The Condor 95:896-903 0 The Cooper Omlthological Society 1993

SPATIAL AND TEMPORAL ABUNDANCE PATTERNS OF RUDDY QUAIL-DOVES (GEOTRYGON MOKWVi4) NEAR MANAUS, BRAZIL’

PHILIP C. STOUFFER~ AND RICHARD 0. BIERREGAARD, JR. BiodiversityPrograms, NHB 180, SmithsonianInstitution, Washington,DC 20560

Abstract. We analyzed patterns of abundanceof Ruddy Quail-Doves (Geotrygonmon- tana) based on 12 years of mist-net data (457 captures)from terrajirme forest near Manaus in central Amazonian Brazil. Unlike most understory at the study site, G. montana varied greatly in abundance. Quail-doves disappeared for months and then reappeared, usually during the wet season.In some months they became one of the most frequently netted birds. Quail-doves avoided isolated forest fragments of one ha, although abundance did not differ among fragments of 10 ha, 100 ha, and continuous forest. Peak abundance varied among years, as did the timing of peak abundance.In general,the annual pattern of quail-dove abundance was correlated with the annual rainfall pattern. Considering all 12 years of data, however, quail-dove abundanceduring a given three-month period was not correlatedwith rainfall during that period, but with rainfall in the sameperiod in the previous year. No quail-doves were recaptured more than a few weeks apart; thus individual birds did not return to the same site from year to year. Since quail-doves feed mainly on fallen fruit, these resultssuggest that they may range over wide areasto exploit regional differences in fruit production. Key words: Amazonian Brazil; Geotrygonmontana; migration; rainfall; Ruddy Quail- Dove:seasonal movements.

INTRODUCTION portunity for relatively short distance altitudinal The understoty community of terra firme migration suchas is common in Central America forest in central Amazonian Brazil is character- (Levey 1988a, Stiles 1988, Loiselle and Blake ized by permanently resident that show 199 1) and southeasternBrazil (Sick 1983). A sec- little seasonal variation in abundance as mea- ond reason for the lack of migration may relate sured by mist net captures (Bierregaard 1990a). to the difference in structure of understory com- This area is south of the wintering range for most munities between well-studied sites in Central neotropical migrants (e.g., Blake et al. 1990, Stotz America and Amazonia. Among speciessampled et al. 1992). Austral migrants that winter in equa- by mist-netting, frugivores and nectarivores are torial Brazil include few forest birds (Bierregaard more common in Central America (Karr et al. 1990a). In other tropical regions, forest birds 1990), and are more prone to large- and small- commonly make relatively small scale migra- scalemovements than are insectivores (Terborgh tions to take advantage of seasonalvariation in and Weske 1969, Levey and Stiles 1992). resources,especially differences in flower and fruit The Ruddy Quail-Dove (Geotrygon montana) production as a function of habitat or altitude is one of the few speciesthat exhibit pronounced (Morton 1977, Blake and Loiselle 199 1, Date et variation in abundance in the forests near Ma- al. 199 1, Levey and Stiles 1992). Such move- naus, Brazil, presumably as a result of large-scale ments appear to be much less common in the population movements (Bierregaard 1990a). Amazon Basin than in Central America (Ter- Basedon over seven years of mist net data, Bier- borgh and Weske 1969, Lovejoy 1975, Terborgh regaard (1990a) found it to be more abundant in et al. 1990). the wet season, although there was strong vari- One reason such migrations are less common ation among years. Of the 37 common species in Amazonia may relate to the geographyof the examined, G. montana was the most variable in region. By virtue of its vast expanse with little abundance, disappearing for months at a time. altitudinal variation, Amazonia offers little op In Panama and at La Selva, Costa Rica, abun- dance of G. montana is also highly variable (Stiles and Levey, in press;Karr, pers. observ. cited in I Received12February 1993.Accepted 13 May 1993. 2 Present address: Department of Biological Sci- Karr et al. 1990). ences,Southeastern Louisiana University, Hammond, G. montana is distributed from southern Mex- LA 70401-0814. ico to northern Argentina, including Caribbean

P961 RUDDY QUAIL-DOVES IN AMAZONIAN BRAZIL 897 islands (AOU 1983). It is generally found in the The forest is characterized by an average can- interior of moist to wet forests,where it feedson opy height of 30-35 m with occasionalemergents fallen fruits, digestingboth pulp and seeds(Skutch that reach up to 55 m. The understory is rela- 1949; Schubart et al. 1965; Cruz 1974; Davis et tively open and dominated by palms. Density of al. 1985; Hilty and Brown 1986; pers. observ.). fertile understory plants is low compared to other It nests in low vegetation or on decaying stumps neotropical sites, probably becauseof poor soils (Skutch 1949). Active nests were found on the (Gentry and Emmons 1987; seea more complete study site in 1983, 1987, and 1992, and we sus- description ofthe study area in Lovejoy and Bier- pect the bird nested on the site in other years of regaard 1990). Rainfall at Reserva Ducke, 50 km high abundance (D. F. Stotz and A. Whittaker, south of the study site, averagedabout 2.5 m/year pers. comm., pers. observ.). This quail-dove is from 1966 to 1990, with annual peaks from Jan- especially well suited to a study based on mist uary to April (see also RESULTS; rainfall data net captures (see below) as it rarely perches off courtesy of the Departamento de Climatologia the ground and typically flies only one to two m of INPA). above the ground. Results presented here are based on a netting As for many understory birds, preliminary and banding program that began in 1979. All analysis suggestedthat G. montana showsspatial nets were NEBBA-type ATX (36 mm mesh, 12 variation in abundance associatedwith fragment x 2 m). A larger mesh would be more efficient size. Data presentedin Bierregaard and Lovejoy for quail-doves, but since we used the same net (1989; Appendix) suggestthat G. montana de- size at all times, this does not bias our results. creasedin abundance in one ha forest fragments A total of over 55 transects of 100 m (8 nets), in comparison to larger fragments and continu- 200 m (16 nets), or 400 m (30 nets) were netted ous forest. for one day at a time (06:OOto 14:00) at various Here we examine the patterns of spatial and intervals (see Bierregaard 1990a for more de- temporal abundance of G. montana based on 12 tails). Although interspecific differencesin abun- years of mist net capture data. We asked the dance based on mist net capture data must be following questions. How does abundance vary viewed cautiously (see discussion in Karr 198 1, within and among years?Are quail-doves equally Remsen and Parker 1983) we consider the tech- abundant in continuous forest and in patchesof nique effective for determining abundance of one, 10 and 100 ha? How is temporal variation Geotrygon montana based on our knowledge of related to seasonal variation in rainfall? Does the bird’s behavior (see also INTRODUC- temporal variation represent a consistent migra- TION). tion pattern? How can this pattern be explained For most analyses we lumped captures and basedon the ecologicalcharacteristics of the bird? net-hours for three month periods (“quarters” hereafter) that correspondto rainfall seasonality. METHODS Capture rate was distributed bimodally across This study was conducted in terra jirme forest fragment sizesbecause of the low number of cap- 80 km north of Manaus, Brazil (2”3O”S, 6o”W) tures in one ha fragments and frequent absences in the study area of the Biological Dynamics of from larger reserves, so we analyzed fragment Forest Fragments Project. Although some parts size effectsusing a non-parametric test for ran- of the area have been cleared for cattle ranching, domized blocks (Sokal and Rohlf 198 1:446). We providing the opportunity to study the effectsof counted eachquarter with samplesfrom the three fragmentation (e.g., Bierregaard 1990b, Lovejoy fragment sizes and continuous forest as a block, and Bierregaard 1990) these local disturbances thus controlling for variation among quartersand are within an area ofunbroken forestthat extends years. We analyzed relationships among rainfall, for hundreds of km. Here we include data from mass, and abundance using Spearman rank cor- five fragments of one ha, four fragments of 10 relation. Mass data did not violate assumptions ha, two fragments of 100 ha, and continuous forest. Continuous forest data include the frag- of parametric analyses, allowing us to estimate ments before they were isolated by cutting the the variance in mass due to variation among surrounding forest, and five sites that have not years using a model II ANOVA (Sokal and Rohlf been isolated. The greatestdistance between sites 1981:205). We provide details on other tests as is about 60 km. they are used. 898 PHILIP C. STOUFFER AND RICHARD 0. BIERREGAARD, JR.

: 0 I\ 1980 1981 1982 1983 1984 1985 1986 1987 ,988 ,989 ,990 I199

YEAR

FIGURE I. Monthly capture rate of Geotrygonmomma from October I979 to October 1991, excludingsame- day recaptures.This figure only includes months with >200 net-hours, so gaps in the line represent periods with reduced sampling(e.g., late 1986 and early 1990).

RESULTS peaks the abundance of quail-doves relative to other understory birds became quite high; quail- CAPTURE RATE doves were the most frequently netted bird in A total of 457 captures of quail-doves (excluding March 1983 (10.6% of captures) and in March same day recaptures) were recorded in 239,000 1986 (8.3% of captures), and they were the sec- net-hr between October 1979 and October 199 1 ond most commonly netted species in several (Fig. 1). Runs tests for the two longest periods other months. In most years no or very few quail- of uninterrupted data, November 1979 through doves were captured between June and Novem- January 1983 and March 1983 to July 1986 ber. There were some irregularities in this pat- showedsignificant variation in capturerates (both tern, however. Quail-doves were present from P < 0.005). In general, the times of highestquail- June 1982 through July 1983, after which there dove abundance were January through April, al- were almost no captures until August 1984. A though peak capture rate varied from ~4 to > 19 striking feature of quail-dove captures was an captures/1,000 net-hr (Figs. 1,2). During capture absolute lack of recaptures across years-only

25-

JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC

MONTH FIGURE 2. Monthly mean capture rate +SD. Also shown is the maximum for each month. All months had a minimum capture rate of zero. RUDDY QUAIL-DOVES IN AMAZONIAN BRAZIL 899

600

JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC

MONTH FIGURE 3. Monthly rainfall *SD at ReservaDucke from 1965-1991. Also shownis the minimum and maximum for eachmbnth. nine quail-doves were recaptured,none more than capture rate and mean rainfall for all years com- five weeks after it was first banded. bined (Figs. 2, 3) rainfall and capture rate were not correlated when the data were examined CAPTURE RATE AND FRAGMENT SIZE quarter by quarter for the entire period (Fig. 4a, To analyze fragment size effectswe lumped cap- r = 0.160, P = 0.283). Rainfall in the same quar- tures by quarters based on rainfall (Fig. 3: early ter one year previous was significantly correlated wet season,Dee-Feb; late wet season,Mar-May; with capture rate, however (Fig. 4b, r = 0.369, early dry season,June-Aug; and late dry season, P = 0.0 11). This relationship was especially close Sept-Nov). For 26 quarters with data from all from 1979 to 1983. Capture rate was not related size classes,one ha fragments had lower capture to capture rate one year before (r = 0.274, P = rates than larger fragments and continuous forest 0.124),which suggeststhat abundancecycles were (Table 1, x2 = 13.035, df = 3, P < O.OOS),but not due to population cycles. there was no difference among fragments of 10 ha, 100 ha, and continuous forest (x2 = 0.122, CONDITION AND CAPTURE RATE df = 2, P > 0.9). Hereafter in analysesbased on Male and female quail-doves differed in mass capture rate, we exclude captures and net-hours (ANOVA P = 0.0014), and both sexes showed from one ha reserves. substantial variation (adult males: K = 115.6 g, SD = 15.7, range = 70-165 g, n = 169; adult RAINFALL AND CAPTURE RATE females: x = 111.4 g, SD = 16.5, range = 74- Rainfall data from Reserva Ducke show the wet- 170 g, IZ = 154). We used quarterly mean mass test months to be December through May (Fig. to examine the relationships between quail-dove 3). March through May were the most consis- abundance and mass and between rainfall and tently wet months; in some years almost no rain fell earlier in the wet season, from December TABLE 1. Quail-dove capturesin forestfragments through February. June through September were and in continuousforest. Capture rates followed by the the driest months, with the lowest among-year sameletter do not differ. variation. Among-year variation was pro- nounced in October and November, as the rains RW?WC Number of Number of Capture rate/ came in some yearsbut the dry seasoncontinued sire (ha) captures net-hours 1,000 net-hr in others. In general, capture rate and rainfall 1 6 13,400 0.448 A were positively correlated (Spearman rank cor- 10 41 21,940 1.467B relationofmonthlymeans: Y= 0.755, P= 0.0045). 100 39 21,970 1.775B >lOO 330 201,800 1.635B Despite the clear relationship between mean 900 PHILIP C. STOUFFER AND RICHARD 0. BIERREGAARD, JR.

Figure 4a

- 1000

? - 800 5 II 2 - 600 g d

YEAR

i‘ ‘ 800 .k

0 19791980 1981 ,982 1983 1984 1985 1986 1987 1988 1989 1990 1991

YEAR FIGURE 4. Quarterly capture rate and quarterly rainfall (a). Quarterly capture rate and rainfall in the same quarter in the previous year (b).

mass. After adjusting for sexual dimorphism, DISCUSSION quarterly mean mass was not significantly cor- ABUNDANCE PATTERNS related with abundance or rainfall, although the positive relationship between capture rate and Analysis of abundance data clearly indicated that mass approached significance (capture rate: r = quail-doves avoided one hectare fragments but 0.320, P=O.O53;rainfall: r= -0.115, P=O.498; did not discriminate among larger fragments and rainfall in the same quarter one year before: Y = continuous forest (Table 1). This result was also -0.107, P = 0.530). Mass varied significantly suggestedby the capture data presented in Bier- among years (F = 2.13, P = 0.0408) but inter- regaard and Lovejoy (1989). Canopy fruit pro- annual variation accountedfor only 3.4% of mass duction is probably lowest per unit area in one variation. hectare reservesbecause many large trees die or RUDDY QUAIL-DOVES IN AMAZONIAN BRAZIL 901 blow over. Also, most accounts of Geotrygon individuals of 27 speciesof canopy tree showed montana suggestthat it prefers areas of closed highestfruit production between September and forestto edgesand treefall gaps(e.g., Skutch 1949) May, after a flowering peak from July to Septem- as was quantitatively shown for G. veraguensis ber (Alencar et al. 1979). Presumably fruit pro- in Costa Rica (Levey 1988b). One hectare frag- duction is determined by rainfall before the pe- ments are hotter and drier than larger fragments riod of flowering and fruit maturation, accounting (Kapos 1989) and thus may be microclimatically for the time lag between rainfall and quail-dove unsuitable for G. montana, which has been shown appearances. to prefer wetter sites in a heterogeneousforest in Studies of tropical birds have not addressed Panama (Karr and Freemark 1983). multi-year patterns in fruit and fruit-eating bird Since quail-doves recolonized larger frag- abundance, but the relationship between bird ments, their absencefrom one hectare fragments density and food availability across years has was due to active avoidance of these habitat been examined for sparrowsin arid areas of the patches,a different processthan that which leads western US, where overwintering birds eat seeds to long-term absence of other understory birds produced the summer before. Summer rainfall from fragments.Obligate ant-followers and some influences seed production (Pulliam and Brand species that typically forage in mixed-species 1975) and correlateswith sparrow abundance in flocks are also especially vulnerable to fragmen- southeasternArizona (Dunning and Brown 1982). tation (Bierregaard and Lovejoy 1989). These An alternative explanation for the time lag in species quickly leave fragments after isolation quail-dove responseto rainfall is that abundance (Bierregaard and Lovejoy 1989) and do not re- in Manaus correlates with reproductive success colonize fragmentsthat remain isolated. Absence of the population the year before, which in turn from isolated fragments appearsto be due to the relates to rainfall during the period of reproduc- unwillingness ofthese speciesto crossopen areas. tion. Unfortunately, this hypothesis is difficult Most ofthese speciesbecome more likely to reap- to consider becauseof the lack of recapture data. pear in fragments (although they do not neces- Patterns of quail-dove abundance were not re- sarily persist) as the secondary growth that con- lated to regular movements by individual birds nects fragments to continuous forest becomes or to population cycles. No birds were captured taller (P. C. Stouffer and R. 0. Bierregaard, un- in two different years; even though quail-doves publ. data). Other forest speciesthat use edges bred successfullyon the site, we know of no adults and secondarygrowth persisteven in one ha frag- or juveniles that returned to the area. Thus in- ments (Bierregaard and Lovejoy 1989). Canopy dividual quail-doves were not making predict- speciesthat readily crossopen areas, such as pi- able movements, such as returning to a breeding geons, parrots, oropendolas, and some toucans site. This low recapture rate contrasts markedly and tanagers, also use fragments (pers. observ.). with most understory speciesat the site. On reg- Capture data also clearly showeda relationship ularly netted lines in continuous forest the over- between quail-dove abundance and rainfall. As all recapture rate for all specieswas about 40% was previously noted by Bierregaard(1989a) and (Bierregaard 1990a). by Tostain (1989) in French Guiana, quail-doves Finally, capture rate and rainfall did not sig- were most abundant during the wet season.Quail- nificantly affect mass. If anything, there may be doves responded not to rain directly, but with a a positive relationship between capture rate and time lag of one year (Fig. 4). Since quail-dove mass.Variation in masswas mostly due to intra- abundance is not linked directly to rainfall, quail- quarterly differencesrather than variation among dove appearancesand disappearanceswere not quarters or years. a responseto physiological stress(sensu Karr and POSSIBLE MOVEMENT PATTERNS Freemark 1983). Data from other neotropical forests show that canopy fruits are most abun- Although it is clear that quail-doves disappear dant in the late dry season or wet season (e.g., from the Manaus area, the extent and direction Frankie et al. 1974; Terborgh 1983, Ch. 2; see of their movements are unknown. We doubt that summary of data from Barro Colorado Island, quail-doves simply move from terrajirme forest Panama and La Selva, Costa Rica in Levey et into vdrzea or igapd forest along watercourses, al., in press). At Reserva Ducke a sample of 81 since they have not been recorded from those 902 PHILIP C. STOUFFER AND RICHARD 0. BIERREGAARD, JR. habitats around Manaus. Regional variation in We suspectthat G. montana is rarely forced to phenology has not been studied, but rainfall data make suchdesperate movements, since we found suggestthat latitudinal movements from Manaus little variation in condition among years. The to the north would allow quail-doves to most relatively high variation in quail-dove mass may easily track changesin fruit resources. Rainfall reflect an ability to store fat during times of food patterns shift most dramatically to the north of abundance or before moving to another area. Manaus. In Roraima, about 800 km to the north, rainfall seasonality is the reverse of that in Ma- ACKNOWLEDGMENTS naus (SUDAM 1984). D. Stotz (pers. comm.) has We thank the banders and mateiroswho have helped observedquail-doves there in September, during operate net lines and enter data. The staff at INPA’s Roraima’s wet season,but not in March, during Departamento de Climatologia cheerfully provided Roraima’s dry season.Rainfall patterns differ lit- rainfall data. Andrew Whittaker, Doug Stotz, and Tan- tle to the east and west of Manaus, and season- ia Sanaiotti shared their personal observations of ality changesmuch more gradually to the south movements of quail-doves and other birds around Ma- naus. Insightful comments by Doug Levey and Doug (SUDAM 1984). Stotz improved the manuscript. We thank the World Becauseit has a large range without subspecific Wildlife Fund, the Instituto National de Pesquisasda variation, G. montana appearsto be predisposed Amazonia (INPA), Pew Charitable Trusts, McDonalds to making movements without regard for geo- Corporation, US-AID, the National Park Service, and severalprivate donors for their financial support. This graphical barriers (see discussion in Bierregaard is publication 107 in the BiologicalDynamics of Forest 1990a). Indeed, quail-doves move between Ca- Fragments Project Technical Series. ribbean islands(Robertson and Given 1980). This contrasts markedly with many Amazonian un- LITERATURE CITED derstory birds, which differ at the speciesor sub- ALENCAR,J. C., R. A. ALMEIDA,AND N. P. FERNANDES. specieslevel across most major rivers (see dis- 1979. Fenologiade espkciesflorestais em floresta cussion in Haffer 1985). tropical Gmidade terra firme na AmazBnia central. An exception to the typical pattern of quail- Acta AmazBnica 9:163-198. dove abundance occurredin 1984 and, to a lesser AMERICANORNITHOLOGISTS UNION.’ 1983. Check- extent, 1985 (Fig. 1). This may have been related list of North American birds, 6th ed. Allen Press, Lawrence, KS. to an El Nifio event in 1983, which dramatically BIERREGAARD,R. O., JR. 1990a. Speciescomposition altered rainfall patterns in parts of the neotropics. and trophic organization of the understory bird The 1983 El Nifio stronglyaffected rainfall around community in a central Amazonian terra firme Manaus, but only for three months. It may have forest, p. 217-236. In A. H. Gentry [ed.], Four neotropical rainforests. Yale Univ. Press, New also altered phenology and fruit production else- Haven, CT. where in the range of the Manaus quail-dove BIERREGAARD,R. O., JR. 1990b. Avian communities population. Thus quail-dove abundance may re- in the understory of Amazonian forest fragments, flect not only local availability of food, but also p. 333-343. In A. Keast led.], Biogeographyand the availability in other parts of the population’s ecology of forest bird cbm&nities.- Academic Publishing, The Hague. The Netherlands. range. A similar relationship was proposed by BIERREGAARD,~R.O., JR:, A&D T. E. LOVEJOY. 1989. Pulliam and Parker (1979) to account for vari- Effectsof forest fragmentation on Amazonian un- ation in winter sparrow abundance in the deserts derstory bird communities. Acta AmazBnica 19: of the southwestern US. 215-241. Other birds that feed on canopy fruits have BLAKE,J. G., AND B. A. LOISELLE.199 1. Variation in resourceabundance affects capture rates ofbirds been suspectedof making seasonal movements in three lowland habitats in Costa Rica. Auk 108: near Manaus, but abundance of these birds is 114-130. difficult to quantify. Willis (1977) reported sea- BLAKE,J. G., F. G. STILES,AND B. A. LOISELLE.1990. sonal variation of Amazona autumnalis at Re- Birds of La Selva Biological Station: habitat use, trophic composition, and migrants, p. 161-182. serva Ducke, which we also suspectfor A. fari- In A. H. Gentry [ed.], Four neotropicalrainforests. nosa at our site (pers. observ.). Ramphastos Yale Univ. Press, New Haven, CT. toucans,including many individuals in very poor CRUZ, A. 1974. 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