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).

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; 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.

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.

RESUMEN

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

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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.

TABLE 1 (Continued)
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.

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

TABLE S1 (Continued)
	English name	Category	Size (mm)	Forest type
				Lowland rainforest	Premontane forest	Monatane forest
	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).