather index {P 0.001; fable 3)
their lick u.se during warm days (/^ < 0.001; Lick u.se (ui fair weather mornings (a mea-
Table 3). The year-to-year differences were sure of the potential lick use), anti lick use on
not significant for 8 of 12 species (all P > all tlays, including raiiiouts (a measure of the
0.05; Table 3). F(u the remaining four species actual lick use), showed almost itlentical
140 THE WILSON BULLETIN • Vol. 116, No. 2, June 2004
of
07:30).
reported.
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Brightsmith • WEATHER EEEECTS ON AVIAN GEOPHAGY 141
month-to-month patterns (Fig. 2). The differ- of the observations and significantly reduced
ence in lick use between fair weather morn- total lick use. Reasons why birds use the lick
ings and all mornings combined suggests that less in fog are unknown but could be due to
inclement weather caused an annual 29% re- difficulties in navigation, increased chance of
duction in early morning lick use. Monthly collision during flight, or increased probability
reduction in lick use ranged from 6% in Au- of predation (Pyle et al. 1993, Bevanger
gust to 46% in February. Among the 12 taxa 1994). Parrots using this site come from at
analyzed, reduction in lick use ranged from 16 least 16 km (DJB unpubl. data) and navigation
to 37%. over such distances could be more difficult or
When rain or fog occurred from 05:00 to dangerous in foggy conditions. In general, an-
07:30 it almost completely prevented the early imals approaching geophagy sites are very
morning species from using the lick. On 7 of wary (Izawa 1993, Burger and Gochfeld
21 such days, a small number of individuals 2003) presumably due to increased predator
of the “early morning species” would occa- densities in the vicinity of geophagy sites
sionally use the lick in the late morning or (Klaus and Schmid 1998). This wariness is
afternoon. Flowever, the number of individu- evident at the Tambopata lick and may con-
als of early morning species using the lick on tribute to the low rate of predation recorded
these afternoons was always small and total during our work {n = 4 confirmed kills in
use of the lick averaged <2% of what would 4,282 hr of observation [DJB unpubl. data],
have been expected in the early morning in an area with 34 species of raptors [Rain-
(mean = 8.7 ± 6.1 individuals, range 1-19; forest Expeditions 2001]). Birds may be more
mean/y,.j^, = 87.5 ± 72.5 bird min, n = 7 wary or unwilling to go to the lick during fog
afternoons; mean/,-,^ = 2,540 ± if fog reduces their ability to detect approach-
2,365 bird min, n = 606 mornings). ing predators. The significant interaction be-
Lick use the day before did not show the tween fog and month found for Mealy Parrots
predicted negative correlation with lick use suggests that the negative effect of fog varies
for all taxa combined (Table 2). When ana- depending on the month. This could be due to
lyzed independently, five taxa showed signif- seasonal variation in the density offog or var-
icant positive correlations between lick use on iation in Mealy Parrots’ responses to fog.
consecutive days (all P < 0.05; Table 3). Sim- Weather index had a strong effect on total
ilarly, the number of days since the lick was lick use. The birds used the lick much less on
used did not show the predicted positive cor- rainy mornings and more on sunny mornings.
relation with lick use (Table 2), and when taxa While correlations do not prove causality, my
were analyzed separately, four species showed observations indicate that birds did not arrive
negative correlations between these variables in the area of the lick on rainy mornings, and
(all P < 0.05; Table 3). they frequently abandoned not just the lick it-
self, but the entire area around the lick as
DISCUSSION
I storms approached or as rain began. These ob-
Twenty-eight species were seen eating clay servations suggest that rain directly reduced
at this site, making it the most species-rich the use of the lick. It is concei\able that the
[ avian geophagy site documented (Diamond et reduction in lick use was due to the birds not
al. 1999, Burger and Gochfeld 2003, Bright- wanting to perch on oreat wet soil; the finding
smith and Ararnburu in press). As with other that lick use was less on mornings after over-
sites, parrots dominated and pigeons and Gal- night rain provides some support for this.
liformes were observed regularly. As hypoth- However, the clays the birds prefer arc water-
esized, inclement weather (morning rain, proof due to the high clay aiul sodium con-
1 overnight rain, and morning fog) reduced a\i- tents ( fan 1996, Gilardi et al. 1999. Brights-
I an lick use. Lick u.se varied seasonally but did mith and Ararnburu in press). Water docs not
1 not vary among years. 1 did not find the hy- penetrate these soils and should ha\e little or
pothesized increase in lick use following tlays no effect on their chemical composition. The
'
of low bird use or periods of inclement weath- finding that lick use on rainy mornings was
i er. reduced is consistent with other stuilies that
—
1 Weather effects. hog occurred during 20% have shovMi general reductions in birtl activity
j
142 THE WILSON BULLETIN • Vol. 116, No. 2, June 2004
during inclement weather (Beintema 1989, probably not ecologically significant, as these
Keast 1994, Lengagne and Slater 2002). birds use the liek mueh more during the late
Observers in Tambopata have long believed morning and afternoons, outside the time pe-
that total liek use is less during the cold riods considered in these analyses (Burgerand
weather associated with polar cold snaps or Gochfeld 2003, DJB unpubl. data). Yellow-
friajes. Such cold weather is known to reduce crowned Parrots and White-eyed Parakeets
the level of bird aetivity in warm tropical cli- showed significant declines during the course
mates (McClure 1975, Barry and Chorley ofthe study; the reasons for these declines are
1998). My analysis does not support this con- unknown. There were no significant anthro-
tention, but it should be noted that the present pogenic habitat changes near the study site.
data set contained only 13 mornings of bird Both species are predominantly associated
data during friajes. Red-and-green Macaws with successional habitats, but the Dusky-
and Orange-cheeked Parrots did show the ex- headed Parakeet {Aratinga weddellii) and
pected decreased lick use with decreased min- Blue-headed Parrots (Pionus menstruus) that
imum temperature, suggesting that they may share these habitats show no similar declines
reduce lick use during eolder mornings. (Forshaw 1989). There are at least two other
When analyzed separately, 9 of 12 species major clay licks within 50 km of the Tambo-
showed reductions in lick use due to inclem- pata Researeh Center, and birds moving
ent weather. Reasons for the variation among among these licks could cause the fluctua-
taxa are not known and there are no clear in- tions. Alternatively, the declines may be part
ter-specifie patterns that suggest an explana- of natural population cycles.
tion. The parrot species studied here are Compensation for lick use lost to inclement
—
thought to eat soil for sodium and protection weather. On days when it rained during the
from dietary toxins (Gilardi et al. 1999, early morning (before 07:30), >95% of the
Brightsmith and Aramburu in press). Unfor- members of the nine “early morning” parrot
tunately, our understanding of the ecologieal species listed in Table 1 did not eat soil, even
importance of geophagy at this time is insuf- if the rest of the day was clear and sunny.
ficient to extrapolate the ecological conse- Every day there were groups of large macaws
quences ofthis reduetion in clay consumption. that used the lick in the late morning and af-
However, if elimate change alters the timing, ternoon (DJB unpubl. data). As a result, large
distribution, or quantity of rainfall, it could numbers of parrots that were rained out in the
have unexpeeted eonsequences for these geo- morning could have joined these macaw
phagous species. groups and used the lick later in the day. In-
—
Seasonal and annual effects. Geophagy is stead, only a few birds oeeasionally joined
highly seasonal for nearly all species studied, these groups. Effeets of weather are strongest
and the birds at Tambopata are no exception on behaviors that are not essential for imme-
(March and Sadleir 1975, Jones and Hanson diate survival, such as singing, migrating,
1985, Sanders 1999, Keppie and Braun 2000). communal roosting, and flying (Pyle et al.
For most species, seasonal changes in geoph- 1993, Keast 1994, Cougill and Marsden
agy are elosely linked to diet changes or re- 2004). In comparison, either foraging is not as
produetion (Jones and Hanson 1985, Smedley strongly suppressed by inclement weather
and Eisner 1996, Sanders 1999). This appears (Stinson et al. 1987) or lost foraging oppor-
to be the case in Tambopata, as well, where tunities are made up through increased effort
parrots show a sharp increase in lick use dur- after the weather clears (Durell et al. 2001).
ing breeding (DJB unpubl. data). The strong effects ofclimate and the apparent
Overall lick use did not vary significantly laek of compensation when birds are denied
among years, despite the fact that floods, land- access to soil suggest that birds do not suffer
slides, and the natural change in the river dire eonsequences ifthey are unable to eat soil
course have altered the faee ofthe lick during for a few days, but more detailed studies are
the eourse of this study. For Red-and-green needed to test this hypothesis.
and Blue-and-yellow maeaws, the total To date, there are no data on how often in-
amount of lick use in the mornings increased dividual birds eat elay. An anecdotal account
signifieantly as the study progressed. This is in Munn (1992) suggests that Red-and-green
Brightsmith • WEATHER EEEECTS ON AVIAN GEOPHAGY 143
Macaws in Manu come to the lick once every tection from toxins hypothesis, most parrots
2 to 3 days. If this were the case for the early ate clay first thing in the morning before going
morning species at Tambopata, I should have off to forage. In addition, birds did not com-
found greater lick use on days after the lick pensate for missed days. These lines of evi-
was not used, or that lick use was negatively dence suggest that protection from toxins
related to lick use the previous day. However, could be driving lick use. However, evidence
I found that lick use was not correlated with from a nearby site suggests that these species
liek use on the previous day. This suggests choose soil based on its sodium content and
that the birds make daily decisions to visit the not its ability to adsorb dietary toxins
lick based on weather and season and not the (Brightsmith and Aramburu in press). Further
amount oftime since they have last eaten clay. insight into lick use would be gained by stud-
It also suggests that the birds do not consume ies that compare foraging behavior and tox-
more clay to compensate for missed days. For icity of foods eaten on days when birds do
five taxa, the number of birds the day before and do not have aecess to clay, and by com-
was positively correlated with lick use, and parative studies of birds that use the lick in
for four ofthese taxa the numberofdays since the early morning with those that use the lick
they had used the lick was negatively associ- later in the day.
ated with lick use. The hve species involved The causes and consequences of geophagy
(two large macaws. White-bellied Parrot, are admittedly complex. Detailed physiologi-
White-eyed Parakeet, and Blue-throated Pip- cal and geochemical studies have provided us
ing-Guan) span the range of habitat prefer-
with insights into the potential benehts ofthis
ence, body size, abundanee, group size, sea- behavior (Freeland et al. 1985, Jones and Han-
sonality of lick use, and time of day of lick son 1985, Gilardi et al. 1999, Mahaney et al.
use, making interpretation of this Ending dif- 1999). However, few studies have tied these
ficult. — results directly to the ecology and behavior of
Reasons for soil consumption. Previous species in the wild. This study shows that in-
studies suggest that birds in southeastern Peru
clement weather reduces lick use and that
consume soil for protection from dietary tox-
birds do not eat more soil to compensate for
ins, sodium dehciency, or both, and the find-
geophagy opportunities lost to inclement
ings of this study may provide some insight
weather. These Endings suggest that neutrali-
(Diamond et al. 1999, Gilardi et al. 1999,
zation oftoxins could be driving avian geoph-
Brightsmith and Aramburu in press). The soil
agy in this system, but investigators must con-
protects the birds from toxins by direct ad-
tinue to explore the complex temporal, sea-
sorption, stimulation of the gut to produce
more mucus, and formation of a physical bar- sonal, spatial, and taxonomic patterns in soil
rier between toxic foods and the gut lining consumption if we are to determine its true
ecological importance.
(Gilardi et al. 1999). In addition, sodium and
other minerals in the soil may protect the
ACKNOWLEDGMENTS
small intestine from tannins (Freeland et al.
1985). The soil stays in the digestive tract for
approximately 12 hr; thus, protection from stuIdyt,liaenskpeaclliatlhleyvmolyuntleieekrisltehaatdeeroslleHe.terWlildkaetrasolnor.thMi.s
toxins requires daily ingestion of clay before Dragiewic/, O. (lon/akv. A. Mra\o. and A. l igari. 1
foraging (Gilardi et al. 1999). Because protec- also thank the Instituto Naeional de Keeursiis Natura-
tion from toxins is only effective over the les in Lima and Puerto Maklona(.k> lor permission to
short term, birds should not compensate for eonduet this research. I thank Amahle lor her help
days when soil was not consumed. However, with data entiy, tlie stalTol lamhopata Research ('en-
the effect of soil on sodium balance is likely ter, and Rainforest lApeilitions lor their supiiort. This
to last over more than Just 12 hr and birds manuscript was jireatly ini[iro\etl by the comments ol
could make up for missed days through in- i:. Villalobos. .1. Murder. M. (Joehleld. C. \\\ekoH. K.
creased consumption on fair weather days. In fBoerr^l.iealpndwiatnhatnhoenystmatoiustsicarle\iaen\a\leyr.sesI.thIahniksI’woMrakrriwoatst
addition, the timing of clay consumption luiuleil by the PairthWateh Institute. Kamforesi I-\pe-
should be less important if sodium delicicncy ilitions. KaleiyhDurham ('aj!C Bird .So<,iety. W. aiul I..
is driving lick use. As predicted by the pro- .Smith. .1. lioyd. and other pri\aie ilonors.
