CHICK GROWTH AND BREEDING SUCCESS OF THE BURROWING PARROT

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1 The Condor 104: The Cooper Ornithological Society 2002 CHICK GROWTH AND BREEDING SUCCESS OF THE BURROWING PARROT JUAN F. MASELLO 1 AND PETRA QUILLFELDT Institut für Ökologie, Friedrich-Schiller-Universität Jena, Dornburgerstr. 159, D Jena, Germany Abstract. We present the first data on the breeding biology of wild Burrowing Parrots (Cyanoliseus patagonus). We studied chick growth and breeding success at the largest colony of the species in the province of Río Negro, Patagonia, Argentina, during the breeding season. A very high fledging success was observed and related to the absence of nest predation and the colonial breeding system. Safe nest sites were also thought to favor large mass recession of the nestlings before fledging. Mortality during the nestling period tended to be higher for fourth and fifth nestlings of a brood, indicating that brood reduction occurred. Burrowing Parrots in the study colony showed large variability in growth parameters between nestlings, possibly related to the hatching asynchrony observed. Allometric relationships for egg mass, clutch size, relative clutch mass, and nestling period of 29 wild psittaciform species are described and compared with the data from the Burrowing Parrots. Key words: breeding success, chick growth, Cyanoliseus patagonus, hatching order, mass recession, Patagonian Conure, Psittaciformes. Desarrollo de los Pichones y Éxito de Nidificación de Cyanoliseus patagonus Resumen. Presentamos aquí los primeros datos de la biología reproductiva en estado silvestre del loro Cyanoliseus patagonus. Se estudió el crecimiento de los pichones y el éxito de nidificación en la colonia más importante de la especie (provincia de Río Negro, Patagonia, Argentina) durante la temporada de cría Se observó un alto éxito de emplumamiento de los pichones relacionado a la ausencia de depredación en el nido y al sistema colonial de nidificación que presenta la especie. Los sitios de nidificación seguros habrían favorecido la pronunciada pérdida de masa corporal observada en los pichones antes de abandonar el nido. La mortalidad durante el período de nidificación tendió a ser más alta para el cuarto y quinto pichón de la nidada, indicando la existencia de reducción de la camada. Los loros de la colonia estudiada mostraron gran variabilidad en los parámetros de desarrollo de los distintos pichones, estando ésto posiblemente relacionado con el nacimiento asincrónico de los pichones. Se describen también relaciones alométricas para la masa del huevo, el tamaño de la nidada, la masa relativa de la nidada y el período de permanencia en el nido de 29 psittaciformes silvestres y se comparan con los datos de C. patagonus. INTRODUCTION Few studies of Psittaciformes (parrots and cockatoos) have been conducted in the wild, and these studies consider only 8% of the psittaciform species. Such a lack of information is of particular concern as parrots and cockatoos have become the most endangered order of birds in the world during the last few decades. Collar et al. (1994) showed that 26% of the 350 species of Psittaciformes are at risk of global extinction while another 11% are near threatened. This situation is even worse when the Neotropical parrots are considered alone: 31% of the Latin Manuscript received 27 February 2001; accepted 17 April Present address: G.-Keller-Weg 4, D Wogau, Germany. b8maju@excite.com American and Caribbean species are at serious risk of global extinction (Collar 1996). The principal sources of threat arise from loss, fragmentation or degradation of breeding habitat, collection of birds for the live trade, introduction of exotic species, and persecution and hunting. But some key features of their breeding biology also contribute to the fragility of the group: long lifespans, the commonly monogamous breeding system, the almost invariable habit of nesting in holes, and the absence of strong territoriality beyond the immediate vicinity of the nest, which contribute in several species, especially in the Neotropics, to colonial breeding systems. Some of the most important parrot research and conservation work is carried out in the Neotropics (Snyder et al. 2000). However, for many Neotropical parrot species there is still a lack of [574]

2 CHICK GROWTH AND BREEDING SUCCESS OF THE BURROWING PARROT 575 basic biological data, which are necessary for the identification of specific threats, the monitoring of populations, and the evaluation of the conservation measures taken. The Burrowing Parrot (Cyanoliseus patagonus) is one of the most southern Neotropical parrots. These parrots have long lifespans, their breeding system is socially and genetically monogamous (Masello et al. 2002), and they breed in big colonies, digging holes in high cliffs. Formerly, Burrowing Parrots were very common in Argentina, but now they are only regionally abundant. The species decline in parts of Argentina is due to increasing persecution as a crop pest, conversion of grasslands to croplands, and trapping for the increasing live bird trade (Bucher and Rinaldi 1986, Nores and Yzurieta 1994, Collar 1997, Juniper and Parr 1998). Burrowing Parrots are among the most frequently sold Psittacidae in Europe (Guix et al. 1997). In addition, some of their key breeding features, especially the habit of breeding in large and well-known colonies, can contribute to the species fragility and decline. Until now, the only available biological information on this species came from birds shot during control campaigns (Bucher et al. 1987), from semicaptive birds of the bloxami race in Chile (Beltrami et al. 1995), and from captive birds (de Grahl 1979, 1985, Rohbiller 1990, Jones 1992, Westen 1995). Information on the breeding of wild Burrowing Parrots is urgently needed for management of this species. Considerable variation in growth is common to many altricial bird species (Gebhardt-Henrich and Richner 1998). Environmental factors, internal factors, and hatching-rank effects, among others, can cause variation in growth. Burrowing Parrot nestlings hatch asynchronously, generating a size rank at the time of hatching that can amplify variations in final body size and cause differential survival. A detailed description of Burrowing Parrot chick growth would be of great value for planned projects of sustainable harvesting of the species. The aim of this study was to obtain detailed field data on the breeding biology of Burrowing Parrots, to describe variation in breeding success and chick growth within a wild population, and to provide a comparison with other members of the Psittaciformes. METHODS STUDY SPECIES AND SITE Burrowing Parrots are highly gregarious colonial birds that can form large flocks and roosts, sometimes in excess of 1000 birds. In Argentina, the species occurs from the Andean slopes in the northwest to the Patagonian steppes in the south (Darrieu 1980, Bucher and Rinaldi 1986). Burrowing Parrots generally inhabit open grassland, but are also reported from wooded valleys with cliffs and farmland to about 2000 m above sea level. The breeding birds arrive at the colonies 1 2 months before egg laying and leave the breeding site gradually as the young fledge. Southern populations then migrate to the north, sometimes reaching as far as Uruguay (Bucher and Rodríguez 1986). Burrowing Parrots excavate their own nest burrows by tunneling into the faces of sandstone, limestone, or earth cliffs (Leonardi and Oporto 1983). Nesting pairs use burrows that they have dug in previous seasons, but they enlarge the burrows every year (Masello et al. 2002). Each burrow is occupied by a single pair. Burrowing Parrots do not use nesting material but, rather, deposit their eggs on the sandy bottom of the nest chamber (Masello et al. 2001). Burrowing Parrots lay one clutch per season. The female incubates the eggs for about 24 days (de Grahl 1985) while the male provides food (D. Clarke, pers. comm.). They have a socially and genetically monogamous breeding system with intensive biparental care (Masello et al. 2002). The sexes share in chick feeding. The nestlings remain in the nest for about 60 days (Masello et al. 2002). After fledging, the young are fed by the adults for approximately four months (Westen 1995). The study was carried out between October 1999 and February 2000 at El Cóndor, the largest breeding colony of Burrowing Parrots in the province of Río Negro, Patagonia, Argentina. The colony is located on a sandstone cliff, extending for 5 to 10 km (Yorio and Harris 1997), but a 1-km stretch (41 3 S, W) is by far the densest with 6750 active nests (JFM, unpubl. data). In the densest sector of the colony, 79 nests were selected and monitored every 5 days as part of an ongoing study of the breeding behavior of the species. A subset of 29 nests was selected for the chick growth study and inspected every 5 days by climbing the cliff face. When

3 576 JUAN F. MASELLO AND PETRA QUILLFELDT an adult was present in a nest, it was captured and weighed to the nearest 1 g using a digital balance. Burrowing Parrots tend to desert in response to disturbance during the incubation period and during the first week after hatching (de Grahl 1985, Masello et al. 2002). In order to reduce observer influence, nests were not disturbed until about 5 days after the estimated hatching date of the last chick of a clutch. Clutch size was determined by visual inspection of the nests using a flashlight, and without capturing the adults. At the time of the first measurement, when nestlings were still clearly different sizes, the hatching rank was determined, and nestlings were individually marked. Nestlings lighter than 100 g were first marked with nail enamel on their claws. When the nestlings reached 100 g, they were banded with numbered steel bands. BREEDING PARAMETERS The following parameters of breeding success were recorded: (1) clutch size, the number of eggs laid per nest; (2) relative clutch mass, the total clutch mass as percentage of the adult body mass; (3) hatching success, the percentage of eggs laid that hatched; (4) fledging success, the percentage of hatchlings that fledged; (5) successful attempts, the percentage of nests with at least one fledged chick. The breeding parameters of Burrowing Parrots were compared with all available data for wild parrots. This comparison included 29 psittaciform species from all over the world. Only studies of more than four nests per species were included. GROWTH PARAMETERS Five growth parameters were recorded each time the nest was inspected during the eight weeks of chick development. (1) Body mass, using a digital balance to the nearest 1 g; (2) tarsus length and (3) bill length, using calipers to the nearest 0.1 mm; (4) wing length, the distance from the anterior surface of the radiocarpal joint to the tip of the longest primary, using a wing rule to the nearest 1 mm; and (5) length of the medial tail feather using a feather rule to the nearest 1 mm. Prefledging measurements were taken the last time the nestlings were found in the nests (i.e., 1 4 days before fledging), but only nestlings older than 55 days were included in the analyses. FIGURE 1. Growth curve for the bill length of Burrowing Parrot nestlings during the breeding season in Río Negro, Patagonia, Argentina. Individual wing and tail growth rates of nestlings were determined for the linear phase of the growth curves. The beginning and end of the approximately linear phase of both wing growth and tail growth were defined in terms of wing and tail length. For each chick, growth rates were calculated using the time elapsed between these measurements. Tarsus growth rate could not be determined because most of its linear growth phase occurs during the first 10 days after hatching. Observations were avoided during these 10 days due to the possibility of adult nest abandonment. The ages of nestlings whose hatching dates were not known were calculated from a growth curve for the bill length of known-age nestlings (Fig. 1, y /(1 (29.0/x) 1.1 ), r 0.99, F 3, , P 0.001). STATISTICAL ANALYSES All analyses of chick growth included only nestlings that survived to fledging. Chick growth data were fitted to models using the SigmaPlot 4.00 nonlinear regression procedure (Jandel Scientific 1997). One-way repeated measures ANO- VA was carried out in order to analyze how growth is influenced by hatching order in a brood. Nestlings were classed in three categories: first, middle, and last hatched for this analysis, and to allow comparisons between broods of different sizes. Data were analyzed using Sigma Stat 2.03 (Jandel Scientific 1995) and SPSS 10.0 (SPSS Inc. 1999). All means are given SE. The significance level used is P 0.05.

4 CHICK GROWTH AND BREEDING SUCCESS OF THE BURROWING PARROT 577 FIGURE 3. Survival to fledging of Burrowing Parrot nestlings according to the hatching order of the nestlings during the breeding season in Río Negro, Patagonia, Argentina. Numbers above each bar are sample sizes (nestlings). FIGURE 2. Percentage of 29 Burrowing Parrot nests with one, two, three, four, or five eggs, nestlings and fledglings during the breeding season in Río Negro, Patagonia, Argentina. Numbers above each bar are sample sizes (nests). RESULTS BREEDING SUCCESS Of 79 nests, 67 (85%) contained eggs, four (5%) collapsed during the breeding season, and the remaining eight (10%) were empty. In 11 marked nests with eggs, we abandoned observation of the nestlings because they moved into inaccessible parts of the nest. Of 56 nests with eggs that we could inspect over the breeding season, three (5%) were abandoned during the incubation period and three (5%) were abandoned after hatching. In the subset of 29 monitored nests, the mean number of eggs laid per nest (clutch size) was (range 2 to 5, n 29 nests, Fig. 2). The nestlings hatched asynchronously with an interval of 2 days between nestlings. From 110 eggs laid in 29 nests, 99 (90%) nestlings hatched, a mean of nestlings per nest (range 1 to 5, Fig. 2). In most of the nests all eggs hatched (72% of nests), but in some nests one egg (21%), two eggs (4%) or three eggs (3%) failed to hatch. The mean hatching date of the first nestlings of a clutch was 8 November (range 25 October to 25 November). A total of 91% of the hatched nestlings survived to fledging. The mean number of juveniles fledged per breeding pair was (range 0to5,n 29 breeding pairs, Fig. 2). Nestling survival was affected by the hatching order. Mortality during the nestling period tended to be higher for fourth and fifth-hatching nestlings in a clutch (Fig. 3). Nestlings at the study colony fledged between 30 December and 23 January at a mean age of days (range 53 to 68 days, n 88 nestlings). Nestlings from a brood fledged asynchronously, with an interval of 2 3 days be-

5 578 JUAN F. MASELLO AND PETRA QUILLFELDT TABLE 1. Variation in chick growth of Burrowing Parrots in Río Negro, Patagonia, Argentina, during the breeding season Growth parameter Peak mass (g) Age at peak mass (days) Mass loss (%) Prefledging mass (g) b Prefledging wing length (mm) b Prefledging tarsus length (mm) b Prefledging bill length (mm) b Prefledging tail length (mm) b Age at tarsus length of 25 mm (days) Age at wing length of 50 mm (days) Age at wing length of 180 mm (days) Wing growth (mm day 1 ) c Age at tail length of 50 mm (days) Age at tail length of 150 mm (days) Tail growth (mm day 1 ) c Mean SE Range Min. Max. n a a Number of chicks for which the parameter could be measured or calculated. b Last measurement: one to four days before fledging. c Determined for the approximately linear phase of the growth curves tween nestlings (Masello and Quillfeldt, unpubl. data). CHICK GROWTH Body mass increased rapidly to a mean peak mass of g (Table 1). This value was reached at a mean age of 38 days, and equals 119% of the average adult body mass of g (range to g, n 120) for birds captured in the studied colony. Mass growth was described by a quadratic regression (Fig. 4, y x 0.2x 2, r 0.77, F 2, , P 0.001). The mean mass loss from the peak mass to fledging was 23% (Table 1). Nestlings fledged at a mean mass of g (Table 1). Tarsus growth followed a logistic growth pattern (Fig. 4, y /(1 (11.6/x) 6.2 ), r 0.82, F 3, , P 0.001). The nestlings reached a mean prefledging tarsus length of 29.7 mm (Table 1), which was similar to the tarsus length of adults (Mann-Whitney U 1231, P 0.9). Wing growth was well described by a logistic regression (Fig. 4, y /(1 (36.1/x) 2.3 ), r 0.97, F 3, , P 0.001). Wing growth continued after fledging, such that no asymptotic values could be determined. The mean prefledging wing length of the nestlings was mm (Table 1), which equals 92% of the average adult wing length of g (range to g, n 121) for birds captured in the studied colony. Tail growth also followed a logistic growth pattern (Fig. 4, y /(1 (50.1/ x) 2.2 ), r 0.97, F 3, , P 0.001), and also continued after fledging, such that no asymptotic values could be determined. The mean prefledging tail length of nestlings was mm (Table 1), which equals 72% of the average adult tail length of g (range to g, n 119) for birds captured in the studied colony. Individual wing and tail growth rates of nestlings were determined during the approximately linear phase of the growth curves. The mean wing growth rate was 4.8 mm day 1 and the mean tail growth was 4.0 mm day 1 (Table 1). These approximately linear phases were found between 50 and 180 mm for wing growth and between 50 and 150 mm for tail growth. The linear phase of wing growth started at a mean age of 15 days and finished at a mean age of 42 days, while on average, nestlings started linear tail growth at the age of 25 days, and finished at 50 days (Table 1). INFLUENCE OF HATCHING ORDER ON CHICK GROWTH Some growth parameters of the Burrowing Parrot nestlings were influenced by hatching order. The mean peak mass was g(n

6 CHICK GROWTH AND BREEDING SUCCESS OF THE BURROWING PARROT 579 FIGURE 4. Growth curves of 87 nestling Burrowing Parrots during the breeding season in Río Negro, Patagonia, Argentina. 16) for first-hatched nestlings, g(n 17) for middle-hatched nestlings, and g(n 16) for last-hatched nestlings (repeated measures ANOVA, F 2,30 5.5, P 0.01; Tukey post-hoc test: first vs. last, P 0.01). Last-hatched nestlings reached peak mass at 44 days old, which was significantly later than first and middle-hatched (F 2, , P 0.001; first vs. last, P 0.01, middle vs. last, P 0.001). The last chick of a brood also was lighter prior to fledging than its first-hatched sibling: g vs g(F 2,18 3.7, P 0.05; first vs. last, P 0.05). First-hatched nestlings fledged with longer wings than their siblings (F 2,18 3.7, P 0.02; first vs. last, P 0.02, first vs. middle, P 0.04). First-hatched nestlings reached a wing length of mm (n 13) while middle and last-hatched nestlings reached mm (n 11) and mm (n 13) respectively. First-hatched nestlings reached a tarsus length of mm (n 15), which was longer than the mm (n 18) reached by last-hatched nestlings (F 2,31 6.3, P 0.01; first vs. last, P 0.01). The remaining growth parameters (Table 1) were not statistically significantly influenced by hatching order. ALLOMETRIC RELATIONSHIPS In order to evaluate the data for Burrowing Parrots we reanalyzed the presently available breeding data for wild psittaciform species and compared our data to it (Table 2). As described for Australian Psittaciformes (37 species, Saunders et al. 1984), we found a positive linear relationship between egg mass and body mass of adult parrots (Fig. 5a, y x, r 0.92, P 0.05), as well as between nestling period and body mass of adult parrots (Fig. 6a, y x, r 0.86, P 0.05). Saunders et al. (1984) mentioned for an average Australian parrot species of 400 g an average nestling period of 58 days and an egg mass of 19.9 g. In our analysis of the world s parrots we found the same average nestling period (58 days) as Saunders predicted from Australian data for a 400-g parrot species. Our prediction of the average egg mass (17.3 g) is lower than that mentioned in Saunders et al. (1984) but similar to the value given by Rahn et al. (1975).

7 580 JUAN F. MASELLO AND PETRA QUILLFELDT TABLE 2. Breeding parameters of Psittaciformes in the wild, reported in the literature. Studies with n 4 were not considered. Results are statistical means except when authors reported ranges, in which case we used the median. When authors did not give body mass, values from Dunning (1993) or Collar (1997) were adopted. In dimorphic species female body mass was used. Relative clutch mass is the total clutch mass as a percentage of adult body mass. Hatching success is the percentage of eggs laid that hatched. Fledging success is the percentage of hatchlings that fledged. Successful attempts is the percentage of nests in which at least one chick fledged. Nomenclature follows Juniper and Parr Species White-tailed Black-Cockatoo Calyptorhynchus latirostris Yellow-tailed Black-Cockatoo Calyptorhynchus f. funereus C. funereus xanthanotus Red-tailed Black-Cockatoo Calyptorhynchus banksii Glossy Black-Cockatoo Calyptorhynchus lathami Galah Eolophus r. roseicapillus E. roseicapillus assimilis E. roseicapillus kuhli Pink Cockatoo Cacatua leadbeateri Little Corella Cacatua sanguinea Western Corella Cacatua pastinator Body mass (g) Egg mass (g) Nestling period (days) Clutch size Relative clutch mass (%) Hatching success (%) Fledging success (%) Juveniles fledged per breeding pair Successful attempts (%) References Saunders Saunders et al Saunders et al Saunders et al. 1984, Smith and Saunders Garnett et al Rowley 1990 Saunders et al Saunders et al Rowley and Chapman Smith and Saunders Saunders et al. 1984, Smith and Saunders 1986, Smith 1991 Long-billed Corella Saunders 1997, Cacatua tenuirostris Saunders and Smith 1981 Kea Jackson 1963, Nestor notabilis Diamond and Bond Moorhouse 1991 Kaka Nestor meridionalis Red-shining Parrot Prosopeia tabuensis Crimson Rosella a Platycercus elegans Red-fronted Parakeet Cyanoramphus novaezelandiae b Rinke Saunders et al. 1984, Krebs 1998, Krebs et al Taylor 1985, Robinet and Salas 1999

8 CHICK GROWTH AND BREEDING SUCCESS OF THE BURROWING PARROT 581 TABLE 2. Continued. Species Ouvea Parakeet Eunymphicus cornutus Kakapo Strigops habroptilus Blue-and-yellow Macaw Ara ararauna Scarlet Macaw Ara macao Red-and-green Macaw Ara chloroptera Pacific Parakeet Aratinga strenua Thick-billed Parrot Rhynchopsitta pachyrhyncha Burrowing Parrot Cyanoliseus patagonus Monk Parakeet Myiopsitta monachus Green-rumped Parrotlet a Forpus passerinus Canary-winged Parakeet Brotogeris versicolorus Bahama Parrot Amazona leucocephala Puerto Rican Parrot Amazona vittata Green-cheeked Amazon Amazona viridigenalis Yellow-cheeked Amazon Amazona autumnalis Yellow-headed Amazon Amazona oratrix Body mass (g) Egg mass (g) Nestling period (days) Clutch size Relative clutch mass (%) Hatching success (%) Fledging success (%) Juveniles fledged per breeding pair Successful attempts (%) References Robinet and Salas b 100 c 3 9 Powlesland et al Munn Munn Munn Wermundsen Lanning and Shiflett 1983, Enkerlin-Hoeflich et al This study Navarro and Bucher 1990, Navarro et al Beissinger and Waltman 1991, Waltman and Beissinger Paranhos and Marcondes-Machado Gnam 1991, Gnam and Rockwell Snyder et al Enkerlin-Hoeflich Enkerlin-Hoeflich Enkerlin-Hoeflich 1995 a Studies conducted on birds breeding in nestboxes. b Estimated according to Hoyt c Nestling period includes period in nest and in immediate surroundings.

9 582 JUAN F. MASELLO AND PETRA QUILLFELDT In accordance with the findings of Saunders et al. (1984) we found an inverse relationship between clutch size and body mass. This relationship was described by an exponential regression (Fig. 5b, y e 0.006x, r 0.86, F 2, , P 0.001). We also considered the total clutch mass as a percentage of body mass. The relationship between adult body mass and relative clutch mass was also well described by an exponential regression (Fig. 5c, y x, r 0.99, F 2, , P 0.001). The exponential relationship found between nestling period and relative clutch mass is shown in Fig. 6b (y e 0.057x, r 0.85, F 2, , P 0.001). Burrowing parrots had an average egg mass of 13 g, which was very close to the expected value from the linear regression (Fig. 5a). The average nestling period of 63 days observed in Burrowing Parrots in El Cóndor was 11 days longer than expected from the linear regression (Fig. 6a). The exponential regression between the nestling period and relative clutch mass also indicated that Burrowing Parrot nestlings have a longer nestling period than expected (Fig. 6b). Observed clutch size was very close to that expected from the exponential regression for clutch size and body mass (Fig. 5b). The relative clutch mass observed (Table 2) was equal to the value predicted by the exponential regression for relative clutch mass and body mass (Fig. 5c). DISCUSSION This study describes for the first time parameters of breeding success and chick growth of Burrowing Parrots in the wild. We found very high fledging success, differential mortality of nestlings related to hatching order, large variability in growth parameters between nestlings, and large mass recession of the nestlings before fledging. FIGURE 5. Relationships between (a) egg mass, (b) clutch size, and (c) relative clutch size, and the average adult body mass of wild Psittaciformes. Data for Burrowing Parrots are marked by a triangle. FLEDGING SUCCESS The breeding success recorded here for Burrowing Parrots is the highest so far recorded for parrots in the wild. Parrots commonly lose many nestlings through predation (e.g., Navarro and Bucher 1990, Enkerlin-Hoeflich 1995, Garnett et al. 1999); therefore the high fledging success of Burrowing Parrots observed in this study could be due to the absence of predation. The colony is located in an unstable cliff, and the nests are located between 4 and 17 m high; thus access for predatory mammals and reptiles is very difficult. In addition, the high density of parrots in the part of the colony we studied may repel potential avian predators such as Barn Owls (Tyto alba), Chimango Caracaras (Milvago chimango), and American Kestrels (Falco sparverius), which occur in the vicinity. Studies on the evolution of coloniality have focused mainly on two hypotheses, that colonial living reduces predation and that it improves food-finding (Wittenberger and Hunt 1985). However, the factors in-

10 CHICK GROWTH AND BREEDING SUCCESS OF THE BURROWING PARROT 583 fluencing coloniality vary from species to species and no general hypothesis has so far been validated (Rolland et al. 1998). However, the high fledging success observed in this study does not necessarily imply high reproductive success. Nestlings are not independent at fledging, but are fed for a further four months by their parents (Westen 1995). Juvenile mortality could not be measured in this study, but generally appears to be high in psittaciform birds (Robinet and Salas 1999). After fledging, many carcasses of depredated nestlings were found in areas surrounding the colony, and many nestlings were killed by cars on a nearby road, indicating a high juvenile mortality in Burrowing Parrots. Moreover, years with inclement weather could lead to lower fledging success than that observed during the breeding season Although no cases of predation at the nest were detected and, thus, nestling mortality was low, three nests were abandoned and all the nestlings of these broods died. This could be due to adult mortality during the breeding season. Local farmers shoot parrots during the breeding season on their private land, supposedly to protect crops. In addition, some local farmers also poison grain in order to kill birds, and some tourists shoot parrots during the holiday season for entertainment (Bucher and Rinaldi 1986, JFM, pers. obs.). Furthermore, on at least one occasion a breeding bird banded for our project was captured for the pet trade and sold to Spain (R. Cardon, pers. comm.). Nestling survival was also affected by the hatching order of the nestlings in a brood. Mortality during the nestling period tended to be higher for fourth and fifth nestlings of a brood, indicating that brood reduction occurs in Burrowing Parrots as in other psittaciform species (Smith 1991, Beissinger and Waltman 1991, Stoleson and Beissinger 1997, Krebs 1999, Robinet and Salas 1999). FIGURE 6. Relationships between nestling period and (a) average adult body mass and (b) relative clutch mass for wild Psittaciformes. Data for Burrowing Parrots are marked by a triangle. VARIABILITY IN CHICK GROWTH Patterns of avian growth are often highly variable within species and populations. Food availability (quantity or quality) or delivery rates may constrain chick development (Lack 1968). Growth rates of individual nestlings could thus reflect both environmental and parental quality (Gebhardt-Henrich and Richner 1998) and may be highly variable in years of abundant food (Boersma and Parrish 1998). Burrowing Parrots in the study colony showed enormous variability in growth parameters. We assume that food availability in the breeding season was normal because precipitation during 1999 was close to average for the region compared with precipitation data for the past 30 years (Servicio Meteorológico Nacional- Argentina, unpubl. data). The present data suggest that first-hatched nestlings of a brood received more food than middle and last-hatched nestlings, and that these differences in food delivery rate were responsible for some variation in growth. A similar pattern has been found for other psittaciform species (Rowley and Chapman 1991, Smith 1991, Stoleson and Beissinger 1997). With the present data, from only one breeding season, we could not examine the environmental component of growth. Future analyses should examine differences in growth rates under different environmental conditions, for example across several breeding seasons, as well

11 584 JUAN F. MASELLO AND PETRA QUILLFELDT as individual differences in food delivery among pairs. MASS RECESSION The phenomenon of mass recession in nestlings prior to fledging has previously been described primarily for oceanic species, swallows, and swifts (Ricklefs 1968). Mass recession in Psittaciformes can be observed in the growth curves of several cockatoos (Saunders 1977, 1982, 1986, Smith 1991), in the Monk Parakeet (Myiopsitta monachus, Navarro and Bucher 1990, Aramburú 1997), in the Green-cheeked Amazon (Amazona viridigenalis, Enkerlin-Hoeflich 1995), and in the Thick-billed Parrot (Rhynchopsitta pachyrhyncha, Enkerlin-Hoeflich et al. 1999) but the topic has not been discussed by these authors. We found large mass recession in Burrowing Parrots. Mass recession has been attributed to several causes, such as drying out of the feathers, the high energy demands of rapid feather growth, starvation periods, and decrease in the size of digestive organs (Ricklefs 1968). Recently, Morbey et al. (1999) rejected the former hypotheses of mass recession for Cassin s Auklets (Ptychoramphus aleuticus), and suggested instead that parental provisioning behavior and nestling departure decisions interact to cause prefledging mass recession. In their model, irregular provisioning and nest safety were two important features contributing to the evolution of mass recession. Burrowing Parrot nestlings remained in the nest 11 days longer than expected from the allometric relationships found for Psittaciformes. Nest safety was high in the present study, suggesting that remaining in the nest did not pose additional predation risk to the nestlings, but contributed to the magnitude of mass recession observed during this study. Further work is required in order to obtain a more complete understanding of the high fledging success observed in and its relation to the colonial breeding system of Burrowing Parrots. Long-term studies would be desirable to better understand the influence of temporal changes in environmental conditions on reproductive success. To better understand chick growth variation it would be necessary to examine differences in growth rates under different environmental conditions as well as individual differences in food delivery between pairs. ACKNOWLEDGMENTS We wish to thank Adrián Pagnossin, María Luján Pagnossin and Mara Marchesan for assistance with fieldwork, Dr. Roger Mundry for statistical advice, Dr. John Sloggett for checking the English of the manuscript, the Servicio Meteorológico Nacional (Buenos Aires, Argentina) for providing the precipitation data and two anonymous referees for useful comments on the manuscript. This project was supported partially by the City Council of Viedma (Río Negro, Argentina), and a grant of the state of Thuringia, Germany (Landesgraduiertenstipendium). The present study was carried out under permission of the Dirección de Fauna de la Provincia de Río Negro, Argentina (Exp. no DF-98). LITERATURE CITED ARAMBURÚ, R. M Descripción y desarrollo del pichón de la cotorra Myiopsitta monachus monachus (Aves: Psittacidae) en una población silvestre de Argentina. Revista Chilena de Historia Natural 70: BEISSINGER, S. R., AND J. R. WALTMAN Extraordinary clutch size and hatching asynchrony of a Neotropical parrot. Auk 108: BELTRAMI, M., J. NARANJO, C. SARMIENTO, L. ULLOA, L. ALFARO, AND P. OLGUIN Reproductive behaviour of Cyanoliseus patagonus byroni in semi-captive conditions. Boletín del Museo Nacional de Historia Natural Chile 45: BOERSMA, P. D., AND J. K. PARRISH Flexible growth rates in Fork-tailed Storm-Petrels: response to environmental variability. Auk 115: BUCHER, E. H., M. A. BERTIN, AND A. B. SANTAMARIA Reproduction and molt in the Burrowing Parrot. Wilson Bulletin 99: BUCHER, E. H., AND S. RINALDI Distribución y situación actual del loro barranquero (Cyanoliseus patagonus) en la Argentina. Vida Silvestre Neotropical 1: BUCHER, E. H., AND E. N. RODRíGUEZ Sobre la presencia del loro barranquero (Cyanoliseus patagonus) en el Uruguay. Hornero 12: COLLAR, N. J Priorities for parrot conservation in the New World. Cotinga 5: COLLAR, N. J Family Psittacidae (Parrots), p In J. del Hoyo, A. Elliot, and J. Sargatal [EDS.], Handbook of the birds of the world. Vol. 4. Sandgrouse to Cuckoos. Lynx Edicions, Barcelona. COLLAR, N. J., M. J. CROSBY, AND A. J. STATTERSFIELD Birds to watch 2: the world list of threatened birds. BirdLife International, Cambridge, UK. DARRIEU, C. A Las razas geográficas de Cyanoliseus patagonus (Aves: Psittacidae). Neotrópica 26: DE GRAHL, W Zucht des kleinen Felsensittichs (Cyanoliseus p. patagonus). Gefiederte Welt 103: DE GRAHL, W Papageien: Lebenweise, Arten, Zucht. Eugen Ulmer, Stuttgart, Germany.

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