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Revista de Biología Tropical

versión On-line ISSN 0034-7744versión impresa ISSN 0034-7744

Rev. biol. trop vol.67 no.2 San José abr. 2019

http://dx.doi.org/10.15517/rbt.v67i2supl.37252 

Artículo

Effect of El Niño and La Niña on abundance of frugivorous and nectarivorous terrestrial birds in three tropical forests

El efecto de El Niño y La Niña sobre la abundancia de aves frugívoras y nectarívoras terrestres en tres bosques tropicales

Gilbert Barrantes1 

Luis Sandoval1 

1 Escuela de Biología, Universidad de Costa Rica, Montes de Oca, San José, Costa Rica; gilbert.barrantes@gmail.com; biosandoval@hotmail.com * Correspondence

Abstract

El Niño and La Niña climatic oscillations have dramatic effects on population dynamics and community structure of different animals. For marine birds, El Niño phenomenon drastically increases their mortality and reduces their reproductive success. In terrestrial ecosystems, the lack of long-term longitudinal data limits our understanding of the impact of El Niño and La Niña on bird populations and communities. We analyzed changes in abundance of frugivorous (large, medium, and small) and nectarivorous birds on three tropical forest types (lowland, premontane and montane) during El Niño, La Niña and neutral years using data from 16 Christmas’ Bird Counts in Costa Rica. Abundance of large and medium size frugivores increased during La Niña events, and the abundance of nectarivores during El Niño in the lowland forest, but neither of these events affected the abundance of small frugivores. In the montane forest, abundance of all four bird groups increased during El Niño, but decreased during La Niña events. Abundance of large, and small frugivores increased in the premontane forest during La Niña events, but other bird groups were not affected by La Niña. The abundance of small frugivores also increased during El Niño. We hypothesize that changes in abundance of frugivores and nectarivores during La Niña and El Niño events is probably correlated with fluctuations in food resources as it has been reported for other terrestrial tropical ecosystems.

Key words: El Niño; La Niña; nectarivorous birds; frugivorous birds; climatic change

Resumen

Las oscilaciones climáticas causadas por el fenómeno de El Niño y La Niña tienen efectos drásticos sobre la dinámica de las poblaciones y la estructura de las comunidades. Para aves marinas, el fenómeno de El Niño incrementa drásticamente su mortalidad y reduce su éxito reproductivo. En ecosistemas terrestres, la falta de datos a largo plazo limita nuestro entendimiento sobre el impacto de El Niño y La Niña sobre la dinámica de las poblaciones y comunidades de aves. Nosotros analizamos los cambios en la abundancia de aves frugívoras (grandes, medianos y pequeños) y nectarívoras en tres tipos de bosque tropical (lluvioso de tierras bajas, premontano y montano) durante los años de El Niño, La Niña, y años neutrales usando datos de al menos 16 conteos de navidad (Christmas’ Bird Counts) en Costa Rica. La abundancia de frugívoros grandes y medianos incrementó durante los años de La Niña, y la abundancia de nectarívoros durante el Niño en el bosque lluvioso de tierras bajas, pero ninguno de estos eventos afectó la abundancia de frugívoros pequeños en este bosque. En el bosque montano, la abundancia de los cuatro grupos de aves incrementó durante los años de El Niño, pero disminuyó durante los años de La Niña. La abundancia de frugívoros grandes y pequeños aumentó en el bosque pre-montano durante los años de La Niña; sin embargo, la abundancia de los frugívoros medianos y los nectarívoros no fue afectada por los eventos por La Niña o El Niño. La abundancia de frugívoros pequeños también aumentó durante El Niño en este bosque. Proponemos la hipótesis de que los cambios en la abundancia de las aves frugívoras y nectarívoras reflejan fluctuaciones en el recurso alimentario, como ha sido reportado en otros ecosistemas terrestres tropicales.

Palabras clave: El Niño; La Niña; aves nectarívoras; aves frugívoras; cambio climático

Introduction

The evaluation of the changes in patterns of bird abundance is important for our understanding of factors that could affect population dynamics (survival and mortality) and animal communities (changes in species composition) (Holt, 1993; Yodzis, 1993; Brown, 1995). In bird communities, species often adjust the timing of molting, migration and reproduction to fluctuations in food resourses, which in turn respond to predictable, seasonal climatic changes (Stiles, 1985; Loiselle & Blake, 1991; Worthington, 1996). Unpredictable climatic anomalies such as El Niño Southern Oscillation (hereafter El Niño) and presumably La Niña phenomenon, have a strong impact on survivorship and reproduction in many bird populations, and consequently affect the community structure (Grant & Grant, 1983; Stiles, 1992; Jaksic & Laso, 1999). El Niño occurs approximately every 4.1 years (Glynn, 1988), but oscillates between two and ten years (Philander, 1985). El Niño and La Niña represent extremes in sea-surface temperatures, with El Niño being above mean temperature and La Niña below it (Andreoli & Kayano, 2005).

The impact of El Niño and La Niña on bird populations often varies between taxonomic groups. Seabirds are presumably more strongly affected than land-bird species. For example, rates of survivorship and reproduction of many marine bird species (e.g., Phalacocrorax bougainvilli, Sula variegata, Pelecanus thagus, Nonnopternum harrisi, Diomedea irrorata, and Spenicus mendiculus) that nest in the area of maximum impact of El Niño are drastically reduced, particularly during strong El Niño events (Idyll, 1973; Boersma, 1978; Tovar, Guillen, & Cabrera, 1987; Rechten, 1985; Hays, 1986; Valle, Cruz, Cruz, Merlen, & Coulter, 1987; Glynn, 1988). During the strong El Niño events food supply for marine birds (e.g., the sardine Sardinops sagax and the anchovy Engraulis ringens) decrease strikingly, precluding birds to reproduce or greatly increasing mortality, particularly of juveniles (Ashmole, 1971; Hays, 1986; Anderson, 1989).

The effect of El Niño events on terrestrial bird populations in the Neotropics is difficult to evaluate for several reasons. First, occurrence, duration and intensity of El Niño are unpredictable (Cai et al., 2014). Second, the occurrence and intensity of La Niña is even less predictable (Grimm, Ferraz, & Gomes, 1998). Third, there is a lack of long-term monitoring data needed to evaluate the impact of these unpredictable climatic phenomena on the dynamics of bird populations in tropical forests (Wolfe & Ralph, 2009). During El Niño events, precipitation in general decreases in the Neotropical region, producing extensive droughts in areas where rains dominate year-round under normal conditions (Nobre & Shukla, 1996; Andreoli & Kayano, 2005; Paxton, Cohen, Paxton, Németh, & Moore, 2014), although precipitation at more localized scales could be higher in some areas during El Niño years (Villalobos & Retana, 2000). On the contrary, La Niña which sometimes occurs right after El Niño or not at all is often considered the anti-Niño because it has roughly the opposite effect on climatic conditions (Philander, 1985; Brenes & Bonilla, 2012). Our main objective here is then to test the effect of El Niño and La Niña events on the abundance of terrestrial bird populations in three different forest types in Costa Rica. We used data from Christmas Bird Counts from 1984 to 2011, the longest data set of bird abundance in Costa Rica. The effect of the El Niño is extremely variable over Central America (Ropelewski & Halpert, 1987; Enfield & Mayer, 1997; Sheffield & Wood, 2008). For instance, Waylen, & Caviedes (1996) and Giannini, Kushnir, & Cane (2000) show that El Niño events in Costa Rica produce contrasting climatic conditions between Pacific (decreases rainfall) and Caribbean slopes (increases rainfall). Thereby, we expect contrasting results on bird abundance among forest types since the effect of El Niño could affect differently each forest.

Materials and methods

Study sites: We selected three localities for which long term monitoring data (≥ 16 years) on bird abundance and species composition is available. This data set allows comparisons among multiple events of El Niño, La Niña, and neutral years. The three localities include three forest types: lowland rain forest (La Selva Biological Station, Caribbean slope), premontane forest (Grecia, Pacific slope), and montane forest (Monteverde, continental divide that includes portions of both Caribbean and Pacific slopes). Forest vegetation for La Selva and Monteverde were described by Hartshorn, (1983) and Haber, (2000) respectively. Vegetation in Grecia consists of a matrix of large sugar cane and coffee plantations, urban habitats and large fragments of riparian premontane forest.

Bird abundance data: We obtained bird species abundance from Christmas’ Bird Counts (CBC) conducted in each locality under Audubon protocol (National Audubon Society, 2010). CBCs use a standard protocol that consists of counting bird species and abundance inside a circle of 24 km in diameter (452.4 km2 area). In each locality, the circle includes the largest area of most forest types in that locality; the location of the circular sampling area is set prior to the first CBC and this location is maintained through time. Additionally, CBCs are conducted during a single 24 h period started at 00:00 h and finished at 24:00 h on the same routes year after year, which increases the comparative power of the data over time. The period of time analyzed varied across localities: lowland rain forest from 1985 to 2011, premontane forest from 1984 to 2003, and montane forest from 1994 to 2010. Data on CBC were obtained from The Organization for Tropical Studies (OTS, 2010) (http://www.ots.ac.cr/cbc_laselva) and National Audubon Society (http://www.christmasbirdcount.org).

For each locality, we selected resident large frugivorous (> 30 g), medium size frugivorous (20 - 30 g), small frugivorous (< 20 g), and nectarivorous bird species (Table S1). We selected this subset of species because they fulfilled the following criteria: (1) species are conspicuous reducing their false-positive identification, and (2) species main food resource (fruits and nectar) are seasonal and influenced by rainfall levels that change according to El Niño and La Niña occurrence. We only used species recorded in 50 % or more of the CBC in each locality.

Statistical analyses: We compared bird abundance (e.g. count frequency) of species included in each of the four-bird diet-categories for each of the forest types and three weather events (i.e., El Niño, La Niña, neutral years) using Generalized Linear Models with a Poisson distribution or quasipoisson distribution when residuals were over-dispersed (GLM, library MASS). We used Zero Inflated Models (library glmmADMB) with a negative binomial probability distribution when the number of ceros exceed those expected by a Poisson (or quasipoisson) distribution. With the negative binomial probability distribution, we could accomplish the assumptions of normality of residuals and homoscedasticity. El Niño, La Niña, or neutral years were defined with the Oceanic Niño Index (ONI), obtained from https://ggweather.com/enso/oni.htm. Events are defined by the National Oceanic and Atmospheric Administration (https://www.noaa.gov/) as five consecutive overlapping 3-month periods with values of the ONI index above the +0.5o anomaly for warm (El Niño) events, or below the -0.5º anomaly for cold (La Niña) events. For the analyses we included the median value (negative or positive) of the 3-month periods for each year defined as El Niño, La Niña, or neutral. Thus, the statistical models included bird-diet categories, weather events, the co-variable “ONI”, which account for the variation in climatic conditions during of El Niño, La Niña, and neutral years, and the total number of person-hours per bird count as another covariate in the analyses (i.e., time) to account for yearly-variation in effort and total distance covered, and species as random factors within the model. All analyses were done using the R statistical language, version 3.0.1 (R Core Team, 2013).

Results

The number of El Niño, La Niña, and Neutral years were similar for all three study sites. Lowland rain forest included seven years in each of the three weather categories; the premontane forest included six El Niño and La Niña years, and seven neutral years; and the montane forest included six El Niño years, seven La Niña years, and five neutral years.

Lowland rain forest: We tested the effect of weather events on the abundance of 17 large frugivorous (LF), 27 medium size frugivorous (MF), 36 small frugivorous (SF), and 12 nectarivorous (Nc) bird species in the lowland forest (Table S1). The abundance of large and medium size frugivores increased significantly during La Niña events in comparison to neutral years (Table 1, Fig. 1), and the abundance of Nc during the El Niño events relative to neutral years. Abundance of SF was not affected by La Niña or El Niño events; nor El Niño affected significantly the abundance in any of the three groups of frugivores (Table 1). Neither we found significant differences in the abundance of frugivores and nectarivores between La Niña and El Niño events (Table 1). The ONI did not have a significant effect on frugivorous and nectarivorous birds in the lowland rain forest (Table 1).

Fig. 1 Mean, standard error, and confidence intervals for three groups frugivorous birds (large, medium size, and small), and nectarivorous birds in three forest types (lowland, pre-montane, and montane). The mean was estimated from the intercept of the statistical models, which directly correlate with the mean values of the variables included in the models. 

TABLE 1 Comparison between climatic events (El Niño, La Niña, and Neutral years) for Large frugivores, Medium size frugivores, Small frugivores, and Nectarivores in three forest types based on Generalized Linear Models with a Poisson probability distribution. 

Lowland rain forest
Large frugivores
Effect Coefficient SE T P
Neutral 2.64 0.32 8.13 (446) 0.0000
Niño - Neutral 0.18 0.10 1.81 (446) 0.0708
Niña - Neutral 0.31 0.09 3.27(446) 0.0011
Niña - Niño 01.2 0.16 0.79 (446) 0.4274
ONI 0.05 0.05 0.92 (446) 0.3532
Counting hours 0.00 0.00 8.79 (446) 0.0000
Medium frugivores
Effect Coefficient SE T P
Neutral 2.33 0.24 9.55 (696) < 0.0001
Niño - Neutral 0.00 0.09 0.40 (696) 0.9681
Niña - Neutral 0.25 0.08 2.99 (696) 0.0029
Niña - Niño 0.25 0.14 1.75 (696) 0.0806
ONI 0.09 0.05 1.90 (696) 0.0581
Counting hours 0.00 0.00 8.25(696) < 0.0001
Small frugivores
Effect Coefficient SE T P
Neutral 2.26 0.19 11.57 (896) < 0.0001
Niño - Neutral 0.12 0.02 1.60 (896) 0.1089
Niña - Neutral 0.02 0.07 0.23 (896) 0.7881
Niña - Niño -0.10 0.11 -0.85 (896) 0.3928
ONI -0.01 0.04 -0.19 (896) 0.8428
Counting hours 0.00 0.00 11.33 (896) < 0.0001
Nectarivores
Effect Coefficient SE T P
Neutral 1.85 0.33 5.11 (321) < 0.0001
Niño - Neutral 0.24 0.10 2.33 (321) 0.0203
Niña - Neutral 0.12 0.10 1.19 (321) 0.2352
Niña - Niño -0.12 0.16 -0.76 (321) 0.4491
ONI 0.00 0.06 0.08 (321) 0.9382
Counting hours 0.00 0.00 5.66 (321) < 0.0001
Pre-montane forest
Large frugivores
Effect Coefficient SE T P
Neutral 0.00 0.69 0.00 (104) 0.9968
Niño - Neutral 0.05 0.27 0.19 (104) 0.8485
Niña - Neutral 0.80 0.24 3.27 (104) 0.0015
Niña - Niño 0.74 0.44 1.70 (104) 0.0913
ONI 0.22 0.14 1.62 (104) 0.1069
Counting hours 0.03 0.00 6.00 (104) < 0.0001
Medium frugivores
Effect Coefficient SE Z P
Neutral 1.28 0.54 2.40 (228) 0.017
Niño - Neutral 0.28 0.26 1.10 (228) 0.272
Niña - Neutral 0.01 0.20 0.07 (228) 0.942
Niña - Niño -0.27 0.40 -0.67 (228) 0.504
ONI -0.07 0.13 -0.49 (228) 0.623
Counting hours 0.02 0.00 4.92 (228) < 0.001
Small frugivores
Effect Coefficient SE T (339) P
Neutral 0.29 0.29 0.98 (338) 0.3254
Niño - Neutral 0.29 0.15 1.99 (338) 0.0469
Niña - Neutral 0.41 0.12 3.29 (338) 0.0011
Niña - Niño -0.29 0.15 -1.99 (338) 0.5462
ONI 0.10 0.07 1.49 (338) 0.1370
Counting hours 0.02 0.00 5.96 (338) < 0.0001
Nectarivores
Effect Coefficient SE T P
Neutral 0.26 0.32 0.82 (266) 0.4147
Niño - Neutral 0.16 0.21 0.75 (266) 0.4522
Niña - Neutral 0.14 0.19 0.72 (266) 0.4680
Niña - Niño -0.02 0.35 -0.05 (266) 0.9611
ONI 0.13 0.11 1.21 (266) 0.2244
Counting hours 0.02 0.00 4.99 (266) < 0.0001
Montane forest
Large frugivores
Effect Coefficient SE T P
Neutral 1.61 0.37 4.35 (268) < 0.0001
Niño - Neutral 0.77 0.17 4.42 (268) < 0.0001
Niña - Neutral -0.45 0.14 -3.20 (268) 0.0016
Niña - Niño -1.23 0.27 -4.65 (268) < 0.0001
ONI -0.42 0.09 -4.39 (268) < 0.0001
Counting hours 0.00 0.00 4.22 (268) < 0.0001
Medium frugivores
Effect Coefficient SE T P
Neutral 1.98 0.29 6.73 (506) < 0.0001
Niño - Neutral 0.93 0.15 5.98 (506) < 0.0001
Niña - Neutral -0.46 0.12 -3.81 (506) 0.0002
Niña - Niño -1.39 0.23 -6.14 (506) < 0.0001
ONI -0.52 0.08 -6.15 (506) < 0.0001
Counting hours 0.00 0.00 2.78 (506) 0.0055
Small frugivores
Effect Coefficient SE T P
Neutral 2.09 0.21 10.06 (829) < 0.0001
Niño - Neutral 0.50 0.13 3.77 (829) < 0.0001
Niña - Neutral -0.55 0.10 -5.24(829) < 0.0001
Niña - Niño -1.05 0.13 -3.77 (829) < 0.0001
ONI -0.30 0.07 -4.18 (829) < 0.0001
Counting hours 0.00 0.00 4.69 (8.29) < 0.0001
Nectarivores
Effect Coefficient SE Z P
Neutral 1.62 0.28 5.87 (468) < 0.0001
Niño - Neutral 0.68 0.14 4.66 (468) < 0.0001
Niña - Neutral -0.47 0.12 -4.14 (468) < 0.0001
Niña - Niño -1.15 0.21 -5.57 (468) < 0.0001
ONI -0.41 0.08 -5.35 (468) < 0.0001
Counting hours 0.00 0.00 3.06 (468) < 0.0001

The intensity of the climatic event (ONI Index) was included in the model.

The corresponding degrees of freedom are included in parentheses besides the T-values.

The Z-values correspond to the Zero Inflated Models.

Pre-montane forest: For the premontane forest, we analyzed the abundance of 6 LF, 12 MF, 19 SF, and 15 Nc bird species. In this forest, the abundance of LF and SF increased significantly during La Niña events when compared with neutral years (Table 1, Fig. 1), but it did not affect the abundance of MF nor Nc. The abundance of SF also increased during El Niño, but it did not affect the abundance of other groups. The ONI had no effect on abundance of any of the bird groups (Table 1).

Montane forest: For the montane forest, we analyzed the abundance of 17 LF, 30 MF, 49 SF, and 26 Nc bird species. In this forest the abundance of all three groups of frugivores and the nectarivores increased during El Niño events in comparison to neutral years, but decreased for all bird groups during La Niña events (Table 1, Fig. 1). The abundance of all four groups correlated negatively with ONI index values (Table 1). Thus, the abundance of birds in the montane forests has a strong increment during El Niño events, despite that bird abundance decreased as the index ONI increased.

The total number of person-hours per bird count correlated positively with bird abundance in all cases. However, the ONI index had only a significant effect on bird abundance in the Montane forest.

Discussion

The variation in the abundance of frugivorous and nectarivorous birds detected in this study could be the result of temporal and spatial changes in the phenology of flowering and fruiting species (food resources) caused by El Niño and La Niña events. The shifting in the pattern of precipitation, intensity of rainfall, and radiation caused by El Niño and La Niña directly affect the periodicity of phenological phases, the distribution, and mortality of plants (Wright, Carrasco, Calderón, & Paton, 1999; Villalobos & Retana, 2000; Holmgren, Scheffer, Ezcurra, Gutiérrez, & Mohren, 2001; Jaksic, 2001; McPhaden, Zebiak, & Glantz, 2006; Chen & Cane, 2008). For instance, flowering and fruiting of understory plant species correlate with increasing temperature and radiation (Kimura, Yumoto, Kikuzawa, & Kitayama, 2009). Increasing variation of food resources (Wright et al., 1999) could force birds to change their movement patterns or to move to areas where the effect of these climatic anomalies is milder. Such variation could also increase mortality of birds if food resources decrease drastically (Wolfe & Ralph, 2009; Boyle, Norris, & Guglielmo, 2010), and all these factors could affect the abundance of species locally (Jaksic & Laso, 1999).

The fluctuation in bird abundance across bird groups in this study is similar to that reported for other terrestrial ecosystems in the Neotropics. For instance, in Barro Colorado island (Panama) fruit production greatly increases during El Niño events but decreases drastically when a mild dry season (e.g., the Niña event) follows El Niño, thus increasing mortality of frugivorous mammals (Foster, 1982; Wright et al., 1999). In the Galapagos Islands, reproduction and recruitment of Geospiza fortis significantly increased as a result of high production of seeds during the strong rainy season of El Niño 1982-1983 (Grant, 1986). In Chile, the diversity and density of several groups of landbirds increased during El Niño 1997-1998 (Jaksic & Laso, 1999). These changes in diversity and density are presumably a direct consequence of increasing rainfall in the region during El Niño years (Jaksic & Laso, 1999).

The effect of El Niño on climate varies among events and geographical scales. In Chile, total rainfall increases during El Niño but in Barro Colorado Island, rainfall actually decreases during these events, although increases in food resources have in both cases been attributed to El Niño events (Wright et al., 1999; Jaksic, 2001). In Costa Rica, precipitation during the El Niño and La Niña events also varies between slopes and across events (Waylen, Quesada, & Caviedes, 1994; Waylen, & Caviedes, 1996; Waylen, Caviedes, Poveda, Mesa, & Quesada, 1998; Brenes & Bonilla, 2012). This variation affects differently the abundance of the bird groups in different forests. In the lowland forest abundance of frugivores (large and medium size) increased during La Niña years, but El Niño years did not have a significant effect on frugivores abundance, though abundance of nectarivores increased during these events (Table 1, Fig. 1). The montane forest showed an entirely opposite pattern for frugivores. In this forest, the abundance increased consistently for all frugivorous and nectarivorous birds during El Niño events, but their abundance decreased during La Niña. It is notable in the montane forest that El Niño has a strong positive effect on bird abundance, but this abundance tends to decrease if intensity of El Niño increases (Table 1). This suggests that there are at least two different processes affecting bird abundance in montane forests. One that likely makes birds to move uphill during El Niño, and another, perhaps less intense, affecting negatively their abundance at high elevation. In the premontane forest these climatic events had little effect on bird abundance. Only abundance of SF increased during La Niña events, but had no effect on LF, MF, and Nc (Table 1, Fig. 1). It is likely that differences in climatic conditions at small geographical scales affects differently plant phenology, and so avian food resources in each forest type, but until we have detailed information on the climatic conditions along the mountain slopes and their effect on bird food resources, the response to fluctuation in frugivores and nectarivores will remain elusive (Williams-Linera & Meave, 2002).

The changes in abundance during El Niño and La Niña events could be attributed to temporal and spatial fluctuation in food resources, but these climatic events may also affect bird reproduction and survivorship (Wolfe, Ralph, & Elizondo, 2015). Both climatic events may have drastic negative effects at the level of population and community structure. For instance, some populations of Darwin’s finches (Geospiza spp.) fail to reproduce during extremely dry years, which usually coincide with La Niña events, and mortality increases up to 85 % during these years and sex ratio skewed toward males (Boag & Grant, 1981; Boag & Grant, 1984; Grant & Grant, 1983; Grant, 1986). These factors delayed the recovery of populations (Boag & Grant, 1984). Similarly, survivorship of the Long-billed Hermit (Phaetornis longirostris) drastically decreased in a Costa Rican rain forest as a consequence of a flower shortage caused by a severe drought during El Niño event 1972-1973 (Stiles, 1992). Recovery of this population lasted about four years. Bird survival may also depend on the specific habitat features. For instance, in Costa Rica Survivorship of the White-collared Manakin (Manacus candei) was drastically affected by el Niño in disturbed forests but not in near mature forests (Wolfe et al., 2015).

Climate scenario models predict that El Niño events will increase in frequency as global, greenhouse warming increases (Cai et al., 2014). Considering that some populations of terrestrial birds require nearly four years to recover after the impact caused the by El Niño and that the mean period of El Niño occurrence is 4.1 yrs (Glynn, 1988), an increase in frequency of these events would increase the probability of some avian populations to become extinct if they are not capable to recover in a shorter time. We finally highlight the importance of long-term data on bird abundance and phenology of plants to evaluate more precisely the effects of the El Niño and La Niña climatic anomalies on population’s dynamics and community structure of tropical birds.

Ethical statement: authors declare that they all agree with this publication and made significant contributions; that there is no conflict of interest of any kind; and that we followed all pertinent ethical and legal procedures and requirements. All financial sources are fully and clearly stated in the acknowledgements section. A signed document has been filed in the journal archives.

Supporting Information

TABLE S1 Bird species used in the analysis of effect of El Niño and La Niña in three forests of Costa Rica according to the effects of El Niño and La Niña 

English name Category Size (cm) Forest type
Lowland rainforest Premontane forest Monatane forest
TINAMIFORMES
Tinamidae
Nothocercus bonapartei Highland Tinamou Large frugivouros 38 X
Tinamus major Great Tinamou Large frugivouros 43 X X
Crypturellus soui Little Tinamou Medium frugivouros 23 X
Crypturellus boucardi Slaty-breasted Tinamou Large frugivouros 28 X
GALLIFORMES
Cracidae
Ortalis cinereiceps Gray-headed Chachalaca Large frugivouros 51 X X
Penelope purpurascens Crested Guan Large frugivouros 86 X X
Chamaepetes unicolor Black Guan Large frugivouros 64 X X
Crax rubra Great Curassow Large frugivouros 91 X
Odontophoridae
Odontophorus leucolaemus Black-breasted Wood-Quail Medium frugivouros 23 X
COLUMBIFORMES
Columbidae
Patagioenas cayennensis Pale-vented Pigeon Large frugivouros 30 X
Patagioenas speciosa Scaled Pigeon Large frugivouros 32 X
Patagioenas flavirostris Red-billed Pigeon Large frugivouros 30 X X
Patagioenas fasciata Band-tailed Pigeon Large frugivouros 35 X X
Patagioenas subvinacea Ruddy Pigeon Medium frugivouros 28 X X
Patagioenas nigrirostris Short-billed Pigeon Medium frugivouros 26.5 X X
Columbina inca Inca Dove Medium frugivouros 20 X
Columbina passerina Common Ground-Dove Small frugivorous 16 X X
Columbina talpacoti Ruddy Ground-Dove Small frugivorous 16.5 X
Claravis pretiosa Blue Ground-Dove Medium frugivouros 20 X
Leptotila verreauxi White-tipped Dove Medium frugivouros 26 X X X
Leptotila cassinii Gray-chested Dove Medium frugivouros 24 X
Geotrygon veraguensis Olive-backed Quail-Dove Medium frugivouros 21.5 X X
Geotrygon chiriquensis Chiriqui Quail-Dove Medium frugivouros 30 X
Geotrygon lawrencii Purplish-backed Quail-Dove Medium frugivouros 25 X
Geotrygon costaricensis Buff-fronted Quail-Dove Medium frugivouros 28 X
Geotrygon montana Ruddy Quail-Dove Medium frugivouros 23 X
APODIFORMES
Trochilidae
Glaucis aeneus Bronzy Hermit Nectarivorous X
Threnetes ruckeri Band-tailed Barbthroat Nectarivorous X
Phaethornis guy Green Hermit Nectarivorous X
Phaethornis longirostris Long-billed Hermit Nectarivorous X X
Phaethornis striigularis Stripe-throated Hermit Nectarivorous X X
Doryfera ludovicae Green-fronted Lancebill Nectarivorous X
Colibri delphinae Brown Violetear Nectarivorous X
Colibri cyanotus Lesser Violetear Nectarivorous X X
Heliothryx barroti Purple-crowned Fairy Nectarivorous X X
Anthracothorax prevostii Green-breasted Mango Nectarivorous X X X
Heliodoxa jacula Green-crowned Brilliant Nectarivorous X
Panterpe insignis Fiery-throated Hummingbird Nectarivorous X X
Heliomaster constantii Plain-capped Starthroat Nectarivorous X X
Lampornis hemileucus White-bellied Mountain-gem Nectarivorous X
Lampornis calolaemus Purple-throated Mountain-gem Nectarivorous X X
Calliphlox bryantae Magenta-throated Woodstar Nectarivorous X
Selasphorus flammula Volcano Hummingbird Nectarivorous X
Selasphorus scintilla Scintillant Hummingbird Nectarivorous X X
Chlorostilbon canivetii Canivet’s Emerald Nectarivorous X X
Klais guimeti Violet-headed Hummingbird Nectarivorous X X
Phaeochroa cuvierii Scaly-breasted Hummingbird Nectarivorous X
Campylopterus hemileucurus Violet Sabrewing Nectarivorous X X
Eupherusa eximia Stripe-tailed Hummingbird Nectarivorous X X
Elvira cupreiceps Coppery-headed Emerald Nectarivorous X
Chalyburaurochrysia Bronze-tailed Plumeleteer Nectarivorous X
Thalurania colombica Crowned Woodnymph Nectarivorous X X
Amazilia amabilis Blue-chested Hummingbird Nectarivorous X
Amazilia saucerrottei Steely-vented Hummingbird Nectarivorous X X
Amazilia tzacatl Rufous-tailed Hummingbird Nectarivorous X X X
Amazilia rutila Cinnamon Hummingbird Nectarivorous X X
Hylocharis eliciae Blue-throated Goldentail Nectarivorous X
TROGONIFORMES
Trogonidae
Trogon clathratus Lattice-tailed Trogon Medium frugivouros 30 X X
Trogon massena Slaty-tailed Trogon Medium frugivouros 30 X X
Trogon caligatus Gartered Trogon Medium frugivouros 23 X X
Trogon rufus Black-throated Trogon Medium frugivouros 23 X
Trogon collaris Collared Trogon Medium frugivouros 25 X
Trogon aurantiiventris Orange-bellied Trogon Medium frugivouros 25 X
Pharomachrus mocinno Resplendent Quetzal Large frugivouros 36 X X
PICIFORMES
Capitonidae
Eubucco bourcierii Red-headed Barbet Small frugivorous 15 X
Semnornithidae
Semnornis frantzii Prong-billed Barbet Small frugivorous 17 X
Ramphastidae
Aulacorhynchus prasinus Emerald Toucanet Medium frugivouros 29 X X
Pteroglossus torquatus Collared Aracari Large frugivouros 41 X X
Selenidera spectabilis Yellow-eared Toucanet Large frugivouros 36 X
Ramphastos sulfuratus Keel-billed Toucan Large frugivouros 47 X X X
Ramphastos ambiguus Yellow-throated Toucan Large frugivouros 56 X
PSITTACIFORMES
Psittacidae
Eupsittula nana Olive-throated Parakeet Medium frugivouros 23 X
Eupsittula canicularis Orange-fronted Parakeet Medium frugivouros 22.5 X
Ara ambiguus Great Green Macaw Large frugivouros 79 X
Psittacara finschi Crimson-fronted Parakeet Medium frugivouros 28 X X X
Bolborhynchus lineola Barred Parakeet Small frugivorous 16 X
Brotogeris jugularis Orange-chinned Parakeet Small frugivorous 18 X X X
Touit costaricensis Red-fronted Parrotlet Small frugivorous 17 X
Pyrilia haematotis Brown-hooded Parrot Medium frugivouros 21 X X
Pionus senilis White-crowned Parrot Medium frugivouros 24 X X X
Amazona albifrons White-fronted Parrot Medium frugivouros 25 X
Amazona autumnalis Red-lored Parrot Large frugivouros 34 X
Amazona farinosa Mealy Parrot Large frugivouros 38 X
PASSERIFORMES
Tyrannidae
Elaenia flavogaster Yellow-bellied Elaenia Small frugivorous 15 X X X
Elaenia frantzii Mountain Elaenia Small frugivorous 15 X X
Mionectes olivaceus Olive-striped Flycatcher Small frugivorous 13 X
Mionectes oleagineus Ochre-bellied Flycatcher Small frugivorous 12.5 X X X
Zimmerius vilissimus Paltry Tyrannulet Small frugivorous 9.5 X X
Rhynchocyclus brevirostris Eye-ringed Flatbill Small frugivorous 15 X
Tityridae
Tityra semifasciata Masked Tityra Medium frugivouros 21 X X X
Tityra inquisitor Black-crowned Tityra Small frugivorous 18.5 X
Pachyramphus versicolor Barred Becard Small frugivorous 12 X
Pachyramphus cinnamomeus Cinnamon Becard Small frugivorous 14 X X
Pachyramphus polychopterus White-winged Becard Small frugivorous 14.5 X
Pachyramphus aglaiae Rose-throated Becard Small frugivorous 16.5 X
Cotingidae
Querula purpurata Purple-throated Fruitcrow Medium frugivouros 28 X
Cephalopterus glabricollis Bare-necked Umbrellabird Large frugivouros 41 X X
Lipaugus unirufus Rufous Piha Medium frugivouros 23 X
Procnias tricarunculatus Three-wattled Bellbird Medium frugivouros 30 X
Carpodectes nitidus Snowy Cotinga Medium frugivouros 22.5 X
Pipridae
Corapipo altera White-ruffed Manakin Small frugivorous 10 X
Chiroxiphia linearis Long-tailed Manakin Small frugivorous 11.5 X X
Dixiphia pipra White-crowned Manakin Small frugivorous 10 X
Ceratopipra mentalis Red-capped Manakin Small frugivorous 10 X
Manacus candei White-collared Manakin Small frugivorous 11 X
Oxyruncidae
Oxyruncus cristatus Sharpbill Small frugivorous 16.5 X
Vireonidae
Vireo leucophrys Brown-capped Vireo Small frugivorous 12 X
Vireo laniuspulchellus Green Shrike-Vireo Small frugivorous 14 X
Cyclarhis gujanensis Rufous-browed Peppershrike Small frugivorous 14 X
Corvidae
Cyanolyca cucullata Azure-hooded Jay Medium frugivouros 29 X
Calocitta formosa White-throated Magpie-Jay Large frugivouros 46 X
Psilorhinus morio Brown Jay Large frugivouros 39 X X X
Turdidae
Myadestes melanops Black-faced Solitaire Small frugivorous 17 X X
Catharus aurantiirostris Orange-billed Nightingale-Thrush Small frugivorous 16 X X
Catharus fuscater Slaty-backed Nightingale-Thrush Small frugivorous 17 X
Catharus frantzii Ruddy-capped Nightingale-Thrush Small frugivorous 16 X
Catharus mexicanus Black-headed Nightingale-Thrush Small frugivorous 16 X X
Turdus plebejus Mountain Thrush Medium frugivouros 24 X X
Turdus obsoletus Pale-vented Thrush Medium frugivouros 23.5 X X
Turdus grayi Clay-colored Thrush Medium frugivouros 23.5 X X X
Turdus assimilis White-throated Thrush Medium frugivouros 22 X
Ptiliogonatidae
Phainoptila melanoxantha Black-and-yellow Silky-Flycatcher Medium frugivouros 21 X
Ptiliogonys caudatus Long-tailed Silky-Flycatcher Medium frugivouros 24 X
Fringillidae
Euphonia luteicapilla Yellow-crowned Euphonia Small frugivorous 9.5 X
Euphonia hirundinacea Yellow-throated Euphonia Small frugivorous 11 X X
Euphonia elegantissima Elegant Euphonia Small frugivorous 11 X
Euphonia gouldi Olive-backed Euphonia Small frugivorous 9.5 X
Euphonia minuta White-vented Euphonia Small frugivorous 9 X
Euphonia anneae Tawny-capped Euphonia Small frugivorous 11 X X
Chlorophonia callophrys Golden-browed Chlorophonia small frugivorous 13 X X
Passerellidae
Chlorospingus flavopectus Common Bush-Tanager Small frugivorous 13.5 X X
Chlorospingus pileatus Sooty-capped Bush-Tanager Small frugivorous 13.5 X X
Chlorospingus canigularis Ashy-throated Bush-Tanager Small frugivorous 13 X
Icteridae
Amblycercus holosericeus Yellow-billed Cacique Medium frugivouros 23 X X X
Psarocolius wagleri Chestnut-headed Oropendola Large frugivouros 35 X X
Psarocolius montezuma Montezuma Oropendola Large frugivouros 50 X X X
Cacicus uropygialis Scarlet-rumped Cacique Medium frugivouros 23 X X
Icterus prosthemelas Black-cowled Oriole Small frugivorous 19 X
Molothrus oryzivorus Giant Cowbird Large frugivouros 33 X
Cardinalidae
Piranga flava Hepatic Tanager Small frugivorous 18 X
Piranga bidentata Flame-colored Tanager Small frugivorous 18 X
Habia rubica Red-crowned Ant-Tanager Small frugivorous 18 X X
Habia fuscicauda Red-throated Ant-Tanager Small frugivorous 19 X
Chlorothraupiscarmioli Carmiol’s Tanager Small frugivorous 17 X X
Caryothraustes poliogaster Black-faced Grosbeak Small frugivorous 16.5 X
Passerina caerulea Blue Grosbeak Small frugivorous 16.5 X
Thraupidae
Thraupis episcopus Blue-gray Tanager Small frugivorous 15 X X X
Thraupis palmarum Palm Tanager Small frugivorous 16 X X X
Tangara larvata Golden-hooded Tanager Small frugivorous 13 X X
Tangara guttata Speckled Tanager Small frugivorous 13 X
Tangara dowii Spangle-cheeked Tanager Small frugivorous 13 X
Tangara inornata Plain-colored Tanager Small frugivorous 12 X
Tangara gyrola Bay-headed Tanager Small frugivorous 13.5 X
Tangara florida Emerald Tanager Small frugivorous 12 X
Tangara icterocephala Silver-throated Tanager Small frugivorous 13 X
Diglossa plumbea SlatyFlowerpiercer Nectarivorous X X
Chrysothlypis chrysomelas Black-and-yellow Tanager Small frugivorous 12 X X
Chlorophanes spiza Green Honeycreeper Small frugivorous 13 X X
Tachyphonus luctuosus White-shouldered Tanager Small frugivorous 14 X
Tachyphonus delattrii Tawny-crested Tanager Small frugivorous 14.5 X
Tachyphonus rufus White-lined Tanager Small frugivorous 17 X
Lanio leucothorax White-throated Shrike-Tanager Medium frugivouros 20 X X
Ramphocelus sanguinolentus Crimson-collared Tanager Small frugivorous 18.5 X X
Ramphocelus passerinii Passerini’s Tanager Small frugivorous 16 X X
Cyanerpes lucidus Shining Honeycreeper Small frugivorous 10 X
Cyanerpes cyaneus Red-legged Honeycreeper Small frugivorous 11.5 X X X
Dacnis venusta Scarlet-thighed Dacnis Small frugivorous 11.5 X
Dacnis cayana Blue Dacnis Small frugivorous 11.5 X
Coereba flaveola Bananaquit Small frugivorous 9 X X
Saltator atriceps Black-headed Saltator Medium frugivouros 24 X
Saltator maximus Buff-throated Saltator Medium frugivouros 20 X X X
Saltator grossus Slate-colored Grosbeak Small frugivorous 19 X
Saltator coerulescens Grayish Saltator Medium frugivouros 20 X X X

Category refers to the classification of each species according to guild and body size.

Size where obtained from Stiles and Skutch (1989).

Acknowledgements

We thank V. Ruiz-Gutiérrez and three anonymous reviewers for their valuable comments on a previous version of the manuscript and to National Audubon Society and Organization for Tropical Studies for allowing us to use the bird count data. LS was supported during the writing part of this manuscript by scholarships and grants from the Ministerio de Ciencia y Tecnología (MICIT) and the Consejo Nacional para Investigaciones Científicas y Tecnológicas (CONICIT) of Costa Rica, the Government of Ontario and the University of Windsor.

References

Anderson, D. J. (1989). Differential responses of boobies and other seabirds in the Galapagos to the 1986-87 El Niño-Southern Oscillation event. Marine Ecology Progress Series, 52, 209-216. [ Links ]

Andreoli, R. V., & Kayano, M. T. (2005). ENSO-related rainfall anomalies in South America and associated circulation features during warm and cold pacific decadal oscillation regimes. International Journal of Climatology, 25, 2017-2030. [ Links ]

Ashmole, N. P. (1971). Sea bird ecology and the marine environment. In D. S. Farner, & J. R. King (Eds.), Avian Biology (pp. 224-286). New York: Academic Press. [ Links ]

Boag, P. T., & Grant, P. R. (1981). Intense natural selection in a population of Darwin’s finches (Geospizinae) in the Galápagos. Science, 214, 82-85. [ Links ]

Boag, P. T., & Grant, P. R. (1984). Darwin’s Finches (Geospiza) on isla Daphne Major, Galapagos: breeding and feeding ecology in a climatically variable environment. Ecological Monograph, 54, 463-489. [ Links ]

Boersma, P. D. (1978). Breeding patterns of Galapagos penguins as an indicator of oceanographic conditions. Science , 200, 1481-1483. [ Links ]

Boyle, W. A., Norris, D. R., & Guglielmo, C. G. (2010). Storms drive altitudinal migration in a tropical bird. Proceedings of the Royal Society B: Biological Sciences, 277(1693), 2511-2519. DOI: 10.1098/rspb.2010.0344 [ Links ]

Brenes, A., & Bonilla, A. (2012). La Niña 2010-2012. Estudio de Caso Costa Rica: Global Assessment Report on Disaster Risk Reduction. Colombia: Corporación OSSO. [ Links ]

Brown, J. H. (1995). Macroecology. Il: University of Chicago Press. [ Links ]

Cai, W., Borlace, S., Lengaigne, M., van Rensch, P., Collins, M., Vecchi, G., … Jin, F. F. (2014). Increasing frequency of extreme El Niño events due to greenhouse warming. Nature Climate Change, 4, 111-116. [ Links ]

Chen, D., & Cane, M. A. (2008). El Niño prediction and predictability. Journal of Computational Physics, 227, 3625-3640. [ Links ]

Enfield, D. B., & Mayer, D. A. (1997). Tropical Atlantic sea surface temperature variability and its relation to El Niño-southern oscillation. Journal of Geophysical Research, 102, 929-945. [ Links ]

Foster, R. B. (1982). Famine on Barro Colorado Island. In E. G. Jr. Leigh, Rand, A. S., & D. M. Windsor (Eds.), Ecology of a Tropical Forest (pp. 201-212). DC: Smithsonian Institution Press. [ Links ]

Giannini, A., Kushnir, Y., & Cane, M. A. (2000). Interannual variability of Caribbean rainfall, ENSO, and the Atlantic Ocean. Journal of Climate, 13, 297-311. [ Links ]

Glynn, P. W. (1988). El Niño-Southern Oscillation 1982-83: near shore population, community, and ecosystem responses. Annual Review of Ecology and Systematics, 19, 309-345. [ Links ]

Grant, B. R., & Grant, P. R. (1983). Fission and fusion in a population of Darwin’s finches: an example of the value of studying individuals in ecology. Oikos, 41, 530-547. [ Links ]

Grant, P. R. (1986). Ecology and Evolution of Darwin’s Finches. N.J.: Princeton University Press. [ Links ]

Grimm, A. M., Ferraz, S. E. T., & Gomes, J. (1998). Precipitation anomalies in Southern Brazil associated with El Niño and La Niña events. Journal of Climate , 11, 2863-2880. [ Links ]

Haber, W. A. (2000). Plants and vegetation. In N. M. Nadkarni, & N. T. Wheelwright (Eds.), Monteverde: Ecology and Conservation of a Tropical Cloud Forest (pp. 39-70). Oxford: Oxford University Press. [ Links ]

Hartshorn, G. S. (1983). Plants. In D. H. Janzen (Ed.), Costa Rican Natural History (pp. 118-183). Il: Chicago University Press. [ Links ]

Hays, C. (1986). Effects of the 1982-83 El Niño on Humboldt Penguin colonies in Peru. Biological Conservation, 36, 169-180. [ Links ]

Holt, R. D. (1993). Ecology at the mesoscale: the influence of regional processes on local communities. In R. E. Ricklefs, & D. Schluter (Eds.), Species Diversity in Ecological Communities. Historical and Geographical Perspectives (pp. 77-88). Chicago: University of Chicago Press. [ Links ]

Holmgren, M., Scheffer, M., Ezcurra, E., Gutiérrez, J. R., & Mohren, G. M. J. (2001). El Niño effects on the dynamics of terrestrial ecosystems. Trends in Ecology and Evolution, 16, 89-94. [ Links ]

Idyll, C. P. (1973). The anchory crisis. Scientific American, 228, 22-29. [ Links ]

Jaksic, F. M., & Lazo, I. (1999). Response of a bird assemblage in semiarid Chile to the 1997-1998 El Niño. Wilson Bulletin, 111, 527-535. [ Links ]

Jaksic, F. M. (2001). Ecological effects of El Niño in terrestrial ecosystems of western South America. Ecography, 24, 241-250. [ Links ]

Kimura, K., Yumoto, T., Kikuzawa, K., & Kitayama, K. (2009). Flowering and fruiting seasonality of eight species of Medinilla (Melastomataceae) in a tropical montane forest of Mount Kinabalu, Borneo. Tropics, 18, 35-44. [ Links ]

Loiselle, B., & Blake, J. G. (1991). Temporal variation in birds and fruits along an elevational gradient in Costa Rica. Ecology, 72, 180-193. [ Links ]

McPhaden, M. J., Zebiak, S. E., & Glantz, M. H. (2006). ENSO as an integrating concept in earth science. Science , 314, 1740-1745. [ Links ]

National Audubon Society. (2010). The Christmas bird count historical results. Retrieved from http://www.christmasbirdcount.orgLinks ]

Nobre, P., & Shukla, J. (1996). Variations of sea surface temperature, wind stress, and rainfall over the tropical Atlantic of South America. Journal of Climate , 9, 2464-2479. [ Links ]

OTS. (2010). Conteos navideños La Selva OET, 1985-2005. Retrieved from http://www.ots.ac.cr/images/downloads/biological-stations/la-selva/species-lists/bird-counting/7conteos_85_2005Links ]

Paxton, K. L., Cohen, E. B., Paxton, E. H., Németh, Z., & Moore, F. R. (2014). El Niño-southern oscillation is linked to decreased energetic condition in long-distance migrants. PLoS ONE, 9, e95383. DOI: 10.1371/journal.pone.0095383 [ Links ]

Philander, S. G. H. (1985.) El Niño and la Niña. Journal of the Atmospheric Sciences, 42, 2652-2662. [ Links ]

R Core Team, (2013). R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. [ Links ]

Rechten, C. (1985). The waved albatross in 1983 El Niño leads to complete failure. In G. Robinson, & E. M. del Pino (Eds.), El Niño in the Galapagos Islands: the 1982-1983 Event (pp. 227-237). Ecuador: Charles Darwin Foundation for the Galapagos Islands. [ Links ]

Ropelewski, C. F., & Halpert, M. S. (1987). Global and regional scale precipitation associated with the El Niño/southern oscillation. Monthly Weather Review, 115, 1606-1626. [ Links ]

Sheffield, J., & Wood, E. F. (2008). Projected changes in drought occurrence under future global warming from multi-model, multi-scenario, IPCCAR4 simulations. Climate Dynamics, 31, 79-105. [ Links ]

Stiles, F. G. (1985). Seasonal patterns and coevolution in the hummingbird-flower community of a Costa Rican subtropical forest. Ornithological Monograph, 36, 757-787. [ Links ]

Stiles, F. G. (1992). Effects of a severe drought on the population of a tropical hummingbird. Ecology , 73, 1375-1390. [ Links ]

Tovar, H., Guillen, V., & Cabrera, D. (1987). Reproduction and population levels of Peruvian guano birds, 1980 to 1986. Journal of Geophysical Research , 92, 14445-14448. [ Links ]

Valle, C. A., Cruz, F., Cruz, J. B., Merlen, G., & Coulter, M. C. (1987). The impact of the 1982-83 El Niño-Southern Oscillation on seabirds in the Galapagos Islands, Ecuador. Journal of Geophysical Research , 92, 14437-14444. [ Links ]

Villalobos, R., & Retana, J. (2000). Costa Rica: Instituto Metorológico Nacional. In J. W. Jones (Ed.), Comparative Assessment of Agricultural Uses of ENSO-Based Climate Forecasts in Argentina, Costa Rica and Mexico (pp. 49-96). Florida: University of Florida. [ Links ]

Waylen, P. R., Quesada, M. E., & Caviedes, C. N. (1994). The effects of El Niño-Southern Oscillation on precipitation in San José, Costa Rica. International Journal of Climatoloty, 14, 559-568. [ Links ]

Waylen, P. R., & Caviedes, C. N. (1996). Interannual variability of monthly precipitation in Costa Rica. Journal of Climate , 9, 2606-2613. [ Links ]

Waylen, P. R., Caviedes, C. N., Poveda, G., Mesa, O., & Quesada, M. E. (1998). Rainfall distribution and regime in Costa Rica and its response to the El Niño-Southern Oscillation. Conference of Latin Americanist Geographers, 24, 75-84. [ Links ]

Williams-Linera, G., & Meave, J. (2002). Patrones fenológicos. In M. R. Guariguata, & G. H. Kattan (Eds.), Ecología y Conservación de Bosques Tropicales (pp. 407-431). Costa Rica: Editorial Tecnológica de Costa Rica. [ Links ]

Wolfe, J. D., & Ralph, C. J. (2009). Correlations between El Niño - southern oscillation and changes in Nearctic - Neotropic migrant condition in Central America. Auk, 126, 809-814. [ Links ]

Wolfe, J. D., Ralph, C. J., & Elizondo, P. (2015). Changes in the apparent survival of a tropical bird in response to the El Niño Southern Oscillation in mature and young forest in Costa Rica. Oecologia, 178, 715-721. [ Links ]

Worthington, A. (1996). Population sizes and breeding rhythms of two species of manakins in relation to food supply. In E. G. Jr. Leigh, A. S. Rand, & D. M. Windsor (Eds), Ecology of a Tropical Forest (pp. 213-225). Washington DC: Smithsonian Institution Press. [ Links ]

Wright, S. J., Carrasco, C., Calderón, O., & Paton, S. (1999). The El Niño Southern Oscillation, variable fruit production, and famine in a tropical forest. Ecology 80, 1632-1647. [ Links ]

Yodzis, P. (1993). Environment and trophodiversity. In R. E. Ricklefs, & D. Schluter (Eds.), Species Diversity in Ecological Communities. Historical and Geographical Perspectives (pp. 26-38). Chicago: University of Chicago Press. [ Links ]

Received: October 06, 2017; Revised: December 13, 2018; Accepted: January 17, 2019

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