Ardeol a 63(2), 2016, 357-367 DOI: 10.13157/arla.63.2.2016.sc2

NOTES ON THE DIET OF THE ENDEMIC RED-EARED PARAKEET PYRRHURA HOEMATOTIS AND OTHER VENEZUELAN MONTANE

NOTAS SOBRE LA DIETA DE LA ENDÉMICA COTORRA COLIRROJA PYRRHURA HOEMATOTIS Y OTROS LOROS MONTANOS DE VENEZUELA

1 1 Galo BUITRóN -J URAD O * an dVIRGINIA SAN Z

SUMMARY .— Information on the diet of some species of tropical parrots is still scarce. We present data on the feeding ecology of the red-eared parakeet Pyrrhura hoematotis , an endemic and poorly known species of Venezuelan montane forests. Additionally, we describe other observations on the diet of the Venezuelan parakeet Pyrrhura emma , scarlet-fronted parakeet Psittacara wagler i and lilac-tailed Touit batavicus . Red-eared parakeets used thirteen species of plants and their diet consisted principally of arillate seeds, but also included fleshy fruits and flowers. Tree species of Euphorbiaceae were main items in the diet of red-eared and scarlet-fronted parakeets. Leaves and resin of Clusia alata trees are reported for the first time in the diet of the lilac-tailed parrotlet. Our results add basic natural history data that can be useful for the conservation of these restricted distribution species that are threatened by the habitat loss. Key word s: cloud forests, diet, , seed predators, South America, Yacambú National Park.

RESUMEN .— Información acerca de la dieta de algunas especies de loros tropicales es aún deficiente. Presentamos datos sobre la dieta de la cotorra colirroja Pyrrhura hoematotis , una especie endémica y pobremente conocida de los bosques montanos venezolanos. Adicionalmente, describimos otras obser - vaciones sobre la dieta de la cotorra de Emma Pyrrhura emma , aratinga de Wagler Psittacara wagleri y cotorrita siete colores Touit batavicus . La cotorra colirroja utilizó trece especies de plantas y su dieta consistió principalmente en semillas ariladas, aunque también incluyó frutos carnosos y flores. Espe - cies arbóreas de la familia Euphorbiaceae fueron los ítems principales tanto en la dieta de la cotorra colirroja como en la aratinga de Wagler. Las hojas y resina de árboles de Clusia alata son reportadas por primera vez en la dieta de la cotorrita siete colores. Nuestros resultados añaden datos básicos de historia natural que pueden ser útiles para la conservación de estas especies de loros que tienen una distribución restringida y están amenazados por la pérdida de hábitat. Palabras clave : bosques nebulosos, depredadores de semillas, dieta, Parque Nacional Yacambú, Psittacidae, Sudamérica.

1 Laboratorio de Biología de Organismos, Centro de Ecología, Instituto Venezolano de Investigaciones Científicas (IVIC), Caracas 1020-A, Apartado 2032, Venezuela.

* Corresponding author: [email protected] 358 BUITRóN -JURADO , G. an d SANZ , V.

INTRODUCTION and national red lists, despite the lack of data on diet and population size, and a probable The natural history of many tropical parrot recent decline due to habitat loss within its species is still poorly known, although this limited distributional range (Rodríguez and information is essential for their conservation Rojas-Suárez, 2008; IUCN, 2014). Here we (Mack and Wright, 1998; Botero-Delgadillo et present data on the diet of this parakeet from al. , 2010). Detailed data on habitats and diets Yacambú National Park, Venezuela. We also of several tropical parrots are still needed describe a few observations on habitats and to assess their vulnerability to habitat loss diets of other scarcely known South Ameri - and global climatic change, especially for can parrot species: the Venezuelan parakeet endemic species facing a greater risk of Pyrrhura emma , scarlet-fronted Psittacara extinction related to the synergistic effects of wagleri parakeet and lilac-tailed parrotlet narrow ecological niches and limited ranges Touit batavicus , obtained in Yacambú Na - (Walker, 2006; Slatyer et al. , 2013). Diet tional Park and in a montane forest remnant data are also important to understand the in Altos de Pipe, in the Venezuelan Coastal parrots’ role in the functioning and persis - Cordillera. tence of ecosystem s. Parrots form large feeding flocks and are important pre-disper - sal seed predators, probably affecting the MATERIAL AND METHODS recruitment patterns of tropical tree species due to their high removal and consumption Study area rates (Pizo et al. , 1995; Villaseñor-Sánchez et al. , 2010). Conversely, some parrot species Observations were done at two montane pollinate several plant species (Vicentini forest sites in Venezuela. The first area was and Fischer, 1999; Hingston et al. , 2004). the montane forests around El Blanquito, Venezuela accommodates 47 native species within the Yacambú National Park (10° 24’ N of parrots, parakeets and macaws (BirdLife , 66° 55’ W, 1650 m) in the Andes, Lara State. 2014). The biology of many of these is Yacambú National Park covers ca. 27,000 ha poorly known, especially of those, such as and the climate is humid with a mean annual the endemic red-eared parakeet Pyrrhura temperature of 20 °C and an estimated annual hoematoti s, that inhabit humid montane rainfall of over 2000 mm with two peaks, forests. This parakeet inhabits montane in May-July and in October (Goodwin and forests from 600 to 2400 m.a.s.l., although it Lentino, 1990). Lower montane rainforests is found mainly between 1000 to 2000 m.a.s.l. cover most of the park. It is considered an (Hilty, 2003). Two subspecies are recog - Important Area (IBA) due to the species nised on the basis of differences in plumage richness (255) and the presence of several coloration and geographic distribution. P. h. threatened species such as the helmeted hoematotis is found along the western part of curassow Pauxi pauxi , wattled guan Aburria the Coastal Cordillera between Aragua and aburri and rust y- flanked rail Laterallus Miranda states, including Macarao, San Este - levraudi (Lentino and Esclasans, 2005). ban and Henri Pittier national parks. P. h. in - The second site was an isolated forest frag - marginata is only known from a very limited ment (300 ha) in Altos de Pipe (10° 24’ N area on Cubiro, Lara State (Hilty, 2003; 66° 55’ W, 1600 m), a summit of an internal Restall et al. , 2006; Juniper and Parr, 2010). branch of the Coastal Cordillera, Miranda The red-eared parakeet is currently re - State. The climate is humid and rainy with garded as a ‘Least concern’ species in global an annual rainfall of 1063 mm and a mean

Ardeol a 63(2) , 2016 , 357-367 DIET OF VENEZUELAN MONTANE PARAKEETS 359 annual temperature of 17 °C; the site is Machado, 2001). The number of fruits re - covered by mist during several months of moved either by swallowing or carrying the year (Casañas and Jauregui, 2011). The away by a single individual during each vegetation is also classified as lower mon - observation was used to determine the re - tane rainforest, although a variety of habitats moval rate. The diameter of the smallest are found due to the different successional and largest axis (measured with calipers to stages of the vegetation resulting from the the nearest mm) of a sample of at least five past 50 years of land conversion. fruits and seeds of the plant species con - sumed was recorded in the field to determine the size range of items consumed. Specimens Field surveys of food plants were collected and identified by comparison with samples in the National Observations were performed in five 1-ha Herbarium of Venezuela. These data permit - plots in mature and old secondary forests ted us to calculate the overall dietary breadth within both survey sites, at elevations rang - for red-eared parakeets using the standardised ing from 1500 to 1700 m. We observed the Levins niche breadth index (Levins, 1968), parrots during eleven surveys of eight days where values close to zero indicate dietary each, nine carried out monthly from January specialisation and values close to one indi - to October 2011. Two additional surveys cate a broad diet (Krebs, 1999). The index were done in Yacambú in November 2010 was not calculated for the other three species and February 201 2. Parrot observations since too few records were obtained. were performed in the morning from 06:30 Phenological data on the presence and to 12:00, and in the afternoon, from 15:00 to absence of fleshy fruits of 42 tree species 17:00, avoiding heavy rain or mist, yielding in Yacambú were available as part of a con - a total of 280 sampling hours in each study comitant study of frugivorous in both area. Parrots were located using visual and areas (Buitrón-Jurado, 2012). Fruit-bearing aural clues in both study areas. Basic data trees ≥ 10 cm in diameter at breast height such as date, time, flock size, habitat, and (DBH) were registered within each 1-ha plot behaviour were recorded for each encounter. and recorded as an edible source when any When parrots were observed foraging, we frugivorous birds were observed eating them. also recorded the plant species and part eaten Data on the fruit crops of two tree species, (i.e. fruit pulp, seeds, or flowers), foraging Cecropia angustifolia and Tetrorchidium height and technique (gleaning, reaching, rubrivenium were also recorded. Ten mature and hanging) (Galetti, 1997; Kristoch and trees of both species with a trunk diameter Marcondes-Machado, 2001). A feeding bout greater than 10 cm were monitored for nine was defined as an observation of one or more months to determine the number and ripeness individuals feeding on a food source (Ren - of fruits. To visually estimate the number of ton, 2006). In the latter case, the behaviour fruits in a tree, fruits were counted on ten was recorded for a single, randomly chosen branches and the total number of fruiting individual and was assumed to be represen - branches was counted for each tree to calcu - tative of the entire flock, to avoid problems late the total number of fruits on each indi - related to lack of independence of sequential vidual (Chapman et a l. , 1992). These data observations (Renton, 2006; Walker, 2006). were used to explore whether monthly parrot If the birds moved to another plant and abundance was related to fruit availability, started feeding, this was considered as a using Spearman rank correlations. Data are new feeding bout (Kristoch and Marcondes- shown as means ± S. E.

Ardeol a 63(2) , 2016 , 357-367 360 BUITRóN -JURADO , G. an d SANZ , V.

FIG . 1. —A) Monthly number of sightings (means ± S. E.) of red-eared parakeets Pyrrhura hoematotis ; B) Number of fruiting tree species; C) Crop size of ten trees Tetrorchidium rubrivenium (black) and Cecropia angustifolia (grey) during 2011 in El Blanquito, Yacambú National Park, Venezuela. [A) Número de observaciones mensuales (media ± S. E.) de la cotorra colirroja Pyrrhura hoematotis ; B) número de especies de árboles con frutos; C) tamaño de la cosecha de frutos de 10 árboles de Tetrorchidium rubrivenium (negro) y Cecropia angustifolia (gris) durante el año 2011 en El Blanquito, Parque Nacional Yacambú, Venezuela.]

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RESULTS parakeets also included Inga oerstediana pods in their diet; a group o f three was ob - Red-eared parakeet served consuming these fruits on November 2010. Levins’ niche breadth value was 0.65, Flock size and habitat. Red-eared para - and the fruit removal rate varied according keets were observed only in the Yacambú to food plant, ranging from 2 to 24 items –1 National Park during all surveys, although mi n (9.7 ± 2.4, N = 23) (table 1). The they were more frequently recorded in May, sizes of the consumed items ranged from Jun e, and September (fig. 1A). Parakeets 1.6 to 9.6 mm (7.5 ± 0.5, N = 20). Foraging were generally observed flying or perching behaviour included gleaning and acrobatic during the early morning in flocks of 1-25 techniques such as hanging down or reaching individuals (4 ± 0.6, N = 50). Flocks flew out to fruits. Parakeets also took fruits with fast and generally close to the forest canopy. the foot and bit off pieces, on two occasions. At midday, groups were observed resting in the canopy of tall trees. Most records (n = 28) Parakeet abundance and fruit availability. were obtained in tall secondary forest domi - Most tree species were observed carrying nated by trees of Myrcia acuminata , Al - fruits in April, May, and August in Yacambú, chornea triplinervia and the exotic Euca - including almost all the species consumed lyptus, in plots at low altitude in our survey by the red-eared parakeet, with the excep - area . In this area, we observed also a pair tion of Heliocarpus americanus , which was copulating for a few seconds in June 2011. observed with dry indehiscent fruits in Parakeets were also observed (N = 25) on March. Nevertheless, we found no associa - the edges of tall mature forests at 1700 m, tion between the number of tree species these dominated by tree species such as carrying fruits (figure 1B) and the number Pouteria baehniana, Cecropia angustifolia , of parakeets (rs = 0.06, N = 10, P = 0.8 ). Calatola costaricensis and the palm Wettinia Neither was there an association between praemorsa . parakeet abundance and the number of fruits of Cecropia angustifolia (rs = –0.46, N = 9, Diet. We observed 23 feeding bouts (90 P = 0.21 ) nor Tetrorchidium rubrivenium individuals). Red-eared parakeets foraged in (r = 0.45, N= 9, P = 0.2). The fruit abundance the sub-canopy (12 ± 0.8 m, N = 22) and of both tree species is showed in fig. 1C. they fed on thirteen plant species from nine families during the study period (table 1). The main items consumed, based on the Venezuelan parakeet number of feeding bouts, were arillate seeds of Euphorbiaceae, from mature fruits of We obtained three records of this species, Tetrorchidium rubrivenium and Alchornea all in Altos de Pipe where it seems to be triplinervia, and immature fruits of Sapium scarce. The first was on 20 February 2011: a stylare . Capsules of these tree species were group of three individuals were observed less than 10 mm in diameter and contained perched at the top of a tree of Clethra lanata one to three arillate seeds that turned red (Clethraceae) during the morning. A group when ripe. Other items eaten were seeds of three individuals was also recorded on 23 of Croton gossypifolius (Euphorbiaceae), March 2011 resting on branches of a tree of flowers of Erythrina and Ocotea , and fleshy Alchornea triplinervia. Finally, four indi - fruits of Geonoma undata (Arecaceae), viduals were observed at 20 m at the top of Cecropia angustifolia (Urticaceae) and a tree of Eschweilera tenax (Lecythidaceae) Guettarda crispiflora (Rubiaceae). Red-eared on 17 June 2011. All our observations were

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Ardeol a 63(2) , 2016 , 357-367 DIET OF VENEZUELAN MONTANE PARAKEETS 363 made in mature forest where common tree branches (3-5 m up) in a tree of Clusia alata species included Nectandra laurel (Lau - (Clusiaceae; 5 m high, 19.4 cm diameter). raceae), Matayba longipes (Celastraceae) , Their foraging behaviour was remarkable Graffenrieda latifoli a (Melastomataceae) because at least three individuals consumed and the palm Wettinia praemorsa (Areca- the sap of the tree. They scratched the green ceae). A single feeding bout was recorded twigs of the branch-tips to remove the bark on 17 June 2011 when one parakeet con - gently, especially at the base of fresh young sumed the ripe fruits of Cecropia angusti - leaves, from where they licked the emerging fo lia ,10mup in the crown. sap. One of the individuals also broke a leaf petiole and ate the lamin a. A young bud was eaten by another bird, which responded Scarlet-fronted parakeet aggressively to another approaching indi - vidua l. The birds remained silent while The scarle t- fronted parakeet was only feeding, holding on to the branches with recorded in Yacambú where it seemed to both feet while pecking at the leaf bases be a seasonal visitant. Flocks of 3-50 indi - from below. The group chewed and broke viduals (15 ± 3.3, N = 13) were observed, four leaves during the thirty minutes that first in November 2010 and between Sep - they remained perched in the tree. Three indi - tember to November 2011 at 1700 m. Their viduals moved to eat the young capsules of a presence coincided with the fruiting of neighbouring Clusi a tree and remained there species of Euphorbiaceae such as Sapium for another five minutes before flying away. stylare and Tetrochidium rubrivenium . These Our study provides information on the flocks remained perched and feeding for 10 habitat and foraging ecology of four tropical to 30 minutes in emergent trees of Sapium parrot species and is the first detailed study stylare. The forest was tall, as described for of the diet of the endemic red-eared parakeet. the red-eared parakeet. Previous accounts of the ecology of the red- We observed 16 feeding bouts (129 indi - eared parakeet indicate that it inhabits tall viduals) in Yacambú only, all of them on mature forests in Rancho Grande in the immature fruits of Sapium stylare . During Venezuelan Coastal Cordillera, where flocks feeding, birds were noisily cracking fruits and are seen all year round close to the canopy giving frequent calls that can be described and in the forest edges (Lentino and Portas, as “ kleea, kleea, kleeaa ” (record XC131795, 1994). Our findings accord with these pre - available at http://www.xeno-canto.org). The vious observations, since red-eared parakeets parakeets took the capsules directly from were observed in tall mature and secondary the branches (90 %), although some hanging forests. Nevertheless, the tree species com - manoeuvres were also observed. Fruit re - position in Yacambú differs and the vegeta - –1 moval rates ranged from 2 to 11 fruits mi n tion is of lesser stature than the montane (7 ± 0.7, N = 16). forests in Rancho Grande (GBJ pers. obs.). To date, only fleshy fruits of Psidium sp . (Myrtaceae) had been recorded as con - Lilac-tailed parrotlet sumed by the red-eared parakeet (Fernán - de z- Badillo et a l. , 199 4, GBJ per s. ob s.). This species was only recorded in Altos We found, however, that the red-eared para - de Pipe, where we observed a single group. keet fed on a diversity of food resources, Six individuals were observed on 7 October including the fleshy fruits, flowers, and seeds 2010 at 07:45 hrs on the margin of secondary of several tree species, as do other Pyrrhura forest while feeding among the lower species (Toyne et al. , 1992; Ragusa-Netto,

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2007; Botero-Delgadillo et al. , 2010, 2013). feeds on fruits, seeds and flowers and it has The diet of red-eared parakeets included tree been observed eating flowers of Erythrina genera with fleshy fruits such as Cecropia as (Fabaceae), seeds of Heliocarpus (Tilliaceae) well as tree species producing large crops of and fleshy fruits of Turpinia occidentalis arillate seeds, such as Alchornea triplinervia, (Staphyleaceae) (Juniper and Parr, 2010; M. Sapium stylare and Tetrochidium rubrive - González, pers. comm.; GBJ, pers. obs.). nium. These food items have been recorded The same applies to the scarlet-fronted para - previously in the diet of other Andean keet whose diet has been reported to include Pyrrhura specie s, including the white- flowers, fruits and seeds, especially maize breasted P. albipectus and the rose-fronted (Juniper and Par r, 2010). It has been ob - P. rhodocephala parakeets (Toyne, 1992; served eating guavas Psidium guajaba and Aguilar, 1996 ). Nevertheless, none of the Erythrina fusca in Colombia (Rodríguez- Andean species have been reported con - Mahecha and Hernández Camacho, 2002). suming palm fruits, as does the red-eared Our observation on the diet of the scarlet- parakeet (Toyn e, 199 2; Aguila r, 199 6; fronted parakeet in Yacambú showed a heavy Botero-Delgadillo et al. , 2010, 2013). The consumption of immature and mature fruits dietary breadth of the inmarginata form of of Sapium stylare . the red-eared parakeet was similar to values Touit species are among the least known reported with comparable sampling efforts parrots in South America. Data on the diet of for other restricted-range Neotropical para - the lilac-tailed parrotlet and blue-fronted keets, such as the Santa Marta P. viridicata parrotlet Touit dilectissima indicate the con - and Todd’s P. caeruleiceps parakeets (Botero- sumption of Clusia fruits in Colombia and Delgadillo et al. , 2010, 2013). Nevertheless, Ecuador, respectively (Troncoso et al. , 1995; in the view of the separate distributions of Olaciregui and Ureña, 2011; Liu and Lyons, the two red-eared parakeet subspecies, it is 2012). Our observation corroborated the use possible that differences in their diet occur of Clusiaceae by the lilac-tailed parrotlet, and this requires further study. and shows that Clusia trees also could pro - We did not find any correlations between vide additional feeding resources to these parrot occurrence and the number of fruiting such as sap, flowers and leaves. All tree species nor with the two tree species for these resources are consumed by only a few which fruit crop data were available. This species. Nectar has been suggests that re d- eared parakeets do not recorded in the diet of the golden-winged show a strong association with the crops of Brotogeris chrysopterus , yellow-chevroned these tree species, and probably the abun - B. chiriri and white-eyed parakeets Psittacara dance of other food resources (e. g. dry leucophtalmus and the green-thighed parrot seeds) needs to be taken in account. The Pionites leucogaster (Vicentini and Fischer, absence of such correlation, however, could 1999). Sap has been previously recorded in be also associated with the small sample the diet of the military macaw Ara militaris size of our study or from factors unrelated which also includes leaves, as the diets of to feeding resources, such as the availability the reddish-bellied and Todd’s parakeets of nesting cavities (Brightsmith, 2005). (Pizo et al. , 1995; Kristoch and Marcondes- Data on the habitats and diets of the other Machado, 2001; Contreras-González et al. , three parrot species observed are extremely 2009). Further studies are needed, however, scarce. There are no detailed accounts of to corroborate if the consumption of sap, a plant species or parts included in the diet of particular reward for pollinators in Clusia the Venezuelan parakeet. Anecdotal observa - species (Martins et al. , 2007), and leaves is tions indicate that the Venezuelan parakeet frequent among Touit parrotlets.

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The considerable use of arillate fruits of though knowledge about their habitat s, Euphorbiaceae and Clusiaceae among our breeding requirements and populations is parrot species is probably related to the deficient. These species may be at greater greater nutritional value of such fruits rela - extinction risk than the scarlet-fronted para - tive to fleshy and juicy fruit s, which are keet, which has been recently uplisted to richer in carbohydrates and water but poorer ‘Near-threatened’ (IUCN, 2014). The two in protein and fat (Galetti et al. , 2000; Gilar - endemic species of Pyrrhura parakeets occur di and Toft, 2012). Our observations of the in mature montane forests, although they feeding ecology of the four parrot species have a more restricted area of occupancy also suggest that they act as pre-dispersal than the scarlet-fronted parakeet and are less seed predators as do other Psittacidae (Pizo abundant than in the past when flocks of et al. , 1995; Villaseñor-Sánchez et al. , 2010). 100 individuals were recorded (Fernández- All four species included seeds in their Badillo et al. , 1994). Red-eared and Venezue - diets, some of them obtained from imma - lan parakeets face important conservation ture fruits. Nevertheless, the red-eared and issues due to habitat los s. They require Venezuelan parakeets could in addition act urgent population assessments to determine as endozoochorous seed dispersers for their extinction risk, especially the red-eared small-seeded tree species such as Cecropia parakeet which seems to be less tolerant of angustifolia and Guettarda crispiflora, or habitat fragmentation and was not recorded may disperse them by epizoochory (Tella in Altos de Pipe. Further field efforts should et al. , 2015). focus on assessing the population sizes of It has been suggested that the limited areas parrots within Yacambú National Park and of occupancy of some endemic bird species the importance of other feeding resources in Venezuela are related to specific habitats (e.g. dry seeds) on their abundance, as well or to resources available in montane areas as on confirming the presence of red-eared near the coast (Boesman, 1998). The abun - parakeets in nearby national parks that har - dance of tree species with arillate seeds and bour montane forest s, such as El Guache heavy fruit crops, such as Sapium stylare , and Terepaima. Alchornea triplinervia and Tetrorchidium rubrivenium , could be a factor influencing the distribution or movements of the scarlet- ACKNOWLEDGEMENTS .—We would like to thank fronted parakeet in a similar manner to that to Maira Mendez and the Regional Direction of seen in other South American parrots that are INPARQUES Lara for permission to work in known to wander over large areas seeking Yacambú National Park. Valuable field assistance patches of abundant and ephemeral feeding was provided by Leonardo Alvarado and Vilisa Morón. We are also grateful to Leyda Rodríguez resources (Galetti, 1997; Renton, 2001; Ra - and José Grande of the Venezuelan National gusa-Netto, 2004). In Yacambú, our data in - Herbarium (VEN) and Angel Fernández (IVIC) dicated also that sympatric species of para - for helping us with the identification of plant keet s, such as the re d- eared and scarlet species. Our thanks also to María L. González for fronted parakeets, may show different re - sharing observations and Ana Contreras-González sponses to fruit availability. Further studies who provided helpful comments, as well as to two of the relationship between feeding resource anonymous referees who commented on early ver - availability and the seasonal movements of sions of the manuscript. Fieldwork was supported Venezuelan parakeets are needed to eluci - by IDEAWILD, The Rufford Small Grant Foun - date their vulnerability to habitat loss. dation (no. 9163-1) and IVIC. Our research was Red-eared and Venezuelan parakeets are authorised by the Ministerio del Poder Popular considered ‘Least concern’ species even para el Ambiente de Venezuela (Permit No. I-176).

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