Diet composition of nestlings and adults of the threatened Bolivian Swallow-tailed Cotinga Phibalura flavirostris boliviana ( Aves : Passeriformes : Cotingidae ) in Bolivia

tropical birds (Morton 1973). Although Neotropical birds such as manakins (Pipridae) and cotingas (Cotingidae) are considered frugivorous, they supplement their diet with arthropods and small vertebrates, and feed their nestlings partially or wholly on arthropods (Morton 1973; Moermond & Denslow 1985; Stutchbury & Morton 2001). Most fruit contains few nutrients (Moermond & Denslow 1985; Herrera 2001) and a supplementary diet of arthropods containing higher amounts of proteins, permits more rapid growth and development of nestlings (Morton 1973). The advantage of consuming animal protein in this way, likely explains the reports of insects in the diet of nestlings for some frugivorous birds such as Cock-of-the-rock (Luy & Bigio 1994; Snow 2004), Long-wattled Umbrellabird (Karubian et al. 2003), Redruffed Fruitcrow (Muir et al. 2008), Cinnamon-vented Diet composition of nestlings and adults of the threatened Bolivian Swallow-tailed Cotinga Phibalura flavirostris boliviana (Aves: Passeriformes: Cotingidae) in Bolivia

The Swallow-tailed Cotinga Phibalura flavirostris is a Neotropical species that consumes fruit and insects (Snow 2004).It is represented by a subspecies in the Atlantic forest of eastern Brazil (Phibalura flavirostris flavirostris) and another in the Andes of northwestern Bolivia (Phibalura flavirostris boliviana).Recent evidence support the Phibalura to be a member of the Cotingidae family within Phytotominae clade (Berv & Prum 2014).Both these subspecies are threatened by habitat loss and the Bolivian population Phibalura f. boliviana has been considered as a separate and Endangered species (IUCN 2012).Adults of the Bolivian population (Image 1), that inhabit semi-humid forest fragments in Apolo valley (1400-2000 m), were anecdotally observed feeding on fruits of Schefflera morototoni and catching insects in flight (Bromfield et al. 2004;Avalos 2009).However, quantitative details on the diet composition of adults and nestlings of this species are scarce.This information is important, given that the species deserves special conservation in Bolivia.Here, I quantify the nestling diet of the Bolivian Swallow-tailed Cotinga during its breeding months, as well as describing the adult diet during the breeding season.

Methods
I collected fecal samples near the village of Aten (68 0 19'53"W & 14 0 55'56"S, elevation 1400-1690m) in the municipality of Apolo, Department of La Paz, Bolivia (Image 2).This site is situated in the western part of the Andes mountain chain.This fragmented landscape is comprised of semi-humid forest fragments, mountain savannas and grassland zones.The small forest fragments are situated between ridges, ravines and hillsides (Foster & Gentry 1991).Several plants species such as Tapirira guianensis, Cecropia spp., Hyeronima alchornoides, Clusia spp., Nectandra cissiflora, Ficus spp., Pseudolmedia spp., Elaeagia microcarpa, Cyathea spp., Ormosia bopiensis can be found in Aten (Verónica del Rosario Avalos pers.obs.).The mountain savanna of Aten consists of shrubs and small trees like Alchornea triplinervia and Schefflera morototoni scattered over the mountain savanna.The vegetation formation comes from the pluvial and humid forests of the subandean region (series Eschweilera andina-Oenocarpus bataua), which is actually substituted in part by anthropogenic savannas (Navarro & Maldonado 2002).The changes were induced by ancestral destruction and bad natural resource management.The climate is seasonal, characterized by a wet season from October to March, and a dry season from April to August.
I collected fecal masses of nestlings from under seven nests every 2-4 days from November 2005 to February 2006, following recommendations by Sutherland (2004).The fecal masses, which consisted of fruit pulp, seeds and insects, were preserved in 70% ethanol.In the laboratory, I visually estimated proportions of fruit volumes (seeds and pulp remains), and insect using a 4x-stereoscope.Fruits were identified comparing seeds from plants collected in Aten and using botanic references from the National Herbarium of Bolivia (HNB).The number of fruits in each sample was estimated by counting the number of seeds that each fruit could contain.The arthropod remains were determined to the Order level using published identification keys (Ralph et al. 1985;Borror et al. 1989).Arthropod fragments sufficiently large to be identified, such as head capsule and thorax were quantified and mounted on glass slides for classification.
I determined the diet of adult birds by collecting fecal samples from under perches in trees (Sutherland 2004) or below nests that had been deserted during To analyze the variation of diet during the breeding season studied, the fecal masses of seven nests were grouped into an early (November-December) and a late (January-February) periods.Variation in fruit and insect compositions of the two periods was analyzed using the G-test of independence.Significance of the test was checked at α = 0.05.I used the R version 2.15.1 (R Development Core Team 2012) for this purpose.
Fruit composition of nestling fecal masses varied significantly between the breeding periods (G = 38.9,df = 5, P < 0.001).Araliaceae (S. morototoni) was most frequently represented in the diet during November and December followed by Myrsinaceae, Annonaceae and Melastomataceae, and fruit such as Lauraceae, Euphorbiaceae, Myrtaceae, Salicaceae and Araliaceae during January and February.The fruiting trees such as Schefflera patula, Ocotea cuprea, Guatteria cf.tricloclonia and Protium sp. were found in small forest fragments in the middle of ridges.S. morototoni was also found isolated in the mountain savanna (near the forest edge) and at the edge of the forest fragments.
The insect-part of the nestling diet comprised mostly of five orders (Table 1).Winged ants and wasps (Hymenoptera mainly represented by Ponerinae and Myrmicinae) were most frequent (58%), followed by Coleoptera (25%) and Homoptera (13%).The insect composition of the diet varied significantly between the periods (G = 51.5, df = 5, P < 0.01).Beetles, winged ants of the family Myrmicinae and other Hymenoptera were the main component of the nestling diet in the early breeding period, and winged ants of Ponerinae and other Hymenoptera predominated during the late breeding period.

Adult diet
The adult diet composition during the breeding months (from 20 fecal samples collected under perches of trees and eight samples collected in deserted nests) was comprised of 89% fruit (range 60-100 %) and 11% insects (range 0-40 %).All fecal samples of deserted nests contained a mixture of fruit and insects, whereas only 57% of fecal samples collected under perches contained fruit and insects.The fruit consumed by adults consisted mainly of S. morototoni (43%), followed by O. cuprea (15%) (Table 1).The insect-part of the diet was composed mainly of wasps and winged ants (54%), followed by Coleoptera (28%)(Table 1).

The diet of fruit and insects
A substantial proportion of the nestling diet of the Bolivian Swallow-tailed Cotinga was comprised of insects, which is consistent with data from several other species of cotingas (Snow 2004;Muir et al. 2008) and other frugivorous birds (i.e., Wheelwright 1983).Adult birds complement the low-protein content of fruit with insects in order to improve the growth and development of nestlings (Morton 1973;Moermond & Denslow 1985;Stutchbury & Morton 2001).However, as nestlings were 14 days old, fruit increased throughout the nestling period up to 50%, which is similar with nestlings of frugivorous birds such as fruitcrows (Muir et al. 2008).An increase in fruit diet prolongs the length of the nestling period for frugivorous birds (Morton 1973;Stutchbury & Morton 2001), and most cotingas are reported to have long nestling periods (Snow 2004).The nestling-period length for Swallow-tailed Cotinga was 27 days (Avalos 2011), probably a long period that might indicate the influence of fruits for this small to medium-size cotinga.
On the other hand, it is yet unsure if insects are eaten by adults year around.Even if the adults were seen foraging intensely on insects (Avalos 2009), that does not imply they are more insectivorous than nestlings.In fact, 57% of the fecal samples of adults analyzed, and the stomach content of one adult collected in September 2009 (sample # 4700 of Colección Boliviana de Fauna) contained only fruits.This pattern could be explained as a strategy in which adults eat mainly fruits and most insects caught are feed to nestlings (Morton 1973;Moermond & Denslow 1985;Stutchbury & Morton 2001).However, the insectivory could be seasonal or less frequent during some seasons.More information on the availability of food resources and diet in the habitat all year round is needed for better comprehension of resource exploitation.
The fruit composition of nestlings varied according to breeding months studied, suggesting that it could be related to the availability and energy content of ripe fruits.Indeed, at the end of the year the S. morototoni fruit were ripe, and when the fruiting stage ended, nestlings were predominantly fed with Ocotea spp., Hyeronima spp.and other fruiting plants that are found in semihumid forest fragments.Although data on nutritional content of each fruiting plant is scarce, nutritional data of fruiting families indicate that fruits of Euphorbiaceae, Myrsinaceae, Melastomataceae, Annonaceae, and Salicaceae have a high content in carbohydrates (see Snow 1981;Moermond & Denslow 1985), that could supplement the nestlings diet.S. morototoni and Ocotea spp.have a high content of proteins and lipids in their fruits (Snow 1981(Snow , 2004) that could be important to enhance the growth and development of nestlings.
Overall, three or four plant species are suggested to be important for many frugivorous birds, such as cotingas (Moermond & Denslow 1985;Snow 2004).Schefflera morototoni was very important during the breeding periods for adults and nestlings of Bolivian Swallow-tailed Cotinga, similarly to the Cock-of-therocks (Snow 1971;Schuchmann 1984;Luy & Bigio 1994).In contrast, the Brazilian Swallow-tailed Cotingas eat the mistletoe fruit of Loranthaceae, Myrsinaceae and Rubiaceae (Snow 1982;Pizo et al. 2002;Snow 2004).The high proportion of S. morototoni in the diet of the Bolivian Swallow-tailed Cotinga could be influenced by the availability of the fruiting trees.This plant species in different places of Bolivia have flowers and immature fruits throughout majority of the year, except May and January (pers.revision in HNB).The knowledge of fruiting phenology, abundance and tolerance to fires of this plant species, could be useful for a greater understanding of the feeding habits of the Bolivian Swallow-tailed Cotinga.

Conservation implications
Adults and nestlings of Bolivian Swallow-tailed Cotinga consumed fruits from fruiting trees that are found in forest fragments.The birds foraged at isolated trees of S. morototoni which grew near forest fragments (Avalos 2009), similar to some cotingas that forage for fruits in open areas near the forests (Pizo et al. 2002;Silva et al. 2002) or toucans that forage at Ficus trees in grasslands (Graham 2001).However, even though this species uses modified human impacted landscape, it does not indicate that a viable population could be sustained in an extensively modified habitat.A continuation of habitat modification caused by fires and cattle on the mountain savanna and in the semi-humid forest fragments of the Apolo valley could diminish the availability of many fruiting trees that may compromise the bird feeding.My data suggests that any management plan must include contingencies for the conservation of forest fragments, including the small patches of trees and shrubs in mountain savannas, to sustain the food resources needed for Bolivian Swallow-tailed Cotinga.

Figure 1 .
Figure 1.Percentage of fruit and insects in nestling diet of Bolivian Swallow-tailed Cotingas according to age classes.