Short Communication
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Emu, 2011, 111, 217–221
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Nesting biology of the Yellow-faced Parrot (Alipiopsitta xanthops), a species without nest-site fidelity: an indication of high cavity availability? Raphael Igor Dias Programa de Pós-gradua¸c ão em Ecologia, Universidade de Brasília, Brasília, 70253-060, Brazil. Email:
[email protected]
Abstract. Parrots are considered a globally threatened group but, despite that, little is known about the ecology, reproduction and behaviour of many species in the wild, especially those of dry tropical habitats. I studied the breeding biology of the Yellow-faced Parrot (Alipiopsitta xanthops) between 2007 and 2009. Yellow-faced Parrots are endemic to the Cerrado (neotropical savanna) biome of central South America. Their reproductive biology is poorly known and here I provide basic information on reproduction, including breeding success, nest-site characteristics, and whether the availability of cavities is a limiting factor. Average clutch-size was two eggs, and hatching success was high (92%). All nests were in cavities in termite mounds, with used cavities deeper and with wider entrances than cavities that were not used. Entrances to nests were orientated towards the north-east. Although the number of cavities in the environment appears to be high, specific nesting requirements and competition with other cavity-nesting birds and insects may reduce the number of cavities that can be used. Nevertheless, nests were never observed to be reused and site-fidelity appeared to be low. Specific nesting requirements and low site-fidelity may create problems for near-threatened species with declining populations, such as the Yellow-faced Parrot. Additional studies and the immediate implementation of conservation actions are essential to avoid future declines of populations of Yellow-faced Parrots. Additional keywords: breeding success, cavity reoccupation, neotropical, nest-site selection, reproduction.
Introduction Despite the immense interest humans have in parrots (order Psittaciformes), there have been fewer studies on this group in the wild compared with other avian taxa (Collar 1997). In the neotropical region there is a lack of basic biological data for most species of parrot, though there have been a number of recent studies (Renton and Salinas-Melgoza 2004; Sanz and Rodríguez-Ferraro 2006). This is significant because some 31% of neotropical parrots are generally considered at risk of global extinction (Collar et al. 1994), with the main causal factors being loss and fragmentation of habitat (Snyder et al. 2000). Further, within the neotropics, there is little information on the ecology, reproduction and behaviour of parrots of savanna and neotropical savanna habitats, such as the Cerrado biome (Oliveira and Marquis 2002). The Cerrado biome has undergone significant change in structure and extent in the past four decades as a result of intensive agricultural development, including production of soybeans (Klink and Moreira 2002). This lack of basic information makes identification of specific threats and development of conservation measures difficult. As most parrots are secondary cavity nesters they are unable to excavate their own nests and rely on pre-existing cavities, which is important because competition for nesting sites is common (Heinsohn et al. 2003). Unfortunately, most of the information on the availability and attributes of cavities and the use and Royal Australasian Ornithologists Union 2011
frequency of reuse of cavities is based on northern hemisphere studies. There is little known about the effects of cavity availability on populations of cavity-nesting bird in the neotropics (Cornelius et al. 2008). Some studies suggest that limitations on cavity availability in the neotropics might be higher than in temperate regions (Gibbs et al. 1993) whereas other studies have shown low levels of cavity reuse, suggesting that the number of cavities is not a limiting factor (Cockle et al. 2008) and others report high rates of cavity reuse, which is usually linked to low cavity availability (Heinsohn et al. 2003; Sanz and RodríguezFerraro 2006). The species investigated in this study was the Yellow-faced Parrot (Alipiopsitta xanthops), a generalist forager (Araújo 2007; Bianchi 2009) endemic to savanna and neotropical savanna habitats, with a wide distribution in Brazil (Sick 1997) and northern Bolivia (Remsen et al. 1986). The Yellow-faced Parrot was thought to nest in tree cavities (Collar 1997). However, a study in central Brazil only found nests in termite mounds (Bianchi 2009). The species is classified as near threatened because its population is suspected to be declining owing to habitat loss (BirdLife International 2010), and it is considered extinct in the wild in the state of São Paulo (Garcia and Marini 2006). However little is known about its breeding biology, ecology and behaviour (but see Araújo 2007; Bianchi 2009). 10.1071/MU10076
0158-4197/11/030217
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The aim of this study was to gather information on the breeding biology of the Yellow-faced Parrot to improve knowledge of the species in order to help develop conservation strategies. For that purpose, I quantified reproductive rates, identified the characteristics of nests used by Parrots, assessed the effect of cavity availability and the patterns of reuse of nests to discuss possible effects on population demography. Materials and methods Study site and general procedures This study was conducted in central Brazil, at the Fazenda Água Limpa (15560 S, 47550 W), a core area of the Brazilian Cerrado. The Fazenda Água Limpa is an area of 4500 ha, of different vegetation types, from open grasslands (a dry grassland without shrubs or trees) to cerrado sensu stricto (3–8 m tall physiognomy dominated by trees and shrubs but also presenting some herbaceous vegetation) and gallery forests (narrow forest strip following watercourses) (Oliveira-Filho and Ratter 2002). The climate in the region is seasonal, comprising the distinctive dry and wet seasons (Eiten 1993). The study was conducted over three breeding seasons (June– October) from 2007 to 2009. Searches to locate all cavities in the area, in trees and in termite mounds, were conducted, and their position recorded with a GPS. In addition, 40 nesting boxes were provided for the seasons of 2008 and 2009. I conducted searches for nests from June to October. Active nests were identified by searching cavities and determining their contents. Active nests were monitored every 3–5 days, using a mirror fixed on a metal pole (50 cm long) and a flashlight. Details of the nesting site were recorded after nesting was completed and chicks had fledged. Nest-site characteristics measured included: height of the tree or termite mound in which the nest cavity occurred; height of the cavity entrance from the ground; size of the entrance (width at widest point); depth of the cavity; orientation of the cavity (determined using a compass); and percentage of ground-cover of vegetation in 2-m radius of the nest. The same variables were recorded for the nearest unused cavity. After the nest-site measurements, the distance to the nearest neighbouring nest was calculated. Nesting was considered successful when a nestling vanished from the nest with no sign of predation within 5 days of the expected fledging date. Cavities were considered to have been reoccupied when the same cavity was used in subsequent years. Statistical analysis Analyses were performed with the program R (v2.9.2; R Development Core Team 2009). The data were tested for normality and all results are presented as means s.d. Student t-tests were used to examine differences between used and unused sites and the significance level was adjusted for multiple comparisons with Bonferroni correction. To evaluate orientation of cavity entrances, I used circular statistics to calculate directionality of used and unused cavities with Rayleigh’s test (Zar 1999). Differences in mean entrance orientation between both groups of cavities were evaluated with the nonparametric Watson’s test (Zar 1999). Wilcoxon test was used to evaluate the difference between the distance of active nests within a breeding season (2009) and the distance of the same nests to the nearest nest from
R. I. Dias
the previous year (2008). The analysis was restricted to the dataset of the last breeding season to avoid over-duplication of these two distances values between years. Results I found 14 Yellow-faced Parrot nests during the three breeding seasons. I checked an average of 144.00 27.73 cavities per year (range 90–182), in trees and in termite mounds, and found an average of 4.6 0.9 active Parrot nests per year (range 3–6). In the 2008 and 2009 breeding seasons, 40 nest-boxes were placed in trees, but these were not used by Yellow-faced Parrots. On average, 20% of the natural cavities were occupied annually by different bird species with some overlap with the breeding period of Yellow-faced Parrots. Additionally, bees and wasps occupied an average of 8% of cavities per year. Of the 40 nest-boxes, 12% were used by different bird species with some overlap with the breeding period of the Yellow-faced Parrot, and 9% were occupied by bees or wasps (Table 1). All cavities used by the Yellow-faced Parrot were old nests excavated in termitaria by Campo Flickers (Colaptes campestris); these termitaria seemed to be unoccupied by termites. Comparison between used cavities and available cavities in the area revealed that used cavities had a deeper chamber and a wider entrance (Table 2). Moreover, I observed a directionality in the entrance orientation of used cavities (73.52 56.36, R = 0.516, Rayleigh’s z-test; z = 7.22, P < 0.05; Fig. 1) but not for unused Table 1. Numbers of cavities found and checked in trees and termitaria and the numbers of Yellow-faced Parrot nests found over three breeding seasons (2007–09) in central Brazil Forty nest-boxes were also placed in the study area for the 2008 and 2009 breeding seasons Type of cavity
Numbers of cavities
Termite mound Tree Nest-box Total
136 46 40 222
Numbers of nests Yellow-faced Other bird Bees and Parrot species wasps 14 0 0 14
62 24 15 101
23 11 11 45
Table 2. Measurements of cavities used as nests by Yellow-faced Parrots Figures are means s.d.; n = 14 for both samples; significant values after Bonferroni correction are in bold Parameter Height of termite mound (cm) Height of cavity entrance from the ground (cm) Depth of cavity (cm) Width of entrance (mm) Vegetation cover in 2-m radius of nest (%)
Used
Unused
t
P
88.92 ± 14.41
89.21 ± 15.36
0.05
0.96
59.14 ± 15.46
60.69 ± 15.01
0.26
0.79
27.74 ± 5.12 89.73 ± 4.82
20.71 ± 6.85 81.12 ± 6.38
–3.02 –4.02
61.42 ± 22.82
66.42 ± 27.20
0.52
0.005 0.0004 0.60
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Fig. 1. Entrance orientation () for cavities used by Yellow-faced Parrots and for unused cavities. Arrows represent mean direction for each distribution. Means, and their angular deviation, for used and unused cavities are 73.52 56.36 (R = 0.516) and 340.82 74.48 (R = 0.155) respectively (n = 14 for both samples).
cavities (340.82 74.48, R = 0.155, z = 2.79, P > 0.05; Fig. 1), with used cavities on average orientated towards the north-east. There was a significant difference between the orientation of entrances between used and unused cavities (Watson’s test, U2 = 6.06, P < 0.001). Clutch-size was from one to three eggs (mean 2.2 0.6, n = 10 clutches). Hatching success was high, with a total of 92% of all eggs hatching, although not all nests were found at incubation. Hatching was asynchronous, chicks hatching at intervals of 2–3 day. All eggs that hatched produced fledglings. Of the 14 nesting attempts, 64% (nine) were successful and 36% (5) failed, all through predation at the egg stage. Based on Mayfield estimation (Mayfield 1961), the daily survival probability of the Yellow-faced Parrot was 0.987 and the total survival probability considering an entire nesting period of ~72 days was 39%. All predation occurred during the incubation period, which lasts 23–26 days. Fledging occurs approximately 45–50 days after hatching. No cavities were observed to be reused by Yellow-faced Parrots during the study. The mean distance to the nearest active nest within a nesting season for all breeding seasons was 2.38 1.16 km, and for the 2009 season alone was 2.41 0.26 km. The mean distance between nests found in the 2009 breeding season to the nearest cavities used in the previous year (2008) was 1.32 0.55 km. The distance of 2009 nests to nests used in the previous year (2008) was significantly smaller than the distance of active nests being used within the 2009 season (Wilcoxon test, Z = 2.201, P = 0.028). Discussion All 14 nests found in this study were in termite mounds, as found for the species in a previous study in central Brazil (Bianchi 2009) and none was found in tree cavities, as had been reported by Collar (1997). However, unlike other species of
parrot that nest in termitaria in the neotropics (e.g. Brightsmith 2000), Yellow-faced Parrots did not seem to choose active termitaria. It was not clear whether nesting in termite mounds is an effect of the landscape (Bianchi 2009), if Yellow-faced Parrots are actively selecting termite mounds in more open habitats in which to nest, or if they are using termitaria because there is a lack of appropriate tree cavities. Competition, predation, and other selective forces could have favoured the exploration of alternative substrates for nesting, such as termite mounds (Brightsmith 2005). Nesting cavities appeared to be abundant in the study area, with an average of 60% of available cavities unused each year. This is similar to the results of another study of a tropical psittaciform, in which only 43% of available cavities were used for breeding (Murphy et al. 2003). Although it is reasonable to suggest that open habitats with low availability of tree cavities might make termite mounds a key breeding resource (Redford 1984), the study site also had areas with many tree cavities that were not used by Yellow-faced Parrots. The number of suitable cavities, however, is probably lower than the total number available. Cavities selected by Yellowfaced Parrots differed from other cavities available in the area in depth of the cavity, and size and orientation of the entrance: used cavities were deeper, with a wider entrance and faced north-east. All these parameters have been found to be important in other parrot species (Heinsohn and Legge 2003; Rodríguez Castillo and Eberhard 2006). Clutch-size for the Yellow-faced Parrot in the study (1–3 eggs) was smaller than that reported elsewhere in Brazil (Bianchi 2009), in which clutch-sizes of 3–5 eggs was reported. The incubation and fledgling periods in the present study were also a little longer than previously reported (23–26 and 45–50 days respectively). The high hatching success (92%) was comparable to that of other parrots species (Masello and Quillfeldt 2002; Heinsohn and Legge 2003).
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The observed nesting success for the Yellow-faced Parrot is consistent with the overall average of 67% reported for neotropical species (Skutch 1985). In this study, 64% of Yellow-faced Parrot nests successfully produced fledglings, and unsuccessful nests (36%) were lost to predation during incubation. Interestingly, no cavities were seen to be reused by Parrots during the study period. This differed from other studies on closely related parrots, where reuse occurred, though the level of reuse varied, from 10% (Renton and Salinas-Melgoza 1999) to 74% (Rodríguez Castillo and Eberhard 2006). Higher rates of predation or ectoparasitic infestation may have a negative influence on cavity reoccupation (Mazgajski 2007). Consequently, high rates of cavity reuse are considered an indication of low levels of cavity availability (White et al. 2005), or at least low availability of appropriate cavities. Conversely, reuse of cavities may be associated with reproductive success in the previous year (Salinas-Melgoza et al. 2009). For the Yellow-faced Parrot, even the relatively high reproductive success did not increase the rate of cavity reoccupation in subsequent years. Given that the number of suitable cavities is probably much lower than the total reported here, it remains unclear why Yellow-faced Parrots do not reuse cavities. As most parrots are secondary cavity nesters, the distribution of their nests is almost never clustered, because their choice of nesting sites is limited by the distribution of available cavities. Active Yellow-faced Parrot cavities within a breeding season were recorded a mean distance of 2.38 km from the nearest active nest. However, this was a significantly greater distance than the nearest distance to a nest from the previous year (1.32 km). A similar result was observed in the Lilac-crowned Parrot (Amazona finschi), although this species appeared to nest within the same area each year (Salinas-Melgoza et al. 2009). For Yellow-faced Parrots, the distance to nests of the previous year was almost 10 times higher than that observed for Lilac-crowned Parrots, indicating that different pairs may be using the same area. Conclusions and future actions This study showed that the Yellow-faced Parrot, which is considered near threatened (BirdLife International 2010) has specific requirements for nesting and low site-fidelity to individual nestcavities, characteristics that could be problematic in a scenario of increasing loss and fragmentation of habitat. Outside protected areas, the Brazilian Cerrado has been subject to high rates of conversion, especially owing to agricultural development. Recent estimates suggest that almost 80% of the Cerrado has been modified by intensive human use (Myers et al. 2000). Yellow-faced Parrots also appear to be dependent on Campo Flickers for the excavation of cavities that they use for nesting. Consequently, conservation actions should include the protection of both species. Unfortunately, placement of nesting boxes does not seem to be effective in increasing the density of nesting pairs of Yellow-faced Parrots, although they were effective for another species of parrot in the same area, the Blue-fronted Parrot (Amazona aestiva). Other possible conservation actions include the use of artificial nests based on measurements of natural nests, and especially those simulating termite mounds. Although rates of nesting success appeared to be normal, the development of defence systems against predators during incubation could also
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help increase nesting success if the threats to these birds continues to increase. Acknowledgments I am grateful to Alexandre Dias for the revision of, and useful comments on, this manuscript. I thank all my field assistants, especially Débora Goedert. I also thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the scholarship received.
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Manuscript received 12 October 2010, accepted 10 December 2010
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