WILSON BULLETIN Tuesday Aug 17 2004 01:24 PM wils 116_202 Mp_134 Allen Press • DTPro System GALLEY File # 02TQ

Wilson Bulletin, 116(2), 2004, pp. 134±145

EFFECTS OF WEATHER ON PARROT GEOPHAGY IN TAMBOPATA, PERU

DONALD J. BRIGHTSMITH1

ABSTRACT.ÐGeophagy is widespread and well documented for mammals, but avian geophagy has only recently become the subject of serious scienti®c investigation. I analyzed data from 606 mornings of observations at a large avian geophagy site or ``clay lick'' in the southwestern Amazon Basin to examine the effects of weather on lick use. used the clay lick on 94% of the mornings without precipitation or fog. Parrots dominated the site in both numbers of (17) and individuals (Ͼ99%). Weather conditions were signi®- 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% of the mornings, respectively. I estimated that inclement weather caused an annual 29% reduction in geophagy for all 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 of compensation suggest that neutralization of toxins 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, Brightsmith 1974, Davies and Baillie 1988, Benkman and Aramburu in press, Burger and Gochfeld 1992, Smedley and Eisner 1996). Geophagy in press). The soils from these ``clay licks'' occurs on all continents (except Antarctica) apparently 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, Brightsmith and Aramburu in press, phagous behavior within locations over time Burger and Gochfeld in press). Long-term and between locations provides an opportunity studies of geophagy sites are lacking and this to explore the ecological role of geophagy. hinders our ability to understand the ecologi- Weather is known to have strong effects on cal role and relative importance of this phe- bird survival and behavior (Sillett et al. 2000, nomenon. Here, I document the effects of Takagi 2001, Winkler et al. 2002, Cougill and weather on avian geophagy in a lowland trop- Marsden 2004). Rain and lower temperatures ical forest over a 3-year period. cause short-term increases in nutritional stress Geophagy is known for members of the avi- for birds and often reduce the frequency of an orders , Columbiformes, Pas- behaviors not critical to immediate survival, seriformes, Casuariiformes, , and including song, migration, communal roost- Psittaciformes (Jones and Hanson 1985, ing, and ¯ying (Pyle et al. 1993, Keast 1994, Benkman 1992, Wink et al. 1993, Diamond et Lengagne and Slater 2002, Lopez-Calleja and 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 1 Duke Univ., Dept. of Biology, Durham, NC 27708, needed for short-term survival (Finney et al. USA; e-mail: [email protected] 1999, Fischer and Grif®n 2000, Dewasmes et 134 WILSON BULLETIN Tuesday Aug 17 2004 01:24 PM wils 116_202 Mp_135 Allen Press • DTPro System GALLEY File # 02TQ

Brightsmith • WEATHER EFFECTS ON AVIAN GEOPHAGY 135

al. 2001). I hypothesized that inclement the data Ͼ2 days (63 of 93 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 after the 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 NinÄo Southern Oscillation of Study area.ÐI 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 (13Њ 08Ј S, 69Њ 37Ј 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 of rain per year Bird data.ÐObservers 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 (Ͻ1 ha) clearing surrounded ary 2000 to 16 November 2002. Observers be- by mature ¯oodplain forest, successional gan watching the lick before the birds arrived ¯oodplain forest, Mauritia ¯exuosa (Areca- (approximately at sunrise) until the birds ®n- 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 ua 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 ¯owered 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- formed by the Tambopata River's erosion of corded the time, number, and species of the uplifted, Tertiary-age alluvial sediments (RaÈs- ®rst birds that landed on the lick. Starting aÈnen and Salo 1990, Foster et al. 1994, RaÈs- from this point, observers counted all birds on aÈnen 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±60 ϫ zoom). Observers pacity and high sodium levels (Gilardi et al. could readily distinguish all of the common 1999, DJB unpubl. data). bird species on the lick except the two, small, Weather data.ÐFrom June 1995 through green macaws: Chestnut-fronted Macaw (Ara February 2003, researchers at the site record- severa) and Red-bellied Macaw (Orthopsitta- ed weather data. Daily maximum and mini- ca manilata). For this study, these two 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 ¯oodplain forest approximately Data analysis.ÐI analyzed the correlation 20 m from the forest edge. Rain data were between weather variables, month, and lick collected using a standard rain gauge in a use using a quasi-likelihood general linear re- clearing approximately 30 m from the forest gression (e.g., a Poisson regression with ov- edge. Observers recorded the approximate erdispersion; Agresti 2002). This type of mod- time of rainfall on all days, even when not el was needed because the birds traveled in observing the clay lick. We did not collect ¯ocks and descended to the lick en masse, weather data every day and gaps of 1 day to causing the variance in daily lick use to be Ͼ1 month occurred. I calculated mean rainfall greater than the mean. The main effects in- for all months in which there were no gaps in cluded in the analysis were year, month, WILSON BULLETIN Tuesday Aug 17 2004 01:24 PM wils 116_202 Mp_136 • Allen Press DTPro System GALLEY File # 02TQ

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 coef®cient of fog (Pearson product- perature, lick use the day before, the number moment correlation ϭ 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 nonsigni®cant, lick use measured in bird minutes. Bird min- so this interaction term was removed from the utes were de®ned 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 Ϯ SD. min each ϭ 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 ϭ fog, rain, or rain the night before). To measure 1, cloud ϭ 2, and rain ϭ 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, I 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 of lick use recorded on the preceding day. to weather was estimated by the following for- The ``number of days since the lick was used'' mula: (potential lick use Ϫ 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 given morning if the total number of bird min- RESULTS utes recorded was Ͼ10% 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 ϭ 17) and num- was used, I assumed that total lick use was ber of observations (Ͼ99%). 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 justi®ed because on ses presented here. The remaining species 12 mornings, where rain was recorded Ͼ80% were either too uncommon to include in the of the time, total lick use averaged only 39 Ϯ analysis (n ϭ 11) or did not use the lick in 107 bird min (SD) or 1.3% of the lick use for the early morning (n ϭ 4). Of the 13 species ϭ Ϯ fair weather days (meanfair weather days 3051 that used the lick in the early morning, 4 also ϭ 2465 SD, nfair weather days 386). used the lick in the late morning and afternoon The ®rst regression analysis included all (Table 1): Blue-throated Piping- (Pipile variables. Then I excluded all variables that cumanensis), Blue-and-yellow Macaw (Ara did not contribute signi®cantly to the model ararauna), Scarlet Macaw (A. macao), and and reran the analysis. Finally, I ran a separate Red-and-green Macaw (A. chloroptera). analysis on each of the excluded variables to Weather.ÐThe average annual rainfall at determine whether any of them contributed Tambopata Research Center was 3,236 mm. signi®cantly to the model (Pyle et al. 1993). Monthly mean rainfall ranged from 95 Ϯ 57.7 The daily maximum temperature was corre- mm in August (n ϭ 6 years) to 528 Ϯ 172.4 lated with both the daily minimum tempera- mm in January (n ϭ 7 years). The months of ture (Pearson product-moment correlation ϭ 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 ϭϪ0.35), and it ex- tial evapotranspiration (Fig. 1). Rain events of plained less variation than either of the other Ͼ1 mm were recorded on 42% of the days two, so it was eliminated from the analysis. (709 of 1,679 days). The number of days with The interaction coef®cient of fog by daily rain was greatest in January (mean ϭ 18 Ϯ WILSON BULLETIN Tuesday Aug 17 2004 01:24 PM wils 116_202 Mp_137 Allen Press • DTPro System GALLEY File # 02TQ

Brightsmith • WEATHER EFFECTS 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 Ն75% of the observations), U (uncommon, seen Ͻ75% and Ն25%), R (rare, seen Ͻ25% and Ն5%), or O (occasional, seen during Ͻ5% of the observations). For species listed as occasional, the number of times seen is reported in parentheses.

Time of day Abundance Before 07:30 07:30±12:00 After 12:00 at lick Species analyzed in this paper Blue-and-yellow Macaw (Ara ararauna) 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 (Pionites leucogaster) x x U Orange-cheeked Parrot (Pionopsitta barrabandi) x U Blue-headed Parrot (Pionus menstruus) x C Yellow-crowned Parrot (Amazona ochrocephala) x U Mealy Parrot (Amazona farinosa) x C Blue-throated Piping-Guan (Pipile cumanensis) x xxU Additional species recorded at the lick Speckled Chachalaca (Ortalis guttata) x x x R Spix's Guan (Penelope jacquacu) x x x R Orange-breasted Falcon (Falco deiroleucus) x O (1) Plumbeous Pigeon (Patagioenas plumbea) 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 O (1) Cobalt-winged Parakeet (Brotogeris cyanoptera) x x U Gray-fronted Dove (Leptotila rufaxilla) x x O (2) Purplish Jay (Cyanocorax cyanomelas) x x O (4) Blue-gray Tanager (Thraupis episcopus) x x O (4) Crested Oropendola (Psarocolius decumanus)x O (2)

4.1 days, n ϭ 7 years) and least in August The variables month, weather index, fog, and (mean ϭ 5.5 Ϯ 2.6 days, n ϭ 6 years). The rain the night before explained 47% (P Ͻ mean temperature was 24.3 Ϯ 1.4Њ C. Early 0.001) of the variation in total lick use (Table morning fog was recorded on 20% of the days 2). As weather progressed from sunny to (n ϭ 606). Rain was recorded during 12% of cloudy to rainy, and fog duration increased, the observations (n ϭ 606). It rained the pre- total lick use decreased, explaining 7% of the vious night during 8% of the observations (n variation in the data (P Ͻ 0.001; Table 2). ϭ 510); there was no rain or fog of any sort Birds used the lick less on early mornings fol- for 76% of the observations (n ϭ 510). On 80 lowing rain the previous night (P Ͻ 0.05; Ta- days there was heavy rain during the early ble 2). Month explained 39% of the variation morning (and observers did not go to the lick in total lick use (P Ͻ 0.001; Table 2): mean on these days). daily lick use ranged from 4,784 Ϯ 2,387 bird Weather effects on geophagy.ÐBirds used min in August to 257 Ϯ 378 bird min in May the clay lick on 94% of the fair weather morn- (Fig. 2). ings (i.e., without rain or fog during the ob- When each taxon was analyzed separately, servation or rain the night before, n ϭ 386). lick use was negatively correlated with weath- WILSON BULLETIN Tuesday Aug 17 2004 01:24 PM wils 116_202 Mp_138 • Allen Press DTPro System GALLEY File # 02TQ

138 THE WILSON BULLETIN • Vol. 116, No. 2, June 2004

FIG. 1. Mean monthly temperature, rainfall, and estimated evapotranspiration at Tambopata Research Center, 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 weather and month affecting lick use by birds in Tambopata, Peru, 12 January 2000±16 November 2002. Values are presented for combined lick use by 13 species and as the percent deviance explained (regression coef®cient). Coef®cients with negative values indicate that birds used the lick less as the value of the independent variable increased. A single coef®cient 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 signi®cant at P Ͻ 0.001.

Deviance (regression Variable coef®cient) Month 39%***a Weather index 4% (Ϫ0.36)*** Fog 3% (Ϫ0.038)*** Rained night before 1% (Ϫ0.32)* Year NSb Birds yesterday NS Days since usedc NS Daily minimum temperature NS Month:weatherd NS Month:fogd NS Daily minimum:weather indexd NS Total df 509 Total deviance 229190 Deviance explained 47%

a * P Ͻ 0.05, ** P Ͻ 0.01, *** P Ͻ 0.001. b NS ϭ not signi®cant (P Ͼ 0.05). c Days since used is a measure of how many mornings had elapsed since the lick had been used by birds. d Variables separated by a colon indicate interactions. WILSON BULLETIN Tuesday Aug 17 2004 01:24 PM wils 116_202 Mp_139 Allen Press • DTPro System GALLEY File # 02TQ

Brightsmith • WEATHER EFFECTS ON AVIAN GEOPHAGY 139

FIG. 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 to 16 November 2002. Fair weather mornings are de®ned as those without rain, fog, or rain the night before. Error bars indicate Ϯ1 SD. The data for fair weather mornings measure potential lick use while data for all days measure actual lick use. The difference between lick use for fair weather mornings and lick use for all mornings is an estimate of the reduction in lick ϭ ϭ use caused by inclement weather (nfair weather days 307, nall days 643).

er index for 7 of 12 taxa analyzed (all P Ͻ 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 Ͻ 0.001 and P Ͻ 0.05, respectively) while (Table 3). Weather index explained 0.4±6.0% Yellow-crowned Parrots (Amazona ochroce- of the variation in lick use for these species phala) and White-eyed Parakeets (Aratinga (Table 3). As fog increased, lick use decreased leucophthalmus) decreased (P Ͻ 0.05 both signi®cantly for 8 of 12 taxa explaining 0.4± species; Table 3). For Red-and-green Macaw 3.0% of the variation in lick use for these spe- and Orange-cheeked Parrot (Pionopsitta bar- cies (all P Ͻ 0.05; Table 3). Four species used rabandi), lick use increased with daily mini- the lick less on mornings following overnight mum temperature (P Ͻ 0.05 both species). All rains (all P Ͻ 0.05; Table 3) while the White- species showed a highly signi®cant month ef- bellied Parrot (Pionites leucogaster) used the fect, indicating strong seasonality in lick use lick more on mornings following rain (P Ͻ (P Ͻ 0.001; Table 3). Month explained 17± 0.05). Mealy Parrots (Amazona farinosa) 60% of the variation in the data. For Mealy showed a positive interaction between weather Parrots, there were signi®cant effects of index and the daily minimum temperature month by fog and daily minimum temperature suggesting that sun and rain had less effect on by weather index (P Ͻ 0.001; Table 3) their lick use during warm days (P Ͻ 0.001; Lick use on fair weather mornings (a mea- Table 3). The year-to-year differences were sure of the potential lick use), and lick use on not signi®cant for 8 of 12 species (all P Ͼ all days, including rainouts (a measure of the 0.05; Table 3). For the remaining four species actual lick use), showed almost identical WILSON BULLETIN Tuesday Aug 17 2004 01:24 PM wils 116_202 Mp_140 • Allen Press DTPro System GALLEY File # 02TQ

140 THE WILSON BULLETIN • Vol. 116, No. 2, June 2004 re 07: opata, 0.049)*** 0.26)* 1.00)* Parrot Ϫ Ϫ Ϫ , and so are not Yellow-crowned Piping-Guan Blue-throated k less as the value 605 406 1% ( 2% ( 1% ( 2% (0.037)* 16140 30% NS NS NS NS 1891 21% NS NS NS NS 18%*** NS NS 27%*** NS NS NS NS NS NS 5.36)*** Ϫ Parakeet Mealy Parrot 559 Dusky-headed 605 6%*** 1% (0.21)*** 3% ( 145187 48% NS NS NS NS 26217 27% NS NS 27%*** NS NS NS NS NS NS 39%*** NS NS NS NS NS f 0.001. 0.74)*** 0.037)*** 0.11)*** 0.02)** 0.26)*** 0.31)* Parakeet Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ White-eyed Ͻ P 605 477 2% ( 5% ( 3% ( 1% ( 6% ( 65185 25% NS NS NS NS 67502 61% 36%*** NS NS NS NS 17%*** NS NS NS NS NS 11% (0.0018)*** 11% ( 0.33)** 0.030)* 0.60)*** 0.056)*** 0.83)** Ϫ Ϫ Parrot Ϫ Ϫ Ϫ White-bellled 509 406 0.5% ( 6% ( 1% ( 3% ( 2% ( 13579 32% NS NS NS NS 6497 62% NS NS NS NS NS NS NS NS 23%*** 59%*** NS NS NS 0.54)*** 0.069)*** 0.60)* 0.40)** 0.40)* Parrot Macaw Scarfet Macaw Green macaws Ϫ Ϫ Ϫ Ϫ Ϫ Orange-cheeked Blue-and-yellow 406 559 1% (0.083)* 4% ( 1% (0.39)* 1% (0.013)** 1% ( 3% ( 1% ( 1% (0.23)* 2% (0.003)** 2% ( 21081 42% NS NS NS 40211 61% NS NS NS NS 29%*** 60%*** NS NS NS 0.14)* 0.022)* 0.37)* a 0.074)** 0.69)** Ϫ Ϫ Ϫ Macaw Ϫ Ϫ Red-and-green 509 b 442 2% ( 2% (0.17)* 0.4% ( 5% (0.75)*** 1% (0.008)* 2% ( 0.4% ( 0.3% ( 6765 35% NS NS NS NS 120386 57% 23%*** NS NS NS NS 55%*** NS NS NS NS d d 0.001. Ͻ P 0.05). Ͼ P 0.01, *** c c Ͻ d d P Variable Variable Blue-headed Parrot d d 0.05, ** e e not signi®cant ( Ͻ ϭ P NS Variables separated by a colon indicate interactions. * Days since used is a measure ofTotal how df many vary mornings because had different elapsed variables since had the different lick numbers had of been observations used eliminated by due birds. to missing values. The taxon ``green macaws'' is a combination of Chestnut-fronted and Red-bellled macaws. TABLE 3. Quasi-likelihood general linear regression model (Poisson regression with overdispersion) of weather and month on lick use by birds in Tamb a b c d e f Total df Peru, 12 January30). 2000±16 Values November are 2002. presentedof Values as the are percent presented independent deviancereported. for variable explained The 12 (regression increased. model taxa coef®cient). Single uses Coef®cients representing coef®cients the with 13 cannot chi-squared-based negative species analysis-of-deviance be values that test. calculated indicate used All for that the models birds the are clay used categorical signi®cant lick the variable at during lic month the or early interactions morning including (befo month Month Weather index Fog Rained night before Year Birds yesterday Days since used Month:fog Daily minimum weather index Total deviance Deviance explained Month Weather index Fog Rained night before Year Birds yesterday Days since used Month:fog Daily minimum weather index Total df Total deviance Deviance explained Daily minimum temperature Month:weather Daily minimum temperature Month:weather WILSON BULLETIN Tuesday Aug 17 2004 01:24 PM wils 116_202 Mp_141 Allen Press • DTPro System GALLEY File # 02TQ

Brightsmith • WEATHER EFFECTS ON AVIAN GEOPHAGY 141

month-to-month patterns (Fig. 2). The differ- of the observations and signi®cantly 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- dif®culties in navigation, increased chance of duction in early morning lick use. Monthly collision during ¯ight, 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 dif®cult 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 in 21 such days, a small number of individuals press) 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. However, 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 ϭ 4 con®rmed kills in use of the lick averaged Ͻ2% 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 ϭ 8.7 Ϯ 6.1 individuals, range 1±19; forest Expeditions 2001]). Birds may be more ϭ Ϯ ϭ meanlick use 87.5 72.5 bird min, n 7 wary or unwilling to go to the lick during fog ϭ Ϯ afternoons, meanlick use all mornings 2540 2365 if fog reduces their ability to detect approach- bird min, n ϭ 606 mornings). ing predators. The signi®cant 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, ®ve taxa showed signif- seasonal variation in the density of fog or var- icant positive correlations between lick use on iation in Mealy Parrots' responses to fog. consecutive days (all P Ͻ 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, three species observations indicate that birds did not arrive showed negative correlations between these in the area of the lick on rainy mornings, and variables (all P Ͻ 0.05; Table 3). they frequently abandoned not just the lick it- self, but the entire area around the lick as DISCUSSION 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 conceivable that the avian geophagy site documented (Diamond et reduction in lick use was due to the birds not al. 1999, Brightsmith and Aramburu in press, wanting to perch on or eat wet soil; the ®nding Burger and Gochfeld 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 are water- esized, inclement weather (morning rain, proof due to the high clay and sodium con- overnight rain, and morning fog) reduced avi- tents (Tan 1996, Gilardi et al. 1999, Brights- an lick use. Lick use varied seasonally but did mith and Aramburu in press). Water does not not vary among years. I did not ®nd the hy- penetrate these soils and should have little or pothesized increase in lick use following days no effect on their chemical composition. The of low bird use or periods of inclement weath- ®nding that lick use on rainy mornings was er. reduced is consistent with other studies that Weather effects.ÐFog occurred during 20% have shown general reductions in bird activity WILSON BULLETIN Tuesday Aug 17 2004 01:24 PM wils 116_202 Mp_142 • Allen Press DTPro System GALLEY File # 02TQ

142 THE WILSON BULLETIN • Vol. 116, No. 2, June 2004

during inclement weather (Beintema 1989, probably not ecologically signi®cant, as these Keast 1994, Lengagne and Slater 2002). birds use the lick much more during the late Observers in Tambopata have long believed morning and afternoons, outside the time pe- that total lick use is less during the cold riods considered in these analyses (Burger and weather associated with polar cold snaps or Gochfeld in press, DJB unpubl. data). Yellow- friajes. Such cold weather is known to reduce crowned Parrots and White-eyed Parakeets the level of bird activity in warm tropical cli- showed signi®cant declines during the course mates (McClure 1975, Barry and Chorley of the study; the reasons for these declines are 1998). My analysis does not support this con- unknown. There were no signi®cant 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 colder 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 Research Center, and birds moving ent weather. Reasons for the variation among among these licks could cause the ¯uctua- taxa are not known and there are no clear in- tions. Alternatively, the declines may be part ter-speci®c 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.ÐOn days when it rained during the from dietary toxins (Gilardi et al. 1999, early morning (before 07:30), Ͼ95% of the Brightsmith and Aramburu in press). Unfor- members of the nine ``early morning'' parrot tunately our understanding of the ecological 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. ®cient to extrapolate the ecological conse- Every day there were groups of large macaws quences of this reduction in clay consumption. that used the lick in the late morning and af- However, if climate 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 unexpected consequences 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.ÐGeophagy is stead, only a few birds occasionally joined highly seasonal for nearly all species studied, these groups. Effects 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 ¯ying (Pyle et al. For most species, seasonal changes in geoph- 1993, Keast 1994, Cougill and Marsden agy are closely linked to diet changes or re- 2004). In comparison, either foraging is not as production (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 of climate and the apparent Overall lick use did not vary signi®cantly lack of compensation when birds are denied among years despite the fact that ¯oods, land- access to soil suggest that birds do not suffer slides, and the natural change in the river dire consequences if they are unable to eat soil course have altered the face of the lick during for a few days, but more detailed studies are the course of this study. For Red-and-green needed to test this hypothesis. and Blue-and-yellow macaws, the total To date, there are no data on how often in- amount of lick use in the mornings increased dividual birds eat clay. An anecdotal account signi®cantly as the study progressed. This is in Munn (1992) suggests that Red-and-green WILSON BULLETIN Tuesday Aug 17 2004 01:24 PM wils 116_202 Mp_143 Allen Press • DTPro System GALLEY File # 02TQ

Brightsmith • WEATHER EFFECTS 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 ®rst 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 lick 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 of time 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 ®ve taxa, the number of birds the day before and do not have access to clay, and by com- was positively correlated with lick use, and parative studies of birds that use the lick in for four of these taxa the number of days 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 ®ve 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 bene®ts of this ence, body size, abundance, 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 ®nding dif- 1999). However, few studies have tied these ®cult. results directly to the ecology and behavior of Reasons for soil consumption.ÐPrevious 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 de®ciency, or both, and the ®nd- geophagy opportunities lost to inclement ings of this study may provide some insight weather. These ®ndings suggest that neutrali- (Diamond et al. 1999, Gilardi et al. 1999, zation of toxins 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- sorption, stimulation of the gut to produce tinue to explore the complex temporal, sea- 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 (Gilardi et al. 1999). In addition, sodium and ecological importance. other minerals in the soil may protect the small intestine from tannins (Freeland et al. ACKNOWLEDGMENTS 1985). The soil stays in the digestive tract for approximately 12 hr; thus, protection from I thank all the volunteers that collected data for this study, especially my ®eld leaders B. Wilkerson, M. toxins requires daily ingestion of clay before Dragiewicz, O. Gonzalez, A. Bravo, and A. Figari. I foraging (Gilardi et al. 1999). Because protec- also thank the Instituto Nacional de Recursos Natura- tion from toxins is only effective over the les in Lima and Puerto Maldonado for permission to short term, birds should not compensate for conduct this research. I thank C. Amable for her help days when soil was not consumed. However, with data entry, the staff of Tambopata Research Cen- the effect of soil on sodium balance is likely ter, and Rainforest Expeditions for their support. This to last over more than just 12 hr and birds manuscript was greatly improved by the comments of could make up for missed days through in- E. Villalobos, J. Burger, M. Gochfeld, C. Wyckoff, K. Berg, and an anonymous reviewer. I thank P. Marriott creased consumption on fair weather days. In for help with the statistical analyses. This work was addition, the timing of clay consumption funded by the EarthWatch Institute, Rainforest Expe- should be less important if sodium de®ciency ditions, Raleigh-Durham Cage Bird Society, W. and L. is driving lick use. As predicted by the pro- Smith, J. Boyd, and other private donors. WILSON BULLETIN Tuesday Aug 17 2004 01:24 PM wils 116_202 Mp_144 • Allen Press DTPro System GALLEY File # 02TQ

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