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BREEDING SEASONALITY IN CENTRAL AMAZONIAN RAINFOREST BIRDS PHILIP C. S TOUFFER, 1,2,3 ERIK I. JOHNSON, 1,2,4 AND RICHARD O. BIERREGAARD, JR. 1 1 Biological Dynamics of Forest Fragments Project, Instituto Nacional de Pesquisas da Amazônia, Manaus 69011, Brazil; and 2 School of Renewable Natural Resources, Louisiana State University Agricultural Center and Louisiana State University, Baton Rouge, Louisiana 70803, USA Abstract.—Although it has long been recognized that many tropical birds do not share the same narrow breeding periods as temperate birds, conventional thinking considers tropical breeding seasons to be discrete periods generally governed by rainfall seasonality. We used a database of >31,000 captures of 104 species collected over 17 years in rainforest near Manaus, Brazil (2.5°S), to examine timing of breeding. e proportion of individuals with active incubation patches peaked at 7% in the dry season, from October through December. e peak was about twice as high as the lowest rate, in the late wet season (April–June). From 9 to 15 families and ≥20 species bred in every month. Many taxa did not conform to the general pattern, instead peaking in the wet season (e.g., Galbulidae, Sclerurinae, Grallariidae, and Formicariidae). Most well-sampled species, even those with strong seasonal peaks, bred at almost any time of year, a pattern also shown by some individual birds that were captured multiple times in breeding condition. Among the 10 species with >50 incubation patches, all bred in at least 9 months, and 7 bred in 11–12 months. Earlier results from the same data set showed extremely protracted molts that regularly overlapped breeding. Collectively, molt and breeding data suggest that the annual cycle of some equatorial birds, particularly suboscines, differs fundamentally from that of temperate species, with much less fixed timing of breeding. Received 30 September 2012, accepted 26 May 2013. Key words: Amazonia, annual cycle, breeding, incubation patch, molt, phenology, rainforest. Sazonalidade de reprodução de aves florestais na Amazônia central Resumo.—Embora tem sido observado que muitas espécies de aves tropicais não possuam períodos reprodutivos tão estreitos quanto às aves da zona temperada, a fenologia é geralmente considerada associada à sazonalidade da precipitação. Usamos um banco de dados de >31000 capturas de 104 espécies coletado durante 17 anos em uma floresta ombrófila densa de terra firme ao norte de Manaus, Brasil (2.5°S) para examinar a sincronia reprodutiva. A proporção de indivíduos com placas de incubação atingiu um pico de 7% na época seca, de outubro a dezembro, duas vezes maior do que a proporção mínima, no final da época chuvosa (abril a junho). Entre 9–15 famílias e >20 espécies nidificaram todos os meses. Muitos taxons não acompanharam o padrão geral, atingindo seu pico na época chuvosa (e.g. Galbulidae, Sclerurinae, Grallariidae, Formicariidae). Muitas espécies bem amostradas, mesmo com picos sazonais bem definidos, nidificaram em quase qualquer mês, um padrão demonstrado também por indivíduos capturados várias vezes com placas de incubação. Entre as 10 espécies com >50 placas de incubação amostradas, todas nidificaram no mínimo ao longo de nove meses, e sete nidificaram entre 11 e 12 meses. Resultados anteriores do mesmo banco de dados mostraram períodos de muda de penas extraordinariamente prolongados que freqüentemente se sobrepuseram à nidificação. Coletivamente, os resultados de muda e de nidificação sugerem que o ciclo anual de algumas aves equatoriais, particularmente suboscines, difere dos padões encontrados para aves temperadas, com períodos de nidificação bem menos fixos. 529 e Auk 130(3):529540, 2013 e American Ornithologists’ Union, 2013. Printed in USA. e Auk, Vol. 130, Number 3, pages 529540. ISSN 0004-8038, electronic ISSN 1938-4254. 2013 by e American Ornithologists’ Union. All rights reserved. Please direct all requests for permission to photocopy or reproduce article content through the University of California Press’s Rights and Permissions website, http://www.ucpressjournals. com/reprintInfo.asp. DOI: 10.1525/auk.2013.12179 3 E-mail: pstouff[email protected] 4 Present address: National Audubon Society, 6160 Perkins Road, Baton Rouge, Louisiana 70808, USA. The apparently intuitive hypothesis that birds (and other or- ganisms) breed at the time of year that allows them to maximize their reproductive success was a major element in the synthesis of life-history theory, even though research and debate generally focused on clutch size (Lack 1950, 1968; Ricklefs 2000). Accept- ing the generality of this idea required accounting not just for ob- servations favorable to the hypothesis, such as the dramatic pulse in breeding in the temperate zone’s spring and summer, but also for winter-breeding finches and other apparent exceptions (Lack 1950). Early experiments that demonstrated avian response to photoperiod cemented the idea that maintaining an annual cycle is critical for reproduction at the optimal time of year, especially when gonads must mature in advance of a peak of resources (Im- melmann 1971). Although these insights came from temperate birds, North American and European ornithologists migrating to the tropics generally described annual peaks in landbird repro- duction, presumed to conform to peaks in resources for feeding nestlings (e.g., Moreau 1950, Skutch 1950, Ward 1969).

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BREEDING SEASONALITY IN CENTRAL AMAZONIAN RAINFOREST BIRDS

PhiliP C. Stouffer,1,2,3 erik i. JohnSon,1,2,4 and riChard o. Bierregaard, Jr.1

1Biological Dynamics of Forest Fragments Project, Instituto Nacional de Pesquisas da Amazônia, Manaus 69011, Brazil; and2School of Renewable Natural Resources, Louisiana State University Agricultural Center and Louisiana State University,

Baton Rouge, Louisiana 70803, USA

Abstract.—Although it has long been recognized that many tropical birds do not share the same narrow breeding periods as temperate birds, conventional thinking considers tropical breeding seasons to be discrete periods generally governed by rainfall seasonality. We used a database of >31,000 captures of 104 species collected over 17 years in rainforest near Manaus, Brazil (2.5°S), to examine timing of breeding. The proportion of individuals with active incubation patches peaked at 7% in the dry season, from October through December. The peak was about twice as high as the lowest rate, in the late wet season (April–June). From 9 to 15 families and ≥20 species bred in every month. Many taxa did not conform to the general pattern, instead peaking in the wet season (e.g., Galbulidae, Sclerurinae, Grallariidae, and Formicariidae). Most well-sampled species, even those with strong seasonal peaks, bred at almost any time of year, a pattern also shown by some individual birds that were captured multiple times in breeding condition. Among the 10 species with >50 incubation patches, all bred in at least 9 months, and 7 bred in 11–12 months. Earlier results from the same data set showed extremely protracted molts that regularly overlapped breeding. Collectively, molt and breeding data suggest that the annual cycle of some equatorial birds, particularly suboscines, differs fundamentally from that of temperate species, with much less fixed timing of breeding. Received 30 September 2012, accepted 26 May 2013.

Key words: Amazonia, annual cycle, breeding, incubation patch, molt, phenology, rainforest.

Sazonalidade de reprodução de aves florestais na Amazônia central

Resumo.—Embora tem sido observado que muitas espécies de aves tropicais não possuam períodos reprodutivos tão estreitos quanto às aves da zona temperada, a fenologia é geralmente considerada associada à sazonalidade da precipitação. Usamos um banco de dados de >31000 capturas de 104 espécies coletado durante 17 anos em uma floresta ombrófila densa de terra firme ao norte de Manaus, Brasil (2.5°S) para examinar a sincronia reprodutiva. A proporção de indivíduos com placas de incubação atingiu um pico de 7% na época seca, de outubro a dezembro, duas vezes maior do que a proporção mínima, no final da época chuvosa (abril a junho). Entre 9–15 famílias e >20 espécies nidificaram todos os meses. Muitos taxons não acompanharam o padrão geral, atingindo seu pico na época chuvosa (e.g. Galbulidae, Sclerurinae, Grallariidae, Formicariidae). Muitas espécies bem amostradas, mesmo com picos sazonais bem definidos, nidificaram em quase qualquer mês, um padrão demonstrado também por indivíduos capturados várias vezes com placas de incubação. Entre as 10 espécies com >50 placas de incubação amostradas, todas nidificaram no mínimo ao longo de nove meses, e sete nidificaram entre 11 e 12 meses. Resultados anteriores do mesmo banco de dados mostraram períodos de muda de penas extraordinariamente prolongados que freqüentemente se sobrepuseram à nidificação. Coletivamente, os resultados de muda e de nidificação sugerem que o ciclo anual de algumas aves equatoriais, particularmente suboscines, difere dos padões encontrados para aves temperadas, com períodos de nidificação bem menos fixos.

— 529 —

The Auk 130(3):529−540, 2013 The American Ornithologists’ Union, 2013.Printed in USA.

The Auk, Vol. 130, Number 3, pages 529−540. ISSN 0004-8038, electronic ISSN 1938-4254. 2013 by The American Ornithologists’ Union. All rights reserved. Please direct all requests for permission to photocopy or reproduce article content through the University of California Press’s Rights and Permissions website, http://www.ucpressjournals.com/reprintInfo.asp. DOI: 10.1525/auk.2013.12179

3E-mail: [email protected] address: National Audubon Society, 6160 Perkins Road, Baton Rouge, Louisiana 70808, USA.

The apparently intuitive hypothesis that birds (and other or-ganisms) breed at the time of year that allows them to maximize their reproductive success was a major element in the synthesis of life-history theory, even though research and debate generally focused on clutch size (Lack 1950, 1968; Ricklefs 2000). Accept-ing the generality of this idea required accounting not just for ob-servations favorable to the hypothesis, such as the dramatic pulse in breeding in the temperate zone’s spring and summer, but also for winter-breeding finches and other apparent exceptions (Lack

1950). Early experiments that demonstrated avian response to photoperiod cemented the idea that maintaining an annual cycle is critical for reproduction at the optimal time of year, especially when gonads must mature in advance of a peak of resources (Im-melmann 1971). Although these insights came from temperate birds, North American and European ornithologists migrating to the tropics generally described annual peaks in landbird repro-duction, presumed to conform to peaks in resources for feeding nestlings (e.g., Moreau 1950, Skutch 1950, Ward 1969).

530 — Stouffer, JohnSon, and Bierregaard — auk, Vol. 130

Bierregaard [2001] for a general description of the site, and Stouffer et al. [2006] and Johnson et al. [2012] for descriptions of the net-ting protocol). We compiled data on breeding condition from birds banded at the BDFFP during 17 years of banding between 1982 and 2009 (excluding 1994–1998 and 2001–2006). Data were collected at 30 different sampling sites within an area of about 500 km2. For all analyses, we used only captures for which presence or absence of an active incubation patch was unambiguously noted. The in-cubation patch (or brood patch) is characterized by a region of the breast and belly with loss of downy feathers, increased skin vas-cularization, and development of edematous subcutaneous tissue (Jones 1971). Although its development and duration vary among species, the incubation patch generally presents externally obvious edema and vascularization only during egg laying, incubation, and the early nestling stages (Lloyd 1965, Jones 1971, Holcomb 1975). By the time of fledging, the former incubation patch may be identified by the presence of scaly skin (e.g., Lloyd 1965), but our experience suggests that this varies among species and may be difficult to iden-tify unambiguously, so we did not include this criterion. Incuba-tion patches in males are typically less developed than in females, although they remain notably vascularized in species in which both sexes incubate (Jones 1971), including almost all the antbirds, oven-birds, and woodcreepers that dominate our sample (Krabbe and Schulenberg 2003, Marantz et al. 2003, Remsen 2003). Males that do not incubate do not develop incubation patches; we excluded captures of known males for these species (e.g., manakins and tan-agers). Some monomorphic species in our sample are known to have incubation only by the female. For these species (Phaethornis bourcieri, P. superciliosus, Dendrocincla fuliginosa, D. merula, Cer-thiasomus stictolaemus, and Mionectes macconnelli), our estimates of the proportion of birds breeding will be low. For another sub-set of monomorphic species (e.g., some flycatchers, vireos, wrens, and thrushes), it is unknown whether males develop incubation patches, although females are assumed to incubate alone, as they do in temperate species (Fitzpatrick 2004, Collar 2005, Kroodsma and Brewer 2005, Brewer and Orenstein 2010; but see Sick [1993:554] for the suggestion that males may incubate in vireos). Our analy-sis includes all individuals for these species; resultant estimates of proportion of individuals in breeding condition will be biased low for these monomorphic species in which males do not incubate. Finally, although juveniles were excluded from analysis whenever possible, we generally do not know when these species are first ca-pable of breeding, so our analysis certainly includes birds in adult-like preformative plumage that are actually too young to breed.

We excluded same-day recaptures to avoid counting the same breeding individual twice. We typically netted at any given site for a single day at 3-week or greater intervals (usually 1–2 months), so we assume that we did not detect the same incubation patch (or breeding attempt) more than once for a given individual. Many of the small understory birds in our sample probably can renest after failure in <2 weeks (Gill and Haggerty 2012). Rotation among sites also insured that we sampled multiple sites at the same intervals throughout the landscape. Taxonomy is based on the AOU South American Classification Committee checklist (Remsen et al. 2013).

We determined rainfall seasonality on the basis of rainfall collection data from 1987 through 1999 at the BDFFP (Laurance 2001). Seasonal patterns in that data set correspond well to a lon-ger time series ending in 1992 from Reserva Ducke, just outside the city of Manaus (Stouffer and Bierregaard 1993).

Despite these early results describing reproductive seasonality, there has been little effort to understand the degree of seasonal-ity within tropical populations or the variation among species within tropical communities (but for examples from rainforests, see Fogden 1972, Stiles 1980, Wikelski et al. 2003a). This question has important implications for resource use, interspecific interac-tions, and population processes (e.g., Karr 1976, Blake and Loiselle 1991, Poulin et al. 1992). Moreover, seasonality requires a proximal mechanism, such as response to photoperiod, and has expected physiological consequences (e.g., Hau et al. 1998, Wikelski et al. 2000; also see Borchert et al. 2005, Goymann et al. 2012).

What would be the advantage of seasonal breeding by birds in the vast rainforests of lowland Amazonia? Through most of the Amazon, wetter months predictably have twice the rainfall of drier months (Salati 1985). Presumably, responding to seasonal changes would be advantageous in the face of predictable sea-sonal variation in resources associated with rainfall, as has been convincingly demonstrated for Spotted Antbirds (Hylophylax naevioides) in Panama (Wikelski et al. 2000). Breeding at the ap-propriate time may also reduce weather-related nest failure: bur-rows may be vulnerable to flooding, and open cups may become saturated by heavy rains, risks that have been applied post hoc to explain timing of breeding (Moreau 1950, Oniki and Willis 1983, Rasmussen and Collar 2002).

Despite significant rainfall seasonality in lowland Amazonia, the importance of that seasonality for limiting reproduction by birds has not been demonstrated. In central Panama, where the mechanism of seasonal breeding has been best described for Neo-tropical species, the dry season is severe enough that some trees are deciduous. Several months may pass with little or no rain-fall, limiting production of new leaves and insects (Croat 1978, Wolda 1978). Only in parts of eastern Amazonia is the dry season this pronounced. In fact, data from a site in southern Amazonia show a peak in net primary productivity in the dry season (Som-broek 2001). Reduced seasonal variation in resource availability would suggest that the cost of imprecise timing of reproduction would be lower in Amazonia (although phenological data for spe-cific resources would be more directly relevant than just rainfall or productivity). Furthermore, conservative reproductive effort (Stutchbury and Morton 2001; Wikelski et al. 2003a, b) and ener-getic demands of protracted molts (Johnson et al. 2012) may make breeding more opportunistic among individuals of Amazonian species (e.g., Tallman and Tallman 1997), resulting in asynchro-nous or aseasonal breeding at the level of the population.

Before we can address the advantage of breeding at a particu-lar time for a particular species, we need to demonstrate that sea-sonality exists at all. Here we use a large, long-term data set of incubation patches from birds captured at a single central Amazo-nian site to describe timing of breeding in understory birds. Our main questions are (1) when do understory birds breed, (2) how does variation in breeding intensity vary with rainfall seasonality, and (3) are seasonal patterns shared among related species?

Methods

Bird samples come from standardized understory mist netting at the Biological Dynamics of Forest Fragments Project (BDFFP), ~80 km north of Manaus, Brazil (2°30′S, 60°W). The BDFFP includes con-tinuous terra firme forest and forest fragments (see Gascon and

July 2013 — amazonian Breeding Phenology — 531

We wanted to know whether the number of breeding spe-cies or families varied over the course of the year. Number of cap-tures varied among months (n = 1,302–3,873, mean = 2,657), so we could not simply tally the number of breeding taxa given this seasonal variation in sampling effort. To standardize sampling, we used a Monte Carlo approach in SAS (SAS Institute, Cary, North Carolina) by randomly selecting (without replacement) 1,000 cap-tures with incubation patch data for each month, then counting the number of breeding species or families in the random sample. We performed this resampling 100 times for each month.

To analyze whether monthly variation in presence of incuba-tion patches was due to variation among families in their timing of breeding, we used model selection based on logistic regression with SAS PROC GLIMMIX with a logit link. For the seven most common families or subfamilies (see below), we compared three competing models using Akaike’s information criterion (AIC; Burnham and Anderson 2002) to examine whether presence of an incubation patch was best predicted by (1) family alone; (2) fam-ily and month; or (3) family, month, and family * month interac-tion. Model 1 indicates whether individuals in some families are more likely to have incubation patches than individuals in other families, an effect we expect given the differences in incubation period and failure rate, among other factors. Model 2 includes the main effect of family, as in model 1, but also adds the main effect of month. The AIC value of model 2 can be compared with that of model 1 to determine whether adding the monthly pattern in-creases the information of the model. Support for model 2 over model 1 would suggest that some months have higher breeding activity than others. Model 3 includes the same family and month effects as model 2 but adds a family * month interaction. Support for model 3 over models 1 and 2 would indicate that families differ not just in their likelihood of having incubation patches, but also in the seasonality of those incubation patches.

We analyzed broader seasonal patterns, rather than monthly variation, by dividing the year into a wet season (1 January–15 June) and a dry season (16 June–31 December) corresponding to the long-term rainfall pattern (Fig. 1). The transition to the dry

season typically occurs in June, with a marked difference between the beginning and the end of the month (P. C. Stouffer et al. pers. obs.). Thus, we included the first half of June with the wet season, and the second half with the dry season. Considering just two sea-sons allowed us to expand the analysis to taxa with fewer incu-bation patches, including individual species. This rainfall-based calendar also corresponds almost exactly to increasing (dry sea-son) versus decreasing (wet season) day length. We tested whether there was a seasonal effect on the proportion of individuals with incubation patches using logistic regression with GLIMMIX (taxa with >20 incubation patches) or G-tests (taxa with 6–20 incuba-tion patches; taxa with ≤5 incubation patches could not be ana-lyzed with a G-test). We performed these analyses for families and for individual species, although we excluded two poorly sampled families with 6 incubation patches (Columbidae and Cardinali-dae) from the family-level analysis.

Results

General seasonality of breeding.—We recorded at least one indi-vidual with an incubation patch for 104 species. For these species, we examined a total of 31,884 captures, of which 1,917 had incu-bation patches. Breeding was detected in all months, but the peak months, with >7% of birds in breeding condition, were October through January (Fig. 1). April, May, and June all had <4% of birds in breeding condition. This corresponds to a general pattern of increasing breeding over the course of the dry season, from July through December, followed by decreasing breeding through the wet season, from January through June.

The pronounced peak in individuals breeding from October through January conformed to a peak in number of species breed-ing (Fig. 2). When we used resampling to account for unequal sampling effort among months, however, the peak became much smaller, with about 20–40 species breeding each month. Resam-pled data from families showed a similar pattern; 9–15 families bred each month. Seasonal variation in the overall proportion of birds in breeding condition appeared to be driven by high capture rates of

fig. 1. Percentage of captures of birds at the Biological Dynamics of Forest Fragments Project (Brazil), with incubation patches based on captures from 1982 to 2009 (solid line) and monthly rainfall from 1987 to 1999 (from Laurance 2001).

532 — Stouffer, JohnSon, and Bierregaard — auk, Vol. 130

a few species that breed in the dry season, not a strong preference for the dry season across species. In particular, the increase in spe-cies breeding in the early dry season, July and August, appeared to be due to the addition of species within families, in that the number of families breeding remained constant between June and August.

Variation among taxa.—We considered whether monthly breeding activity varied among taxonomic groups. For the seven taxa (families, or subfamilies within Furnariidae) with ≥40 incu-bation patches, model 3, which included a taxon * month interac-tion (number of parameters = 84, –2 log likelihood = 11,664.51, DAIC = 0), was more informative than the model with only the taxon effect (model 1: number of parameters = 7, –2 log likelihood = 12,048.92, DAIC = 230) or the model with the taxon effect and the month effect but without their interaction (model 2: number of pa-rameters = 18, –2 log likelihood = 11,823.13, DAIC = 26.6). Support for model 3, despite its much greater parameterization, demon-strates that seasonality of breeding varied among families (Fig. 3). Although most families conformed to the general pattern of reduced breeding at the end of the wet season and beginning of the dry season, the pattern varied somewhat. For example, breeding in Polioptilidae was high in April and May and lowest in August and September, whereas breeding in Dendrocolaptinae was lowest from April to June but peaked in October and November.

We found nearly equal numbers of taxa preferring the wet or dry season (Table 1). Formicariidae, Galbulidae, Grallariidae, and Sclerurinae strongly favored the wet season, with at least twice the proportion of birds in breeding condition compared with the dry season. Especially pronounced were the Galbulidae, Grallariidae, and Sclerurinae, which were all at least 4× more likely to be in breeding condition in the wet season. In comparison, the Dendro-colaptinae, Furnariinae, Pipridae, Thamnophilidae, and Tityridae favored the dry season, although seldom by as much of a difference as the species that favored the wet season. The strongest dry-sea-son association was in the Pipridae, which were about 3× more likely to be in breeding condition in the dry season.

We found considerable variation in temporal pattern among the species with the largest samples of birds in breeding condition (Fig. 4 shows examples). For example, although most species de-clined in breeding frequency from the end of the wet season into the early dry season, Hypocnemis cantator did not. Glyphorynchus spirurus declined gradually through the early dry season before increasing again in the second half of the dry season. Xiphorhyn-chus pardalotus had an abrupt peak in the dry season, with almost no breeding by January. Willisornis poecilinotus increased in frequency more gradually over the course of the dry season, only declining from the middle to the end of the wet season. Mionectes macconnelli had a peak in the middle of the wet season, with almost no breeding for the rest of the year.

Of the 56 species with ≥6 incubation patches, 7 showed more breeding in the wet season, and 16 favored the dry season (Appen-dix). Some of these differences were quite dramatic, such as the 45 incubation patches of C. stictolaemus that were all in the dry sea-son. In other cases, the significant differences largely reflect the power of a large sample size for species with only slight seasonal variation, such as for G. spirurus. Conversely, it is interesting to note that the species with the second-highest number of incuba-tion patches, W. poecilinotus, showed no seasonal difference in this analysis, probably because its breeding season spanned the end of the wet season and the beginning of the dry season. It was about twice as likely to be in breeding condition from January to March as from May through August (Fig. 4).

Despite the seasonal patterns, many species showed evidence of breeding for all or most of the year, especially the dry season. Number of months with breeding activity clearly scaled with sample size (Appendix); the three species with ≥100 incubation patches all showed evidence of breeding in every month, whereas only one species (Myrmotherula axillaris) with <80 incubation patches bred in every month. Even so, only two species with a sample of ≥20, C. stictolaemus and Mionectes macconnelli, did not breed in at least 8 months. Most gaps in breeding activity were in

fig. 2. Number of species and families of birds at the Biological Dynamics of Forest Fragments Project (Brazil), with incubation patches in each month. Estimated values (means ± SD) are from 100 resamples of 1,000 captures month–1.

July 2013 — amazonian Breeding Phenology — 533

the wet season. In fact, of the species with ≥20 incubation patches, only M. macconnelli and Turdus albicollis did not show evidence of breeding in every month from July through November.

A few individuals were captured with incubation patches multiple times (Fig. 5). For 100 individuals of 27 species that were captured in at least two breeding attempts within a 1-year interval,

fig. 3. Seasonality of breeding of birds at the Biological Dynamics of Forest Fragments Project (Brazil), for taxa with >40 incubation patches. Curves are smoothed by plotting running averages weighted as the value of the present month (50%), the preceding month (25%), and the following month (25%).

taBle 1. Seasonal breeding activity of birds from the Biological Dynamics of Forest Fragments Project (Brazil), for taxa with ≥7 incubation patches. Shown are total number of incubation patches, months with incubation patches, and percentage of captures with incubation patches in the wet and dry seasons. Asterisks refer to sig-nificant seasonal differences based on logistic regression (n > 20) or G-tests (6 < n < 21), indicated in the column with the higher proportion (*P < 0.05, **P < 0.01, ***P < 0.001; see text for details).

Incubation patches Percent incubation patches

Taxon Captures n Months Wet Dry

Trochilidae (hummingbirds) 1,356 25 9 1.8 1.9Galbulidae (jacamars) 397 7 7 4.6 * 0.7Bucconidae (puffbirds) 257 14 8 8.9 3.9Thamnophilidae (antbirds) 11,566 816 12 6.2 7.4 *Conopophagidae (gnateaters) 152 13 7 7.6 9.1Grallariidae (antpittas) 75 10 7 25.9 * 6.3Formicariidae (antthrushes) 413 40 11 14.1 * 7.0Dendrocolaptinae (woodcreepers) 4,992 386 12 5.2 8.8 ***Furnariinae (ovenbirds) 1,403 100 12 3.7 8.7 ***Sclerurinae (leaftossers) 471 26 9 13.3 *** 1.6Tyrannidae (flycatchers) 3,490 122 12 2.8 3.8Pipridae (manakins) 2,315 149 12 2.8 8.0 ***Tityridae (tityras) 601 15 5 0.0 3.6 ***Vireonidae (vireos) 401 25 8 3.3 7.1Troglodytidae (wrens) 643 30 9 4.0 5.0Polioptilidae (gnatcatchers) 502 41 11 9.7 7.6Turdidae (thrushes) 774 32 9 6.2 3.2Thraupidae (tanagers) 578 33 9 4.1 6.5

534 — Stouffer, JohnSon, and Bierregaard — auk, Vol. 130

the mean time between captures with incubation patches was 99 days. Intervals were often in the range of 1–4 months, possi-bly because of renesting after failure. Many birds were breeding again after 4–7 months, almost certainly reflecting breeding at-tempts in both the wet and dry seasons. Two species, G. spirurus

and Gymnopithys rufigula, had >10 individuals recaptured with brood patches after <1 year (Fig. 5). Most G. rufigula bred 2–3 months after their first capture, although some bred 5–6 months later. By contrast, most G. spirurus bred again between <1 and 3 months later, again with some individuals breeding 5–7 months

fig. 4. Examples of annual cycles from five common species of birds from the Biological Dynamics of Forest Fragments Project (Brazil). Monthly val-ues are from running averages based on the values of the present month (50%), the preceding month (25%), and the following month (25%).

fig. 5. Intervals between captures of birds from the Biological Dynamics of Forest Fragments Project (Brazil), for all individuals of all species cap-tured with an incubation patch more than once. Hollow bars show all individuals of all species recaptured at intervals of <1 year. Light gray bars show Glyphorynchus spirurus captured within <1 year. Dark gray bars show Gymnopithys rufigula captured within <1 year. Black bars show all individuals captured at intervals of >1 year. For birds captured at intervals of >1 year, binning is by Julian days between attempts (e.g., a bird with an incubation patch on 1 September 2007 and 30 September 2008 would be binned as <30 days).

July 2013 — amazonian Breeding Phenology — 535

later. For these birds captured within a year, the second detection with a brood patch is possibly influenced by the timing or out-come of the first attempt. Certainly, additional breeding attempts may have gone undetected before, after, or between those we de-tected. Another 26 birds were captured twice with brood patches at an interval of >1 year. In some cases, these birds bred at about the same time of year (Julian dates differing by <61 days or >300 days), but these birds also showed evidence of breeding in opposite rainfall seasons (Julian dates differing by 121–240 days). We cau-tion that these data were collected opportunistically, not in a way that allows definitive explanation of time required to renest, typi-cal breeding intervals, or other potentially interesting questions. Nevertheless, they support the observation that many birds breed without strong fidelity to a particular time of year.

discussion

Our results from ~2,000 incubation patches collected over 17 years lead to several generalizations about breeding seasonality of forest understory birds in the central Amazon. First, there is no major sea-sonal peak in breeding intensity across the entire community. There were more individuals in our sample breeding in the dry season, from October through December (Fig. 1), but this represented only a modest increase in number of species compared with the lowest point of the year, the late wet season. On the other hand, the nadir of breeding activity for almost all species was in the late wet season and very early dry season. Second, some species showed an associa-tion with a particular time of year, but these peaks varied among species and varied temporally between the wet and the dry season (Fig. 4). Third, most species with large samples showed evidence of breeding in almost every month. Data from individual birds also re-vealed breeding in both rainfall seasons, 3 to 6 months apart (Fig. 5). A subset of species with large samples, however, appeared to avoid breeding at certain times of year (Appendix).

Timing of breeding.—How is timing of breeding regulated in central Amazonian birds? Clearly, few species follow the Cen-tral American pattern of most birds breeding after the onset of the rainy season (e.g., Stiles 1983). Further, the proportion of birds in breeding condition at the height of the breeding season is much lower than in some Neotropical species with compara-ble data, which suggests that the Amazonian breeding season is more protracted (Levey 1988, Marini and Durães 2001). For ex-ample, suboscine insectivores in southern Brazil show a peak in brood patches with >80% of individuals breeding in November, early in the wet season. Our monthly proportions for similar taxa seldom pushed past 20% (Fig. 3). We found no general pattern of increased breeding as day length increases; much breeding occurs in the wet season, when days are becoming shorter. On the other hand, the period with the lowest breeding activity corresponds to both the shortest day length and the end of a pronounced wet sea-son. Recent work has shown that adjacent equatorial populations of Rufous-collared Sparrows (Zonotrichia capensis) can breed at quite different times (Moore et al. 2006). These populations have asynchronous endocrine responses associated with their different breeding seasons (Moore et al. 2006). These changes parallel en-docrine changes in temperate birds whose breeding is regulated by photoperiod, indicating that multiple environmental cues can

produce seasonal breeding. Our results suggest that these non-photoperiodic cues, or birds’ response to them, must vary among species, or perhaps even among individuals, a result that has been described for tropical birds since at least 1950 (Skutch 1950) and is consistent with hormonal mechanisms for non-photoperiodic regulation of breeding (Dawson and Sharp 2007).

We do not know how much of the variation that we found, particularly within species, could be driven by variation among years in rainfall (or other environmental variables). Unfortunately, we have too few brood patches within years to examine, for exam-ple, whether wet-season breeding species begin breeding earlier in years when daily heavy rains start in November rather than Janu-ary. Alternatively, it may also be that individuals within a popu-lation tend to molt and breed at the same time from year to year, as in a Costa Rican hummingbird (Phaethornis; Stiles and Wolf 1974), although this is not well supported by our data from indi-viduals captured more than once with incubation patches. There may also be subtle patterns of seasonality to be revealed with more data, such as the bimodal seasonality of a montane furnariid in Ecuador that breeds at the beginning and at the end, but not in the middle, of a long wet season (Greeney 2010).

Possible roles of multiple nesting attempts and molt.—Rela-tively few birds were in breeding condition in our sample. Few spe-cies showed more than 10–15% of individuals with brood patches during their most favorable season for breeding (Appendix). Even so, our data are consistent with many birds attempting to breed multiple times over the course of a year. Incubation patches are a conservative measure of breeding, in that they are conspicuous only during the period of active incubation and brooding of young nestlings. Most of our study species have relatively few downy feathers on the breast, making the initial loss of these feathers a less obvious stage than in many temperate species, especially for males. We also excluded possible old incubation patches from our sample. Thus, the period we included here would correspond roughly to the time of ovulation of the last egg through a few days after hatching, or a period of about 14–28 days for most of our species. For a species that breeds just once a year, the expecta-tion would be that about 4–8% of individuals in a random sample would be in breeding condition. Few species were that low, and many were 2–3 times higher, which suggests at least three breed-ing attempts (or the equivalent number of days of incubation). Our sample also includes some birds that had not yet reached breeding age, and males that do not develop brood patches in some sexually monomorphic species. These demographic classes mask the pro-portion of adult females that are actively breeding. Furthermore, incubating females would be expected to move less, resulting in lower capture probability than at other stages of the seasonal cy-cle. Collectively, these observations suggest that females typically lay multiple clutches, probably in response to high nest failure. Although few quantitative data are available to test the assertion that tropical species suffer higher nest failure than temperate spe-cies (discussed in Brawn et al. 2011), the weak seasonal pattern that we observed may be due to repeated nesting that may stretch over many months.

Protracted breeding with multiple nesting attempts proba-bly means that even if important resources for feeding nestlings were strongly seasonal, most individuals would not be able to take

536 — Stouffer, JohnSon, and Bierregaard — auk, Vol. 130

advantage of them. Thus, it seems simplistic to say that these birds conform to the classic view that appropriate timing of reproduc-tion is under strong selective pressure as a means of maximiz-ing reproductive success through successfully feeding nestlings. Rather, birds may be under selective pressure to be plastic in their breeding, perhaps only avoiding certain periods when chances of success are particularly low (e.g., Fogden 1972). Tropical birds tend to lack the photorefractory period of temperate birds (Beebe et al. 2005, Bentley et al. 2007; but see Gwinner and Scheuerlein 1999), which also suggests that their breeding can respond to ase-asonal opportunities. Relatively low energetic demands resulting from protracted molt, especially when combined with high nest predation, may also favor opportunistic breeding, even during molt (also see Foster 1974).

Molt–breeding overlap occurs in many species at our site, although it is absent or very rare in other species (Johnson et al. 2012). Considering these two stages of the annual cycle together, molting and breeding, may help explain the pattern of breeding seasonality that we described. Additional context for the pattern includes the long duration of molt for most of our study species (seldom <4 months, and often >6 months; Johnson et al. 2012) and extended parental care expected for tropical species (Russell et al. 2004). The most straightforward pattern is for species that breed, then molt, as is also the case for most temperate-zone birds. These species, mainly oscines and flycatchers, but also some other subos-cines, apparently do not initiate breeding again until after comple-tion of molt, which results in an annual cycle with distinct phases. Perhaps these species initiate breeding whenever conditions are appropriate following completion of molt, rather than waiting for some seasonal cue (see discussion of physiological mechanisms in Williams 2012). For individuals that are forced to renest repeat-edly, their next breeding attempt may be delayed compared with individuals who were successful earlier in the previous year. Thus, these species may show seasonality but still breed throughout the year at the level of the population or individual (e.g., G. spirurus; Fig. 5). More data from individual birds could be used to exam-ine whether the sequence of multiple nesting attempts followed by molt affects the timing of breeding and molt in the following year.

For species with molt–breeding overlap, molt may be ex-tremely protracted (e.g., >300 days in Pithys albifrons; Johnson et al. 2012). These species minimize their daily energetic investment in molt but are often molting while they breed. For these species, and a larger subset of species with less frequent molt–breeding overlap and less protracted molt, successful breeding may be more linked to minimizing energetic demands during a period of low resources (or perhaps during a time of the year when heavy rain-fall makes foraging more difficult) rather than capitalizing on a period of higher resources for breeding. This view corresponds to the idea that tropical birds tend to live a low-energy lifestyle that minimizes energy requirements in the face of relatively con-stant conditions, high nest failure, and prioritization of mainte-nance (Ghalambor and Martin 2001, Wikelski et al. 2003b, Russell et al. 2004, Wiersma et al. 2007, Williams et al. 2010; but see Gill and Haggerty 2012). Unfortunately, we cannot evaluate seasonal effects on reproductive success from our sample; perhaps varia-tion among species in within-year variance in reproductive suc-cess drives stronger seasonality by some species than by others.

Additional factors that influence timing of breeding.—Ecolog-ical or evolutionary pressures on timing of breeding might include avoiding competition, either among closely related species, among species with similar foraging strategies, or with nonbreeding mi-grants. Although it seems unlikely to drive breeding seasonality, the general lack of extrapair copulations and intraspecific brood parasitism in tropical forest birds would be an expected conse-quence of asynchronous breeding within a population (reviewed in Stutchbury and Morton 2001). Our analysis shows that timing of breeding differs among families, which suggests that closely related species are clustered, not overdispersed, with respect to breeding, but we do not know whether this is related to a shared resource base or phylogenetic conservatism. We do not have enough information on diet to evaluate competition on the basis of foraging, but evidence so far does not suggest that competition drives timing in the ground-foraging Myrmornis, Hylopezus, For-micarius, and Sclerurus, representatives of four different clades that all breed preferentially in the wet season. Rather, for these species, breeding probably coincides with the period of highest litter arthropod abundance (Pearson and Derr 1986). Compe-tition with migrants can be excluded as a factor at our site be-cause of their low density in forest (Cohn-Haft et al. 1997, Johnson et al. 2011), but we wonder whether it may be important in Central America, accounting for much stronger breeding seasonality at sites with copious year-round rainfall, such as La Selva, Costa Rica (Stiles 1983). At La Selva, breeding peaks in the wet season, which also matches withdrawal of migrants to North America.

Summary.—Although we now have a better description of the pattern of breeding from a long-term sample in equatorial Ama-zonian rainforest, much remains to be learned about the annual cycle of these birds. We cannot evaluate fitness consequences of breeding at different times of year for birds in our sample, but the broad lack of synchrony across and even within species suggests that the annual cycle may generally not be optimized for breeding at a particular time of year. Regulation of breeding, including the annual clock (e.g., Goymann et al. 2012), response to environmen-tal cues (e.g., Hau et al. 1998), energetic and physiological interac-tion with protracted molt (e.g., Johnson et al. 2012), and possibly the hormonal basis of initiating and suspending breeding (Daw-son and Sharp 2007) merit additional attention in Amazonian birds for comparison not only with temperate species, but also with other tropical species that show different seasonal patterns than we found.

AcknowledgMents

We thank the many banders, assistants, and mateiros who helped collect these data. Logistical support from the Biological Dy-namics of Forest Fragmentation Project, Brazil’s Instituto Nacio-nal de Pesquisas da Amazônia, and the Smithsonian Institution made this research possible. Funding for the project has also been provided by the World Wildlife Fund–U.S., the MacArthur Foundation, the Andrew W. Mellon Foundation, U.S. Agency for International Development, U.S. National Aeronautics and Space Administration, Brazil’s Ministry for Science and Technol-ogy, U.S. National Science Foundation (LTREB 0545491), Sum-mit Foundation, Shell Oil, Citibank, Champion International,

July 2013 — amazonian Breeding Phenology — 537

the Homeland Foundation, and the National Geographic Society. The manuscript benefited from helpful suggestions by E. E. De-Leon, H. F. Greeney, C. A. Lindell, K. Mokross, L. L. Powell, J. D. Wolfe, the LSU Bird Lunch group, and two anonymous reviewers. M. Kaller helped unleash the power of GLIMMIX. K. Mokross tidied the Portuguese abstract. This is publication 620 of the Biological Dynamics of Forest Fragments Project Technical Series and 28 in the Amazonian Ornithology Technical Series of the INPA Zoological Collections Program. This article was approved for publication by the Director of the Louisiana Agricultural Experimental Station as manuscript no. 2013-241-9565.

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aPPendix. Seasonal breeding activity for species with ≥6 incubation patches from the Biological Dynamics of Forest Fragments Project (Brazil). Shown are the total number of incubation patches, the months with in-cubation patches, and the percentage of captures with incubation patches in the wet and dry seasons. Plus signs indicate sexually monomorphic species in which the male probably does not incubate, for which our sampling underestimates the proportion of females with incubation patches). Asterisks refer to significant seasonal differences, indicated in the column with the higher proportion (*P <0.05, **P < 0.01, *** P < 0.001; see text for details).

Incubation patches

Percent incubation patches

Species Captures n Months Wet Dry

Glyphorynchus spirurus 2,116 159 12 10.0 ** 6.5Willisornis poecilinotus 1,844 136 12 8.1 7.0Gymnopithys rufigula 1,082 120 12 7.5 12.4 *Dixiphia pipra 1,627 95 11 2.2 7.4 ***Percnostola rufifrons 807 81 12 8.6 10.7Pithys albifrons 2,332 75 11 3.7 3.1Thamnomanes ardesiacus 1,029 71 9 2.3 8.8 ***Thamnomanes caseius 802 61 10 2.7 9.6 **Hypocnemis cantator 559 55 11 10.0 9.8Xiphorhynchus pardalotus 986 53 9 0.9 7.5 ***Myrmeciza ferruginea 251 49 10 18.5 20.0Certhiasomus stictolaemus+ 591 45 6 0.0 12.1 ***Myrmotherula longipennis 583 44 11 7.6 7.5Dendrocincla merula+ 561 44 10 3.8 9.4 *Microbates collaris 488 40 11 9.2 7.8Formicarius colma 364 39 11 15.9 * 7.5Dendrocincla fuliginosa+ 290 35 9 4.8 15.1 *Automolus infuscatus 511 34 11 4.5 7.8Turdus albicollis+ 774 32 9 6.2 3.2Mionectes macconnelli+ 1,257 31 4 5.0 ** 1.6Myrmotherula axillaris 418 26 12 6.1 6.3Hylophilus ochraceiceps+ 373 23 8 2.5 7.1Xenops minutus 280 23 8 2.5 10.5 *Corythopis torquatus+ 328 20 8 3.7 7.2Lepidothrix serena 328 19 9 5.9 5.7Tachyphonus surinamus 309 19 7 6.4 6.1Thamnophilus murinus 207 19 9 6.6 10.3Myiobius barbatus 629 18 6 1.3 3.4Ceratopipra erythrocephala 180 18 5 0.0 15.1 ***Myrmotherula menetriesii 313 17 6 1.3 6.8Cyphorhinus arada+ 279 17 8 7.7 5.6Sclerurus rufigularis 271 17 9 14.3 ** 2.7Corapipo guttaralis 180 17 6 6.9 9.9Philydor erythrocercum 125 15 6 0.0 16.9 ***Phaethornis superciliosus+ 666 14 9 2.0 2.2Schiffornis olivacea 590 14 4 0.0 3.4 **Platyrinchus coronatus 359 14 6 0.0 5.3 **Dendrocolaptes certhia 101 14 6 8.3 15.6Epinecrophylla gutturalis 568 13 8 2.0 2.4Isleria guttata 207 13 6 8.9 4.7Conopophaga aurita 152 13 7 7.6 9.1Malacoptila fusca 224 12 7 7.3 4.5Myrmornis torquata 172 12 6 11.7 4.5Hylexetastes perrotii 82 12 6 0.0 19.1 **Platyrinchus saturatus+ 375 11 5 2.3 3.2

(continued)

540 — Stouffer, JohnSon, and Bierregaard — auk, Vol. 130

Incubation patches

Percent incubation patches

Species Captures n Months Wet Dry

Automolus rubiginosus 164 11 7 10.9 5.1Automolus ochrolaemus 138 11 6 0.0 11.2 **Campyloramphus procurvoides 67 10 7 14.8 15.0Ramphocelus carbo 225 9 7 2.2 5.1Hylopezus macularius 40 7 4 40.0 * 4.0Galbula albirostris 387 6 4 4.6 ** 0.4Geotrygon montana 316 6 3 1.6 2.4Schistocichla leucostigma 149 6 5 4.8 3.7Deconychura longicauda 119 6 4 0.0 8.2 *Frederickena viridis 94 6 5 4.4 7.0Sclerurus mexicanus 85 6 3 16.2 ** 0.0

aPPendix. Continued.