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Food resources and reproductive output of the Austral Parakeet
(Enicognathus ferrugineus) in forests of northern Patagonia
Soledad Díaz
A,C
, Thomas Kitzberger
A
and Salvador Peris
B
A
INIBIOMA-CONICET and Laboratorio Ecotono, CRUB, Universidad Nacional del Comahue, Quintral 1250,
(8400) Bariloche, Río Negro, Argentina.
B
Departamento de Zoología, Facultad de Biología, Universidad de Salamanca, 37071 Salamanca, Spain.
C
Corresponding author. Present address: 256 Cactus Court, Boulder, CO 80304, USA. Email: jisdiaz@gmail.com;
jisdiaz@yahoo.com.ar
Abstract. Assessing use of resources across resource gradients and over time is necessary for determining factors that
influence the natural distribution of birds. We analysed the pattern of availability of food resources, the use of food resources
and the influence of food availability on reproduction and demography for the Austral Parakeet (Enicognathus ferrugineus)
in two southern temperate forests of Argentine Patagonia. The abundance of Austral Parakeets in Nothofagus pumilio
forests co-dominated by Araucaria araucana was generally higher and fluctuated more than abundance of populations
in monospecificN. pumilio forest. This appears to be related to A. araucana providing a larger but more variable food
resource. Austral Parakeets responded quickly to changing availability of resources by modifying their diet if alternative
food resources were available, and reproductive success also increased when seed availability was high. We found mixed
forests to be a unique and important habitat for Austral Parakeets in the northern part of their range, and conservation
management should recognise this special role that mixed N. pumilio–A. araucana forests play in Austral Parakeet ecology.
Additional keywords: Araucaria araucana, habitat use, Nothofagus pumilio, pollen, seed, psitacid, southern temperate
forest.
Received 23 September 2011, accepted 20 April 2012, published online 21 August 2012
Introduction
The availability of food affects avian reproduction by influencing
the timing of breeding initiation, clutch-sizes and nestling sur-
vival, and thus, ultimately, has an effect on vital demographic
rates and population trends (Lack 1966; Martin 1987; Hutto 1990;
Newton 1998; Ferretti et al.2005; Salafsky et al.2007; Verhulst
and Nilsson 2008). Foraging theory predicts that populations of
a species with greater access to food may have greater overall
breeding success than populations in poorer environments
(in terms of quantity or quality of food) (Stephens and Krebs
1989). For example, intra- and inter-annual variation in the
availability of food can affect female nutritional condition and
the onset of breeding, which in turn can have both direct and
indirect effects on the survival of nestlings (Newton 1998;
Salafsky et al.2007; Verhulst and Nilsson 2008; Zárybnická
2009). Furthermore, spatial variation in the availability of food
may affect variation in the breeding success of individuals and
defensive behaviour of breeding pairs, as well as overall popu-
lation growth and density (Newton 1998; Fontaine et al.2009).
Very few studies have considered the influence of temporal
and spatial variation in the availability of food on the reproduction
of neotropical parrots (Psittaciformes) but those that do have
shown an important influence of food supply on the growth and
survival of nestlings (Renton 2002; Masello and Quillfeldt 2003,
2004;Renton and Salinas-Melgoza 2004;Sanz and Rodríguez-
Ferraro 2006). Understanding the influence of environmental
factors on breeding success and population vulnerability to
environmental change is urgently needed for the management
and conservation of Neotropical parrots. The relationship be-
tween inter-annual variation in environmental conditions and
availability of food are particularly important for psittacid species
in temperate regions where marked seasonal variations limit
resource availability and affect parental condition (Masello and
Quillfeldt 2003) and, thus, reproductive parameters, breeding
success and population size.
The Austral Parakeet (Enicognathus ferrugineus) has the most
southerly distribution of any psittacid, being restricted to the
southern temperate forests of Andean Patagonia (36–54S) (For-
shaw 2010). Its distribution coincides with the distribution of
Nothofagus forests (Veblen et al.1996) and, in the northern part of
its range, with the distribution of Araucaria araucana forests
(Gonzalez et al.2006). Both Nothofagus pumilio and A. araucana
have strong masting patterns of seed production (Gonzalez et al.
2006; Heinemann 2007; Sanguinetti and Kitzberger 2008), de-
fined as the intermittent and synchronous production of large
seed crops by individuals in populations of long-lived plants
(Kelly 1994). Yet the cycles between N. pumilio and A. araucana
are not synchronised and vary in length (Gonzalez et al.2006;
CSIRO PUBLISHING
Emu,2012, 112, 234–243
http://dx.doi.org/10.1071/MU12005
Journal compilation BirdLife Australia 2012 www.publish.csiro.au/journals/emu
Heinemann 2007) thereby producing cyclical pulses of food
resources at inter-annual to decadal time-scales that are especially
important to granivores (Ostfeld and Keesing 2000; Schnurr et al.
2002; Areta et al.2009). The Austral Parakeet is granivorous and
depends on flowers and seeds of N. pumilio growing in mono-
specific forests (Díaz and Kitzberger 2006), with almost 100% of
its breeding season diet composed of food derived from
N. pumilio. There are also anecdotal reports of Austral Parakeets
feeding on A. araucana seeds (Gonzalez et al.2006; Sanguinetti
and Kitzberger 2008).
In this paper, we present data on the breeding biology of
the Austral Parakeet in mixed N. pumilio–A. araucana forest
and forests dominated solely by N. pumilio (monospecific
N. pumilio forests), and we analyse the relationship between
reproductive parameters and fluctuations in the availability of
food. By assessing seasonal use of resources in these two forests
we sought to clarify how Austral Parakeets use resources
throughout their range and how they respond to variation in the
availability of food owing to the masting cycles of their food
plants. The main objectives of our study were to determine a
range of reproductive parameters and the relative abundance
of Austral Parakeets, to identify yearly fluctuations in these
parameters, and to identify dietary factors that may be
responsible for any variation observed. We hypothesised that
the reproductive performance and relative abundance of Austral
Parakeets would be highly influenced by tree-species of the
forests they inhabit and the differential patterns of food
available in each of these southern temperate forest types. We
predicted different foraging strategies in populations of Austral
Parakeets in mixed N. pumilio–A. araucana forests compared
to populations in monospecificN. pumilio forests owing to
differences in the diversity, quality and year-round availability
of food. Compared to monospecific forests, we expected that
mixed forests would provide a more stable food source owing
to the non-synchronicty of food resources on inter-annual (due
to masting) and intra-annual (differential phenology) time-
scales. In turn, we predict higher hatching rates and reproductive
success of Austral Parakeets in mixed forests than in monospe-
cific forests.
Methods
Study area and study species
This study was conducted in two representative forests of north-
western Patagonia, Argentina, ~180 km apart, between 2007 and
2010:
*A monospecific forest of N. pumilio (200 ha) in Challhuaco
Valley in the Rio Negro Province (41150S, 71160W). The
elevation of this forest ranges from 1000 to 1400 m above sea
level (asl), with a transition from lowland shrubbe-steppe in
the east to N. pumilio forest in the west. The understory of the
forest consists of the herb Alstroemeria aurea and the low
shrubs Ribes magellanicum and Berberis serrato-dentata.
*A mixed forest of N. pumilio and A. araucana (168 ha) in the
Tromen area in Neuquén Province (39350S71
250W, 1050 m
asl). This forest is fairly flat, with no altitudinal gradient, and the
understorey is dominated by the herb Alstroemeria aurea and
shrub Ribes magellanicum.
Both forests have been affected and shaped by fire events,
although Challhuaco has been more affected by uncontrolled
logging. Climate is similar at both sites, with marked seasons,
consisting of dry summers (December–March) with average
daily temperatures of 17–19C, and periods of intensive rain and
snow between late autumn and early spring (April–September),
with average daily temperatures of 7–8C. Annual mean precip-
itation is 1300–1800 mm in the Challhuaco Valley (Paruelo et al.
1998, Barros et al.1983) and 2000–3500 mm in the Tromen area
(Autoridad Interjurisdiccional de Cuencas, Malalco Meteorolog-
ical Station, data available by request).
Austral Parakeets nest only in tree-cavities, mainly in Notho-
fagus species. Breeding occurs once per year, between December
and March, and the start of nesting is highly synchronised
between nesting pairs living in the same forest. Broods are of
5–8 young, sometimes as many as 11, and both parents help raise
the young (Díaz, in press). Broods are large compared with those
of other Neotropical Psittacidae (Masello and Quillfeldt 2002;
Renton and Salinas-Melgoza 2004; Brightsmith 2005).
Phenology of food items
Over the 3 years 2007–10 we monitored all types of food both
potentially available and seen to be eaten by Austral Parakeets at
both sites. To assess availability of food (i.e. relative abundance of
potentially consumable food types) we recorded the phenological
state of foliage and reproductive structures of all food-types
consumed by Parakeets. In each study site, plant phenology was
assessed monthly along 300 m-long transects located within the
forest, and a minimum of 50 m from roads and trails to avoid the
presence of edge species. In the N. pumilio forest, we sampled
along 18 transects placed every 60 m, orientated perpendicular to
the altitudinal gradient. In the mixed forest, where no altitudinal
gradient was evident, we sampled along 20 randomly placed
transects. Along each transect, ten 10 10-m plots were placed at
20-m intervals starting at 10 m (n= 10 plots per transect). Within
each plot, we visually assessed the number of all trees, shrubs,
herbs and hemiparasitic plants that may be food for Austral
Parakeets. Each transect was considered one sampling unit, so
the value of each transect was recorded as the average of all
plots along the transect. To record phenological stage, monthly
surveys of presence of flowers and fruit were conducted using
binoculars (Zeiss 8 30 Conquest T*, Germany) for all species
present within transect plots. Fruits and seeds were included in the
analysis once they were ripe enough to be eaten, indicated by
colour and size (depending on species), following previous
observations of Parakeets feeding on them (S. Díaz, pers. obs.).
Only reproductively mature trees of N. pumilio and A. araucana
were recorded. Mature trees were defined as those with a diameter
at breast height (DBH) >20 cm, and taller than 5 m for
A. araucana (Sanguinetti and Kitzberger 2008; S. Díaz, pers.
obs.).
Flower and seed production
During the study period and in both study sites, seeds and male
flowers of N. pumilio were quantified once mature. Nothofagus
pumilio is monoecious, so male and female flowers were counted
on the same plants in October and February respectively between
2007 and 2010. A single branch 30 cm long was cut from 20
The diet of Austral Parakeets in Patagonia Emu 235
N. pumilio trees to count the number of flowers and seeds
(40 branches total); trees were randomly selected and were not
from the phenological transects. A. aruacana is dioecious. Pollen
cones of A. araucaria were counted when mature in November,
between 2007 and 2010. Data on production of A. araucana seed
cones were obtained for a broader range of years, from 2005 to
2010, and were counted during January. A. araucana reproduc-
tive structures were counted (using 8 30 binoculars, as above)
on 72 randomly selected trees of each sex. The total number of
cones per tree was estimated by counting at least half of the entire
tree, depending on the amount of visible crown, and then mul-
tiplying the number of counted cones by the percentage measured
to estimate the uncounted cones. The study period included
one marked A. araucana masting year (2007) and two non-
masting years.
To determine annual pollen production, pollen was collected
from 100 male N. pumilio flowers from 10 different N. pumilio
trees and 20 male A. araucana cones from 20 different
A. araucana trees (all randomly selected). Pollen from each
flower or cone was weighed (using a 0.0001-g precision Metter
scale) and used to calculate the mean quantity of pollen produced
per flower or cone. Total pollen production per tree was
calculated as: the number of flowers or cones per tree mean
weight of pollen per cone or flower (g). Average annual pollen
production for each species was estimated as the average total
pollen production for all 20 N. pumilio trees for which flowers
were counted and the 72 A. aruacana trees for which cones were
counted.
Seed production of each N. pumilio was calculated as the
number of seeds per cut branch the number of main branches on
the same tree. As seeds were found only in the outer part of main
branches, this method may be an appropriate relative measure,
although it may be an underestimation. Seed production for
A. araucana was estimated by multiplying the average number
of seeds per cone produced that year (Sanguinetti and Kitzberger
2008) by the number of female cones counted on each of the 72
trees measured. In this way, the mean annual production of cones
and seeds was obtained for each year for each species.
Seeds that fall from A. araucana in autumn (March–June)
often remain intact until the following spring (September–
December) and may serve as an important source of pre-repro-
ductive food for Austral Parakeets. Currently, there is no evidence
of any bird other than the Austral Parakeet foraging on fallen
A. araucana seeds from the crop of the previous years, although
wild Boar (Sus scrofa) and rodents frequently eat them
(Sanguinetti and Kitzberger 2008). However, noticeably
different markings on the seed husks left by wild Boars, rodents
and Austral Parakeets allow clear distinction between seed pre-
dators (S. Díaz, pers. obs.). During October–December of
each year, we counted fallen but uneaten A. araucana seeds in
a transect 2 20 m (based on the maximum A. araucana
seed dispersal distance of up to 20 m from an individual tree;
Gonzalez et al.2006), extending from the base of 20 different
female trees. Transects began at the trunk of the tree and were
assigned a random orientation, in such a manner that no overlap
occurred between neighbouring female A. araucana trees. Avail-
ability of A. araucana seeds from the previous season on the forest
floor was included in the spring analysis of food availability
(see Statistical analysis below).
Diet
Diet was assessed by direct observation. Foraging Parakeets were
observed by walking systematically through the study sites
between 0800 and 1100 hours; four observers were used in pairs.
Observations were recorded daily during the first and third weeks
of every month between October and March, and 4 days
per month for the rest of the year (total observation time = 720
observation hours in mixed N. pumilio–A. araucana forest and
588 h in monospecificN. pumilio forest). When a flock (2 birds)
was detected foraging, one bout was recorded (thus ensuring the
independence of each observation), as well as the location, type
of item consumed and the species of plant involved (Galetti
1993; Walker 2007). Feeding bouts varied from a few seconds
to several minutes. A recorded feeding bout was marked as ended
when the flock stops eating (and leaves the area).
Previous observations of the species suggest that all individual
Parakeets in a flock foraged on the same food item at that time
(S. Díaz, pers. obs.).
Reproduction of Austral Parakeets
Breeding was studied at 24 natural nests in the N. pumilio forest
and 39 nests in the mixed N. pumilio–A. araucana forest over the
three breeding seasons (December–March) of the study (2007–08
to 2009–10). All nests in the N. pumilio forest and 89% of nests in
the mixed forest were in N. pumilio trees, with the remaining
mixed-forest nests in A. araucana trees. The number of eggs or
nestlings were determined by inspection of nests using a home-
made wireless inspection camera attached to a telescopic pole, or
by climbing to cavities with ropes and aluminum ladders. The
camera (6 22 cm) was attached to a 20 cm-long flexible metal
support mounted on a 15 m-long pole (in two sections of 7.5 m
that could be used independently or together). Images from the
cavity were viewed from the ground by using a wireless monitor.
When climbing nest-trees, cavities were examined with a mirror
and flashlight. Nest-inspections were performed every other day
(starting from the end of November) to determine the date of
laying, until the clutch was complete (i.e. as Austral Parakeets
lay eggs every 1–2 days, when no new eggs had been laid after
1 week). After this, inspections occurred once per week, until the
end of the nesting period. Inspections were always done when the
female was outside the nest or when all adults away from the area
of the nest-tree. Reproductive parameters determined were date of
laying, clutch-size, hatching success (number of hatched eggs)
and number of nestlings. Reproductive success for each nest was
calculated as the ratio of the number of fledglings to clutch-size,
and the reproductive success of individual nests was calculated
for both sites in each year of the study. No nests failed during the
study period (all fledged at least one young).
Abundance of Austral Parakeets
Relative abundance was determined by counting individuals in
flocks (as well as number of flocks) at social sites where Parakeets
congregated during the early morning (S. Díaz, pers. obs.): two in
the N. pumilio forest and three in the mixed forest. Counts were
made between 0600 and 0900 hours over 4 consecutive days
in each study site, in the period before the start of laying (end of
November; roost survey method suggested by Casagrande and
Beissinger 1997). At each social site, two observers counted
236 Emu S. Díaz et al.
flocks at the same time (thus four observers counted in the
N. pumilio forest and six in the mixed forest at the same time).
For the mixed forest, counts were done from 2005 to 2010,
whereas in the N. pumilio forest, counts were done only for
2007–10. Flock counts were pooled over 1-min periods so that
the maximum number of Parakeets observed at the same time in
all social sites in each forest was considered the relative abun-
dance of Parakeets for the given forest.
Statistical analyses
Diet
The availability of food was defined as the number of available
food types (number of species with seeds or flowers) each month.
Temporal changes in availability were then analysed using a
paired Wilcoxon test to evaluate differences in the number of
available food types between months. A Mantel test was per-
formed to determine possible associations between the availabil-
ity of potential food types and their actual use throughout the year
and between study sites. The Mantel test was performed using
presence (1) –absence (0) matrices of available food types versus
food types that were used (1) –non-used (0). This method of
analysing diet emphasises the diversity of different food types
ingested by the Parakeets, but does not consider the amount of
each food that is eaten. However, the duration of feeding bouts
could not be used as a complementary measure of diet because
Parakeets tend to fly away when they detect an observer. In this
way, the Austral Parakeet’s diet was estimated based on the
frequency of feeding bouts for each food type (Galetti 1993).
Niche breadth was evaluated using the standardised Hurlbert’s
niche-breadth index (Krebs 1989), where values close to 0
indicate dietary specialisation, and values close to 1.0 indicate
a broad diet. Hurlbert’s index uses the Levins’index (Levins
1968) and incorporates a measure of the proportional abundance
of resources. Hurlbert’s index was calculated from observations
of Parakeet diet during October–March using the number of
Parakeets feeding on a given food type and the number of fruiting
individuals of each food plant species recorded in plot transects
each month.
Similarity or overlap in Parrot diet between the two study sites
was evaluated using the Morisita index of similarity (Krebs 1989)
for quantitative data on occurrence of food types in the diet. The
number of Parakeets observed feeding on each food type between
sites was used for this test. This index varies from 0 (no similarity)
to 1.0 (complete similarity).
Reproduction and abundance
The number of eggs and nestlings per nest and reproductive
success (the ratio of the number of fledglings to the number of
eggs per nest) were tested for normality using a Shapiro-Wilk test.
Non-parametric Kruskal–Wallis tests with Dunn post hoc tests
and Mann–Whitney tests were performed to determine if repro-
duction differed between the N. pumilio forest (n= 24) and the
mixed forest (n= 39) over the three years of the study. The relative
abundance of Parakeets in the mixed forest was correlated with
mean seed production of A. araucana from the previous year
using Pearson’s correlation coefficient.
All statistical analyses were performed with R statistical
software version 2.13.1 (R Development Core Team Foundation
for Statistical Computing, Vienna, Austria, www.r-project.org,
accessed 20 March 2012). All mean values are reported s.e., and
variables were consider to be significant at P<0.05 unless stated
otherwise.
Results
Availability of food and consumption
Araucaria araucana has an average of 0.85 g of pollen per cone,
and a mean of 160 male cones per tree in a non-mast year and
626 cones per tree in a mast year; N. pumilio has an average of
0.01 g of pollen per flower, with an average of 24 376 male
flowers per tree. Individual A. araucana cones produce an order
of magnitude more pollen than individual N. pumilio male
flowers. However, based on the estimated weight of pollen per
cone or male flower (above), estimated production of pollen per
A. araucana tree was 136.0–532.1 g and 243.8 g in N. pumilio.
The mean weight of an A. araucana seed is 3.5 g (Sanguinetti and
Kitzberger 2008), and that of a N. pumilio seed is 9.8 mg (Cuevas
2000). The estimated weight of seeds per A. araucana tree was
0.98 kg in non-masting years and 11.875 kg in masting years,
whereas the estimated weight of N. pumilio seeds per tree was
0.2 kg.
Availability of food in the forests during the breeding season
of Austral Parakeets was not significantly different between sites
(Z= 0.2, P= 0.089; Fig. 1). The asynchronous flowering and
seeding phenology of N. pumilio and A. araucana in the mixed
forest provided a more consistent supply of food throughout
the year than in the monospecificN. pumilio forest (Table 1). In
contrast, the monospecificN. pumilio forest showed a critical
scarcity of food at the end of autumn and in winter (April–
September), when little more than leaf buds and fungus were
occasionally available as food. There was no such shortage in the
mixed forest, because A. araucana seeds remained in trees and
on the forest floor and the phenology of N. pumilio in the mixed
forest was more advanced temporally than in the N. pumilio forest
(Table 1).
We observed 93 Austral Parakeet feeding bouts in
the N. pumilio forest on three plant species in two genera
14 1.0
0.8
0.6
0.4
0.2
0
12
10
8
6
4
Number of food items available
Hulbert’s standardised index
2
0
October November December January February March
N. pumilio forest
Hulbert index North Hulbert index mixed
Mixed forest
Fig. 1. Number of food types available and Hulbert’s niche-breadth
index for monospecificN. pumilio forest (Challhuaco) and mixed
A. araucana–N. pumilio forest (Tromen) for each month of the pre-
reproductive and reproductive season of Austral Parakeets.
The diet of Austral Parakeets in Patagonia Emu 237
(75 in N. pumilio and 18 in Misodendrum punctulatum and
M. linearifolium combined, these being hemiparasites of
N. pumilio) and in 133 feeding bouts in the mixed forest on four
plant species in three genera (48 in N. pumilio,72inA. araucana
and 13 in M. punctulatum and M. linearifolium combined). The
main foods consumed were male flowers and cones and seeds of
N. pumilio,A. araucana and Misodendrum species (Table 1).
Austral Parakeets used items as they became available in
both forests (Table 1). There were occasional observations of
Parakeets feeding on ephemeral leaf galls of N. pumilio (flocks
of 5–80 Parakeets in 79 observations), seed galls (136 Parakeets
in 12 observations) and insects from within male cones of
A. araucana (221 Parakeets in 69 observations); these items
served as additional but ephemeral food resources (i.e. available
only for a few days and no longer than 1 week). These data were
not included in the statistical analysis of diet as the availability of
the items was not quantified owing to their short temporal
availability.
Food types selected by Parakeets were significantly
correlated with their availability at both sites (Mantel Test,
r= 0.51, P= 0.04; r= 0.30, P= 0.01). However, the Morisita
indices of similarity for both sites were fairly low in
all months, showing a clear difference between diets in the two
forests (Table 2), owing to the presence of food items from
A. araucana in the mixed forest. Differences between the diets
in the two forests were lowest in January and February (Morisita
indices intermediate), when Parakeets fed on seeds of N. pumilio
in both forests.
In the breeding season, Hulbert’s standardised niche-breadth
index (Fig. 1) showed different patterns at the two study sites. The
index was fairly high for the N. pumilio forest, with the exception
of November, indicating that food was generally used according
to its availability (Fig. 1). In contrast, in the mixed forest, the index
was low during the pollen-feeding period (October–November),
indicating selectivity, and the index increased dramatically in
January and February when food resources were more abundant
(Fig. 1). A 1-month lag was evident between the two forests, with
the peak of food availability in the N. pumilio forest in December,
and in January in the mixed forest (rlagged = 0.85, d.f. = 3,
P= 0.05).
Seasonal patterns of food consumption
In the N. pumilio forest, Parakeets restricted their diet to food
types from N. pumilio and its hemiparasites Misodendrum punc-
tulatum and M. linearifolium (the latter as occasional items; see
Table 1). In another study, the diet in early spring was found to
consist of poorly digestible Misodendrum pollen (Díaz and
Table 1. The availability and use of food items by Austral Parakeets in the two forest sites and temporal relationship with life-history parameters
of Austral Parakeets
Light grey bars indicate common presence of food item; dark grey bars, abundant presence; X, use; O, occasional use and X*, use of previous year’s seed crop.
Life-history phenology: PL, pre-laying (courtship, copulation, prospectingfor nest-cavities, preparation of nest cavity); I, laying and incubation; R, brood-rearing;
F, fledging; NB, non-breeding (timing based S. Diaz, V. Ojeda and A. Trejo, unpubl. data)
Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May Jun. Jul. Aug.
MonospecificN. pumilio forest
Flowers
Nothofagus pumilio XXX
Misodendrum punctulatum OO
Misodendrum linearifolium OO
Seeds and fruits
Nothofagus pumilio XX X X
Misodendrum punctulatum OO
Misodendrum linearifolium OO
Life-history phenology PL I R F NB
Mixed A. araucana–N. pumilio forest
Flowers and male cones
Araucaria araucana XX
Nothofagus pumilio XX X
Misodendrum punctulatum O
Midodendrum linearifolium O
Seeds and fruits
Araucaria araucana X* X* X* X X X X X X
Nothofagus pumilio XX
Misodendrum punctulatum O
Misodendrum linearifolium O
Life-history phenology PL I R F NB
Table 2. Morisita index of similarity comparing diets from the
monospecificNothofagus pumilio forest and mixed A. araucana–
N. pumilio forest during the reproductive season of Austral Parakeets
October November December January February March
Morisita index 0.279 0.265 0.102 0.455 0.367 0.023
238 Emu S. Díaz et al.
Kitzberger 2006). By early November (late spring), after the first
flowers of N. pumilio emerge at lower elevations, Austral Para-
keets switched entirely to highly digestible N. pumilio pollen
(Díaz and Kitzberger 2006). Parakeets continued to feed on pollen
until late December using later flowering N. pumilio at higher
elevations, but there is nonetheless a short period where food is
scarce in late December (Table 1). During this early summer
shortage of food, Parakeets have been reported occasionally
feeding on galling insects (cf. Díaz and Peris 2011) and honeydew
(Díaz and Kitzberger 2006). After the ripening of seeds of the
lowest elevation N. pumilio in early February, the diet of Austral
Parakeets switched almost entirely to seeds of N. pumilio, with
seeds of Misodendrum eaten occasionally. Parakeets continued to
feed on seeds of N. pumilio until April, when most of the seeds had
fallen. Food was extremely scarce in late autumn and winter. At
this time, Parakeets have been reported occasionally feeding on
Misodendrum buds and Cyttaria fungal fruiting bodies (present
study; cf. Díaz and Kitzberger 2006). High specialisation on
N. pumilio pollen in spring and N. pumilio seeds in summer is
reflected in low Hulbert’s indices during November and February
(Fig. 1).
In contrast, in the mixed N. pumilio–A. araucana forest, high-
quality food was more evenly available throughout the year
because both N. pumilio and A. araucana were providing food
resources (Table 1). In early spring (October), the diet consisted of
a combination of pollen from new N. pumilio flowers and
A. araucana seeds remaining on the ground from the previous
autumn that are exposed after snow-melt. By mid- to late spring,
with no altitudinal gradient in the mixed forest and therefore a
shorter period of N. pumilio pollen availability compared to the
monospecificN. pumilio forest, Parakeets fed principally on the
maturing, long-lived male A. araucana cones, but also foraged
occasionally on Misodendrum flowers. A. araucana pollen
formed the main source of food from late spring to early summer,
so the summer gap evident in the N. pumilio forest was absent. By
January, Parakeets gradually switched from A. araucana pollen to
a diet of seeds, first early maturing N. pumilio and Misodendrum
seeds then, by March, to the crop of A. araucana seeds, which
remained available through winter.
Diet and reproductive timing
The timing of the main reproductive stages differed between sites
(Table 1). Clutch completion occurred 20 days earlier in the
mixed forest (mean 8 December, range 4–20 December, n= 39)
compared to the N. pumilio forest (mean 26 December, range 20
December–6 January, n= 24). In the N. pumilio forest, laying
coincided with the end of N. pumilio flowering, whereas in the
mixed forest, laying coincided with the peak of A. araucana
pollen release (late November–early December). In the N. pumilio
forest, incubation coincided with the summer period of food
scarcity (‘food gap’), whereas in the mixed forest incubation
coincided with the availability of A. araucana pollen. Presumably
Parakeets fed their nestlings mainly N. pumilio seeds in the
N. pumilio forest, whereas in the mixed forest they first fed them
with N. pumilio seeds followed with A. araucana seeds during the
last several weeks of their development in the nest. These seed-
based diets continued throughout the fledgling period, in autumn,
in both forests but seeds were available all winter only in the
mixed forest (Table 1).
Spatial and temporal variability in demography
Clutch-size was significantly different between 2007–08 and
2009–10 (Table 3), with higher values in 2007–08 and lower
values in 2009–10 (Table 4). We found no significant differences
in clutch-size between forests in these two seasons, although
clutches tended to be larger in the N. pumilio forest than in the
mixed forest (Table 4). In 2008–09, the pattern in clutch-size was
reversed, with significantly larger clutches in the mixed forest
than in the N. pumilio forest (Table 4).
Table 3. Variation in size of clutches and broods and reproductive success in both forests
Differences between years were assessed with Kruskal–Wallis and post hoc Dunn tests; differences between sites were assessed with
Mann–Whitney tests. Significant results are shown in bold (with Pgiven in parentheses)
Clutch-size Brood-size Reproductive success
Differences between years x
2
= 10.47 (d.f. = 2, P= 0.005) c
2
= 3.06 (d.f. = 2, P= 0.216) x
2
= 9.39 (d.f. = 2, P= 0.009)
08–09 (P= 0.892) 08–09 (P= 0.177)
08–10 (P= 0.014) 08–10 (P= 0.006)
09–10 (P= 0.010) 09–10 (P= 0.605)
Differences between forest types U=5(P= 0.071) U= 3969 (P<0.001) U=96 (P<0.001)
Table 4. Reproductive parameters of Austral Parakeets breeding in monospecificN. pumilio forest and mixed
A. araucana–N. pumilio forest over the 3 years of the study
Figures are means s.d. Reproductive success is the ratio of the number of fledglings to the number of eggs per nest
Year N. pumilio forest Mixed A. araucana–N. pumilio forest
2007–08 2008–09 2009–10 2007–08 2008–09 2009–10
Number of nests 7 7 10 12 20 7
Clutch-size 8 ± 2.4 5.3 ± 0.7 6.1 ± 1.5 6.6 ± 0.8 7.5 ± 1.4 5 ± 0.7
Brood-size 4.5 ± 1.3 3.1 ± 0.4 4.7 ± 1.2 4.3 ± 1.3 6.0 ± 1.5 4.1 ± 0.9
Reproductive success 0.56 ± 0.07 0.6 ± 0.09 0.77 ± 0.12 0.65 ± 0.17 0.8 ± 0.12 0.89 ± 0.18
The diet of Austral Parakeets in Patagonia Emu 239
In contrast to clutch-size, brood-size differed between forests
(Table 3), with significantly larger broods in the mixed forest
than in the N. pumilio forest (Table 4). Also, unlike clutch-size,
we found no differences between years, although in 2009 brood-
size in the mixed forest was larger than in the N. pumilio forest
(Table 4). The patterns of brood-size may indicate a strong
influence of local conditions, such as local availability of food
(Fig. 1), on hatching success in populations of Austral Parakeet
(Fig. 2).
Reproductive success (ratio of number of fledglings to the
number of eggs per nest) varied between years and forests
(Table 3). Mean reproductive success was significantly higher
in the mixed forest for all years combined (mixed forest = 0.77
0.16; N. pumilio forest = 0.69 0.14; Mann–Whitney Test
U= 96, P= 0.043), indicating an ~10% increase in the number
of eggs reaching fledgling stage in the mixed forest. Reproductive
success was also higher in mixed forest compared to the
N. pumilio forest nests in every year (Table 4, Fig. 2).
The mean number of Parakeets in the 200-ha N. pumilio forest
was 153 individuals (s.e. 9.5, range 144–163) over the 3 years of
the study, and remained fairly constant during the 3 years (Fig. 3).
In contrast, the estimated number of Parakeets in the 168-ha
mixed forest was greater and varied more between years, with an
overall mean of 179 individuals (s.e. 102, range: 70–274; Fig. 3)
over the 3 years of the study (Mann–Whitney U= 1296,
P<0.001).
A larger dataset of relative abundance of Parakeets and
production of A. araucana seed cones in the mixed forest between
2005 and 2010 showed a significant correlation between Parakeet
abundance and mean production of A. araucana seed cones in the
previous year (r= 0.97, d.f. =3, P= 0.005; Fig. 4).
Discussion
The overall higher relative abundance of Parakeets in the mixed
forest compared with the monospecificN. pumilio forest, and
the larger fluctuations in numbers, appear to be related to the
larger, but inter-annually variable, year-round resource base of
A. araucana food types in the mixed forest. A. araucana seeds
constitute a nutritionally and quantitatively important food re-
source but there are large differences in the abundance of this
resource between years (Sanguinetti and Kitzberger 2008).
Despite this, A. araucana seeds remain packaged in female cones
for several months until they finally fall to ground in autumn and
winter (Gonzalez et al.2006). Thus, pre-dispersal seed predation
by Parakeets is a low cost foraging activity because Parakeets can
ingest a large number of seeds without moving much within the
canopy or between crowns. Parakeets also feed on any seeds
that fall to the ground (which occurs commonly as the result of
destruction of cones by parrots), particularly when they fall on
snow-covered ground. Thus, as a result of their large size and
persistence on trees or on the ground, A. araucana seeds represent
a fairly constant, abundant, low-cost and accessible source of
food to Austral Parakeets. In contrast, the seeds of N. pumilio are
small, scattered along branches and within the crowns of trees and
forest canopy, remain only briefly on the trees as they mature
rapidly (a few weeks; Rusch 1993) fall to the ground and then
rapidly decompose, and so are then unavailable as food for
Parakeets. Parakeets have only rarely been observed feeding on
ground in N. pumilio forests while seeds are available (S. Díaz,
pers. obs.). Therefore, years of high A. araucana seed production
may increase winter survival of Parakeets because individual
nutritional status before winter is higher and because fallen seeds
are available throughout the winter and early spring. Non-
masting years of A. araucana are a critical period of food scarcity
in mixed forests that are clearly associated with reduced popula-
tions and reproductive success.
1.00
0.90
0.80
0.70
0.60
0.50
0.40
2008 2009 2010
N. pumilio forest
Mixed forest
Number of nestlings per egg per nest
Fig. 2. Reproductive success of Austral Parakeets in monospecific
N. pumilio forest (dotted line) and the mixed A. araucana–N. pumilio
forest (black line) over the 3 years of the study.
300
Parakeets relative abundance
250
200
150
100
50
0
2008 2009 2010
N. pumilio forest
Mixed forest
Fig. 3. Mean relative abundance of Austral Parakeets at each study site
during the three breeding seasons of the study.
300 40
35
30
25
20
15
10
5
0
250
200
150
100
50
02005 2006 2007 2008 2009 2010
A. araucana coner per tree
Mixed forest parakeets
relative abundance
Fig. 4. Mean relative abundance of Austral Parakeets (line) in the mixed
A. araucana–N. pumilio forest from 2005 to –2010 in relation to annual
A. araucana seed production (bars).
240 Emu S. Díaz et al.
In a previous study in monospecificN. pumilio forests, Díaz
and Kitzberger (2006) showed that Austral Parakeets had adapted
to make use of highly nutritious but hard to digest N. pumilio
pollen in food-limited habitats. By destructively harvesting large
amounts of the short-lived N. pumilio flowers along altitudinal
phenological gradients, Parakeets were able to extend the use
of pollen through the entire spring (Díaz and Kitzberger 2006).
In our study we showed that Parakeets also fed on the thick-coated
pollen of A. araucana (as described in Markgraf and D’Antoni
1978) and, by doing so, gain access to a rich source of protein
during a period of otherwise limited availability of food and that
may be crucial to successful breeding. The longevity of male
cones on A. araucana trees (~15–20 days in the tree, 10–15 days
on the forest floor; Gonzalez et al.2006) is much longer than
longevity of flowers of N. pumilio (~10 days in the tree; Premoli
et al.2007). In contrast to the inconspicuous male flowers of
N. pumilio, which are consumed exclusively on the trees, Para-
keets take advantage of the greater longevity of A. araucana cones
by feeding on those that remain intact on the ground after peak
pollination (S. Díaz, pers. obs.).
These patterns of resource tracking and exploitation by Austral
Parakeets concur with optimal foraging theory (Stephens and
Krebs 1989; Moermond 1990), which predict selection of food
resources that require less handling time or lower expenditure of
energy per unit of resource gained. Consistent with this, it may be
predicted that seed predators, such as parrots, will track food
resources in order to exploit temporal and spatial abundances in
seed production. Seasonal variations in diet have been noted for
Indonesian (Walker 2007), Australian (Rowley and Chapman
1991), and some Neotropical (Galetti 1993; Wermundsen 1997;
Renton 2001) parrots. Owing to the scarcity and patchiness of
food resources in pure N. pumilio forests, Austral Parakeets are
forced to move distances of hundreds of metres to several kilo-
metres, but remaining within pure N. pumilio forests, in search of
food and to follow the phenological phases of N. pumilio flower-
ing and seeding (Díaz and Kitzberger 2006). In contrast, foraging
behaviour in mixed N. pumilio–A. araucana forests is very
different. Because food is more evenly distributed throughout
the year, in most years, with no altitudinal gradients influencing
phenology, and is spatially concentrated, Austral Parakeets spend
less time and energy in searching for and handling food in mixed
forests than in N. pumilio forests.
Higher reproductive success in mixed forests is probably the
result of two factors: (1) the availability of A. araucana seeds from
the previous season during the early spring pre-laying period,
particularly in years following masting events and (2) the avail-
ability of protein-rich A. araucana pollen during the breeding
season to supplement the diet. This highlights the importance
of the timing of the availability of food resources, not just the
absolute abundance of food, as a critical factor influencing
reproductive success.
Despite consistently higher reproductive success of Austral
Parakeets in mixed forests, they showed much greater interannual
variation in relative abundance in these forests than the popula-
tions from monospecificN. pumilio forests, which varied little
throughout the study period. We suggest that the stability of
populations in monospecificN. pumilio forests relates to the long
period between masting events, which occur approximately every
10 years, and between which production of flowers and seeds is
low (Cuevas 2000; Heinemann 2007). Our study period was
conducted between masting events. In contrast, A. araucana has
much shorter masting cycles, with masting occurring approxi-
mately every 3–4 years (Gonzalez et al.2006). During our study,
2007 was such a masting year, and 2008 a non-masting year. We
found the change in abundance of Parakeets in response to levels
of A. araucana seed production is delayed by 1 year, with relative
abundance increasing in 2008, following masting in 2007, and
declining in 2009, following a non-masting season.
Smaller populations in years following non-masting seasons
may be a product of higher winter mortality rates or reduced return
rates to breeding habitats, or both, although our data cannot
distinguish between these mechanisms. Interestingly, for those
breeding pairs that do return after non-masting years, we found
reproductive success was lower than in other years within mixed
forests but remained higher than in the monospecificN. pumilio
forests. This may indicate that availability of food types in
spring, such as A. araucana seeds from the previous season and
A. araucana pollen are sufficient for successful initiation of
breeding. The fact that the relative abundance and reproductive
success of Austral Parakeets showed a contrasting pattern in
non-masting years in the mixed forest suggests that relative
abundance may be a poor measure of habitat quality for this
species. This is supported by several studies elsewhere that show
that a density and productivity relationship is not always the rule
in avian populations (see for example review from Bock and
Jones 2004, Johnson 2007) and variables such as survival rates,
reproductive success and rates of disturbance may be also im-
portant and should be considered when estimating habitat quality
(see for example Van Horne 1983; Vickery et al.1992; Pérot and
Villard 2009).
The Austral Parakeet is the most southerly distributed parrot in
the world, and is highly dependent on forests for shelter, nesting
habitat and food. However, different forest types differ in the
availability of these important resources, not only in quantity but
also in the timing of resource availability. We found Austral
Parakeets clearly responsed to differing resource availability in
contrasting habitats. Austral Parakeets showed a clear functional
response (Kitzberger et al.2007) to changes in the availability of
food by optimising their diet to include the most abundant,
concentrated and nutritional food types. Further, Austral Para-
keets showed a numerical response (Ims 1990) in abundance in
response to the A. araucana masting cycle. We found mixed
forests, in which N. pumilio provides abundant nesting sites
(Ojeda 2006; Díaz, in press) and A. araucana provides a rich
and stable food source, are clearly a unique and important habitat
for Austral Parakeets in the northern part of their distribution.
However, forests of A. araucana have a very restricted distribu-
tion and are vulnerable to degradation from invasive species and
human actions (Gonzalez et al.2006). Conservation management
should recognise this special role that mixed N. pumilio–
A. araucana forests play in Austral Parakeet ecology and take
the necessary steps to protect them.
Acknowledgements
The authors thank Cameron Naficy and Paul Edwards for their support, and the
Delegación de Parques Nacionales, especially the staff of Lanin National Park.
Financial support come from the Spanish MEC (project CGL2004–01716-
The diet of Austral Parakeets in Patagonia Emu 241
Feder), Birder’s Exchange, Idea Wild, Rufford Small Grant and a CONICET
(Consejo Nacional de Investigaciones Científicas y Técnicas) doctoral grant to
S. Díaz.
References
Areta, J. I., Bodrati, A., and Cockle, K. (2009). Specialization on Guadua
Bamboo seeds by three bird species in the Atlantic Forest of Argentina.
Biotropica 41,66–73. doi:10.1111/j.1744-7429.2008.00458.x
Barros, V. R., Cordon, V. H., Moyano, C. L., Mendez, R. J., Forquera, J. C.,
and Picio, O. (1983). Cartas de precipitación de la zona oeste de las
provincias de Río Negro y Neuquén. Report. Consejo Nacional de
Investigaciones Científicas y Técnicas, Buenos Aires.
Bock, C. A., and Jones, Z. F. (2004). Avian habitat evaluation: should
counting birds count? Frontiers in Ecology and the Environment 2,
403–410. doi:10.1890/1540-9295(2004)002[0403:AHESCB]2.0.CO;2
Brightsmith, D. J. (2005). Competition, predation and nest niche shifts
among tropical cavity nesters: phylogeny and natural history evolution
of parrots (Psittaciformes) and trogons (Trogoniformes). Journal of Avian
Biology 36,64–73. doi:10.1111/j.0908-8857.2005.03310.x
Casagrande, D. G., and Beissinger, S. R. (1997). Evaluation of four methods
for estimating parrot population size. Condor 99, 445–457. doi:10.2307/
1369951
Cuevas, J. G. (2000). Tree recruitment at the Nothofagus pumilio alpine
timberline in Tierra del Fuego, Chile. Journal of Ecology 88, 840–855.
doi:10.1046/j.1365-2745.2000.00497.x
Díaz S. Biología y conservación de la cachaña (Enicognathus ferrugineus).
El Hornero, in press.
Díaz, S., and Kitzberger, T. (2006). High Nothofagus flower consumption
and pollen emptying in the southern South American Austral Parakeet
(Enicognathus ferrugineus). Austral Ecology 31, 759–766. doi:10.1111/
j.1442-9993.2006.01637.x
Díaz, S., and Peris, S. (2011). Consumption of larvae by the Austral Parakeet
(Enicognathus ferrugineus). Wilson Journal of Ornithology 123,
168–171. doi:10.1676/09-190.1
Ferretti, V., Llambías, P. E., and Martin, T. E. (2005). Life history variation of
a neotropical thrush challenges food limitation theory. Proceedings of the
Royal Society of London. Series B. Biological Sciences 272, 769–773.
doi:10.1098/rspb.2004.3039
Fontaine, J. J., Decker, K. L., Skagen, S. K., and van Riper, C. III (2009).
Spatial and temporal variation in climate change: a bird’s eye view.
Climatic Change 97, 305–311. doi:10.1007/s10584-009-9644-9
Forshaw, J. M. (2010). ‘Parrots of the World.’(Helm: London.)
Galetti, M. (1993). Diet of the Scaly-headed Parrot (Pionus maximiliani)ina
semideciduous forest in southeastern Brazil. Biotropica 25, 419–425.
doi:10.2307/2388865
Gonzalez, M. E., Cortés, M., Izquierdo, F., Gallo, L., Echeverria,C., Bekkesy,
S., and Montaldo, P. (2006). Autoecología de las especies. Coníferas
Chilenas (Gimnospermas): Araucaria araucana.In‘Las especies arbór-
eas de los bosques templados de Chile y Argentina. Autoecología’.
(Ed. C. Donoso Zegers.) pp. 36–53. (Marisa Cuneo Ediciones: Valdivia,
Chile.)
Heinemann, K. (2007). Aspectos espaciales y temporales del establecimiento
de Nothofagus pumilio en claros de bosques maduros en los extremos de
un gradiente ambiental en el Noroeste de la Patagonia. Ph.D. Thesis,
Universidad Nacional del Comahue, San Carlos de Bariloche, Rio Negro,
Argentina.
Hutto, R. L. (1990). Measuring the availability of food resources. Studies in
Avian Biology 13,20–28.
Ims, R. A. (1990). On the adaptative value of reproductive synchrony as a
predator-swamping strategy. American Naturalist 136, 485–498.
doi:10.1086/285109
Johnson, M. D. (2007). Measuring habitat quality: a review. Condor 109,
489–504. doi:10.1650/8347.1
Kelly, D. (1994). The evolutionary ecology of mast seeding. Trends in
Ecology & Evolution 9, 465–470. doi:10.1016/0169-5347(94)90310-7
Kitzberger, T., Chaneton, E. J., and Caccia, F. D. (2007). Indirect effects of
prey swamping: differential seed predation during a bamboo masting
event. Ecology 88, 2541–2554. doi:10.1890/06-1587.1
Krebs, C. J. (1989). ‘Ecological Methodology.’(Harper and Row: New York.)
Lack, D. (1966). ‘Population Studies of Birds.’(Oxford University Press:
New York.)
Levins, R. (1968). ‘Evolution in Changing Environments.’(Princeton Uni-
versity Press: Princeton, NJ.)
Markgraf, V., and D’Antoni, H. L. (1978). ‘Pollen Flora of Argentina.’
(University of Arizona Press: Tucson, AZ.)
Martin, T. E. (1987). Food as a limit on breeding birds: a life history
perspective. Annual Review of Ecology and Systematics 18, 453–487.
doi:10.1146/annurev.es.18.110187.002321
Masello, J. F., and Quillfeldt, P. (2002). Chick growth and breeding success of
the Burrowing Parrot. Condor 104, 574–586. doi:10.1650/0010-5422
(2002)104[0574:CGABSO]2.0.CO;2
Masello, J. F., and Quillfeldt, P. (2003). Body size, body condition and
ornamental feathers of Burrowing Parrots: variation between years and
sexes, assortative mating and influences on breeding success. Emu 103,
149–161. doi:10.1071/MU02036
Masello, J. F., and Quillfeldt, P. (2004). Consequences of La Niña phase of
ENSO for the survival and growth of nestling Burrowing Parrots in the
Atlantic coast of South America. Emu 104, 337–346. doi:10.1071/
MU03039
Moermond, T. C. (1990). A functional approach to foraging: morphology,
behavior, and the capacity to exploit. Studies in Avian Biology 13,
427–430.
Newton, I. (1998). ‘Population Limitation in Birds.’(Academic Press: San
Diego, CA.)
Ojeda, V. S. (2006). Selección de sitios de nidificación y biología
reproductiva del carpintero gigante Campephilus magellanicus (Aves,
Picidae) en el noroeste de la Patagonia, Argentina. Ph.D. Thesis, Uni-
versidad Nacional del Comahue, San Carlos de Bariloche, Rio Negro,
Argentina.
Ostfeld, R. S., and Keesing, F. (2000). Pulsed resources and community
dynamics of consumers in terrestrial ecosystems. Trends in Ecology &
Evolution 15, 232–237. doi:10.1016/S0169-5347(00)01862-0
Paruelo, J. M., Beltrán, A., Jobbágy, E., Sala, O. E., and Golluscio, R. A.
(1998). The climate of Patagonia: general patterns and controls on biotic
processes. Ecología Austral 8,85–101.
Pérot, A., and Villard, M.-A. (2009). Putting density back into the habitat-
quality equation: case study of an open-nesting forest bird. Conservation
Biology 23, 1550–1557. doi:10.1111/j.1523-1739.2009.01272.x
Premoli, A. C., Raffaele, E., and Mathiasen, P. (2007). Morphological and
phenological differences in Nothofagus pumilio from contrasting eleva-
tions: evidence from a common garden. Austral Ecology 32, 515–523.
doi:10.1111/j.1442-9993.2007.01720.x
Renton, K. (2001). Lilac-crowned Parrot diet and food resource availability:
resource tracking by a parrot seed predator. Condor 103,62–69.
doi:10.1650/0010-5422(2001)103[0062:LCPDAF]2.0.CO;2
Renton, K. (2002). Influence of environmental variability on the growth of
Lilac-crowned Parrot nestlings. Ibis 144, 331–339. doi:10.1046/j.1474-
919X.2002.00015.x
Renton, K., and Salinas-Melgoza, A. (2004). Climatic variability, nest
predation and reproductive output of Lilac-crowned Parrots (Amazona
finschi) in tropical dry forest of western Mexico. Auk 121, 1214–1225.
doi:10.1642/0004-8038(2004)121[1214:CVNPAR]2.0.CO;2
Rowley, I., and Chapman, G. (1991). The breeding biology, food, social
organization, demography and conservation of the Major Mitchell or Pink
Cockatoo, Cacatua leadbeateri, on the margin of the Western Australian
wheatbelt. Australian Journal of Zoology 39, 211–261. doi:10.1071/
ZO9910211
242 Emu S. Díaz et al.
Rusch, V. E. (1993). Altitudinal variation in the phenology of Nothofagus
pumilio in Argentina. Revista Chilena de Historia Natural 66, 131–141.
Salafsky, S. R., Reynolds, R. T., Noon, B. R., and Wiens, J. A. (2007).
Reproductive response of Northern Goshawks to variable prey popula-
tions. Journal of Wildlife Management 71, 2274–2283. doi:10.2193/
2006-357
Sanguinetti, J., and Kitzberger, T. (2008). Patterns and mechanisms of masting
in the large-seeded southern hemisphere conifer Araucaria araucana.
Austral Ecology 33,78–87. doi:10.1111/j.1442-9993.2007.01792.x
Sanz, V., and Rodríguez-Ferraro, A. (2006). Reproductive parameters and
productivity of the Yellow-shouldered Parrot on Margarita Island, Vene-
zuela: a long-term study. Condor 108, 178–192. doi:10.1650/0010-5422
(2006)108[0178:RPAPOT]2.0.CO;2
Schnurr, J. L., Ostfeld, R. S., and Canham, C. D. (2002). Direct and indirect
effects of masting on rodent populations and tree seed survival. Oikos 96,
402–410. doi:10.1034/j.1600-0706.2002.960302.x
Stephens, D. W., and Krebs, J. R. (1989). ‘Foraging Theory. Monographs in
Behavioral Ecology.’(Princeton University Press: Princeton, NJ.)
Van Horne, B. (1983). Density as a misleading indicator of habitat quality.
Journal of Wildlife Management 47, 893–901. doi:10.2307/3808148
Veblen, T., Donosos, C., Kitzberger, T., and Rebertus, A. J. (1996). Ecology
of southern Chilean and Argentinean Nothofagus forests. In ‘The Ecology
and Biogeography of Nothofagus Forests’. (Eds T. Veblen, R. S. Hill and
J. Read.) pp. 293–319. (Yale University Press: New Haven, CT.)
Verhulst, S., and Nilsson, J. (2008). The timing of birds’breeding seasons: a
review of experiments that manipulated timing of breeding. Philosophical
Transactions of the Royal Society of London. Series B. Biological Sciences
363, 399–410. doi:10.1098/rstb.2007.2146
Vickery, P. D., Hunter, M. L. Jr, and Wells, J. V. (1992). Is density an indicator
of breeding success? Auk 109, 706–710.
Walker, J. A. (2007). Dietary specialization and fruit availability among
frugivorous birds on Sulawesi. Ibis 149, 345–356. doi:10.1111/j.1474-
919X.2006.00637.x
Wermundsen, T. (1997). Seasonal change in the diet of the PacificParakeet
Aratinga strenua in Nicaragua. Ibis 139, 566–568. doi:10.1111/j.1474-
919X.1997.tb04674.x
Zárybnická, M. (2009). Parental investment of female Tengmalm’s Owls
Aegolius funereus: correlation with varying food abundance and repro-
ductive success. Acta Ornithologica 44,81–88. doi:10.3161/00016
4509X464911
The diet of Austral Parakeets in Patagonia Emu 243
www.publish.csiro.au/journals/emu
