Download Mixed species nesting associations in Darwin`s tree finches: nesting

Biological Journal of the Linnean Society, 2009, 98, 313–324. With 3 figures
Mixed species nesting associations in Darwin’s tree
finches: nesting pattern predicts predation outcome
SONIA KLEINDORFER1*, FRANK J. SULLOWAY2 and JODY O’CONNOR1
1
2
School of Biological Sciences, Flinders University, Adelaide 5042, Australia
University of California, Berkeley, CA, USA
Received 8 December 2008; accepted for publication 26 March 2009
Predation is the main cause of passerine nesting failure. Traditionally, large intraspecific group size is thought to
accrue individuals with fitness benefits from increased predator vigilance and hence lower predation risk. To date,
few studies have investigated interspecific group size in relation to predation risk. In the present study, we
examined predation outcome in Darwin’s small tree finch, Camarhynchus parvulus, in nests with many or few
interspecific neighbours. We tested the predictions: (1) nests in mixed associations have lower predation than do
more solitary nests; (2) mixed species nesting associations covary with nest site vegetation characteristics; (3) older
(i.e. presumably experienced) males more commonly nest in mixed associations than younger males; (4) older males
select more concealed nesting sites; and (5) controlling male age, females prefer to pair with males in mixed
associations than at solitary nests. Almost half of all nests occurred in mixed associations (46%) compared to
solitary nests (54%), and the overall distribution of nests was decidedly nonrandom, displaying a bimodal pattern.
Nest site vegetation characteristics of the focal species were inconsistently associated with nesting pattern, but
older males did select more concealed nesting sites. Controlling differences in surrounding vegetation characteristics, mixed nesting associations experienced markedly lower predation than solitary nests, and females showed
a preference for males in mixed associations, as demonstrated by higher male pairing success. © 2009 The
Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 313–324.
bij_1264
313..324
ADDITIONAL KEYWORDS: age – aggregation – interspecific group – learning – reproductive success – risk
taking – Scalesia highlands.
INTRODUCTION
Predation is the primary cause of nesting failure in
birds (Ricklefs, 1969), and natural selection is predicted to shape behaviours that reduce nest predation
(Martin, 1993). For this reason, nest site selection is
considered an important determinant of nesting
success (Cody, 1985) with evidence that nest site
attributes, such as high levels of vegetation concealment, reduce nest predation (Martin, 1993; Bennett &
Owens, 2002; Kleindorfer, Hoi & Fessl, 2003; Lambert
& Kleindorfer, 2006). Nesting density is also important for nest predation outcome (Varela, Danchin &
*Corresponding author.
E-mail: [email protected]
Wagner, 2007). For example, high nesting success in
colonial breeding birds may result from increased
vigilance for predators, mobbing behaviour, or safety
in numbers (Hamilton, 1971; Goetmark & Andersson,
1984; Møller, 1987; Brown & Brown, 1996). Clearly,
large colonies are also easily detected by predators,
and nest predation may increase with colony size
(Burger, 1981; Brown & Brown, 1996; Varela et al.,
2007). Heterospecific aggregations provide alternative
model systems to understand the costs and benefits of
group living. For example, individuals may benefit
from the differential sensory capabilities of heterospecific group members to detect predators (Sieving,
Contreras & Maute, 2004; Griffin et al., 2005;
Semeniuk & Dill, 2006). The anti-predator function
of heterospecific associations is also proposed as
a potential explanation for heterospecific nesting
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 313–324
313
314
S. KLEINDORFER ET AL.
associations (Mönkkönen & Forsman, 2002; Tarof &
Ratcliffe, 2004).
The term ‘mixed species nesting associations’
refers to a specific nesting pattern in birds, whereby
nests of different species co-occur in space and time
in close proximity to each other (Slagsvold, 1980;
Mönkkönen et al., 1999). Such associations are
often formed with only two nests: one of a large
species (e.g. bird of prey) and the other of a smaller
species (e.g. passerine). Usually, the smaller species
in the mixed species pair has lower predation compared to its solitary nesting counterpart, which,
according to the protector species hypothesis, results
from protection conferred by the larger species
(Slagsvold, 1980; Pius & Leberg, 1998; Quinn et al.,
2003). To date, few studies have investigated variation in the number of species in mixed species
nesting associations in relation to predation
outcome. There is also a paucity of data on the nest
site vegetation structure of mixed nesting associations versus more solitary nests. This information is
important for interpreting the process of nest site
selection and for determing whether mixed nesting
associations are the result of habitat quality,
whereby ‘good areas’ sustain a higher number of
nests and diversity of nesting species. Furthermore,
birds that breed in isolation from conspecifics might
be doing so because of habitat limitation.
Darwin’s finches are an ornithological treasure
and comprise a model system by which to understand oscillating evolutionary dynamics in the wild
(Grant & Grant, 2008). To date, little is known about
the breeding biology of one monophyletic group,
Darwin’s tree finches (Kleindorfer, 2007a). Previous
research on the small tree finch, Camarhynchus parvulus, showed that nesting success was influenced by
nest concealment and male age, whereby older males
built more concealed nests. During the course of nest
searches, Kleindorfer (2007a) noted that some nests
had many heterospecific neighbours, whereas others
appeared to be solitary (P. R. Grant, B. R. Grant &
A. Abzhanov, pers. observ.). These observations provided the impetus for the current study, where we
addressed the questions: (1) do birds nest in close
proximity to other nests of the same or different
species; (2) is the nesting density (either of conspecifics or heterospecifics) associated with nest site
vegetation; (3) is nesting outcome (fledged, depredated) related to nest site vegetation and/or nesting
density; (4) do older (presumably experienced) males
have the same spatial nesting pattern and outcome
compared to younger males; (5) do older males select
more concealed nesting sites than younger males;
and (6) correcting for male age, do females prefer
males in mixed associations (inferred from pairing
success)?
MATERIAL AND METHODS
STUDY
SITE AND STUDY SPECIES
The study was conducted on Santa Cruz Island,
Galapagos Archipelago, in the highland forest surrounding the Los Gemelos craters (0°37′S, 90° 21′W)
(Kleindorfer et al., 2006; Kleindorfer, 2007a, b;
Kleindorfer & Dudaniec, 2009). We recorded nesting
outcome in the small tree finch, Camarhynchus parvulus, and recorded the nesting status of all birds
surrounding nests of the focal species. We sampled
nests from three study plots (each 2000 m2) during
the finch breeding season (January to March) of 2000,
2001, 2002, 2004, and 2005. The plots were separated
by 400 m, and occurred on either side of the main
road. Male small tree finches acquire a black crown
and chin with each year of moult, whereas females
remain olive green/brown throughout their lives (see
below). The birds are socially monogamous (Grant,
1999). Males build a display nest (sometimes two
display nests) and, subsequently, sing in front of the
display nest to attract a mate (Lack, 1947; Kleindorfer, 2007a). The female either rejects the male and his
display nest, accepts the male but the pair builds a
new nest together, or accepts both the male and the
display nest for nesting (Kleindorfer, 2007a). In addition to the role of nest site for pairing outcome, we
have evidence for size assortative pairing in the focal
species (Christensen & Kleindorfer, 2007), which may
be facilitated through morphologically referenced signalling via song (Christensen, Kleindorfer & Robertson, 2006). Specifically, beak size correlates with song
characteristics, and females could predict male beak
and body size from male song (Christensen et al.,
2006).
In addition to the focal species, the common highland species observed to nest in the present study
included: small ground finch Geospiza fuliginosa,
large tree finch Camarhynchus psittacula, woodpecker finch Camarhynchus pallidus, warbler finch
Certhidea olivacea, vermilion flycatcher Pyrocephalus
rubinus, and yellow warbler Dendroica petechia.
NEST
MONITORING
Small tree finch nests were located by systematically
searching study plots 5 days per week for evidence
of singing males, nest building behaviour, or pair
activity at a nest. Each nest was allocated a unique
number. The identity of the pair male and female was
established for most nests (using colour banding;
N = 85 males and 43 females), such that some nests
(N = 59) had unmarked birds (Kleindorfer, 2007a). We
do not believe the inclusion of unmarked birds introduces error into the study because only nests with
continuous male and female activity (i.e. song, nest
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 313–324
NESTING PATTERN AND PREDATION OUTCOME
building, incubation, and feeding) were included as
active nests. All active small tree finch nests were
monitored until the nesting outcome was known. The
age of the focal male was inferred based on the extent
(mm) of black plumage to the crown and chin (see
below). Nesting activity was monitored using 20-min
continuous focal sampling every 2 days (we recorded
male singing, nest building, nest attentiveness, male
incubation feeds to female, nestling feeding, and nest
defence). At the time the focal small tree finch nest
was discovered, we recorded the number of other
active nests per species within a 20 m radius, and
their nesting stage (e.g. nest building, incubation,
nestling, and feeding). Because nest monitoring is
very time consuming, we only used this first observation to record the temporal distribution of nesting
events among neighbouring nests. All neighbouring
nests remained active, and all of the nests of the two
large-bodied finches (i.e. woodpecker and large tree
finch) had eggs or nestlings, although we did not
monitor nesting outcome in nonfocal nests. A possible
source of imprecision associated with scoring only the
first observation of nest activity for nonfocal nests is
that some of these neighbouring nests may subsequently have been abandoned during the small tree
finch nesting cycle. We believe, however, that this
possible source of nesting attrition is relatively
modest because of the infrequent occurrence of nest
abandonment (i.e. generally less than 2%) once
nesting has started (S. Kleindorfer, pers. observ.).
Furthermore, our empirical focus is on the information about potential nesting sites, including the
number of nearest nesting neighbours, that was available to birds when they initially made a decision to
build nests in mixed aggregations or at more solitary
sites, amd not on new information that may have
become available to them after the nest was built.
Parental activity at focal nests was checked every 2
days, and nesting outcome for focal nests was categorized at the end of the nesting event. We considered
three possible nesting outcomes: (1) abandonment, (2)
fledging, and (3) depredation. Fledging was inferred
when nests were empty and chicks had reached the
ninth day from hatching. Predation was assumed for
nests previously containing eggs or chicks that met
the criteria: (1) chicks had not yet reached an age of
possible fledging (ⱕ 8 days old) and (2) the nest was
empty and undamaged, suggesting predation by the
introduced black rat, Rattus rattus, or the nest was
ripped in half or completely missing, suggesting predation by the native diurnal short-eared owl, Asio
flammeus (Bowman, 1961; Abs et al., 1965; Curio,
1969; Kleindorfer, 2007b). Suspected fledging, predation, or abandonment was confirmed by 30 min of
inactivity at the nest. Nests were then collected and
inspected for presence of abandoned eggs, egg shell,
315
or dead nestlings. The area below the nest was also
inspected for the presence of fallen or dead nestlings.
Because the introduced ectoparasite Philornis downsi
is a recent addition to selection pressures on nesting
success, and because the rate of P. downsi infestation
is known to be highest among closely-aggregated
nests (Kleindorfer & Dudaniec, 2009), we did not
include P. downsi parasitism in the assessments of
nesting outcome because this would have introduced
an extraneous bias into nesting outcome data.
NESTING
PATTERN
We recorded the location (GPS Garmin 12XC) and
number of active nests of any bird species (singing,
incubating, or feeding) within a 20 m radius of each
small tree finch focal nest. We also noted the number
of display nests in the area (discussed in Kleindorfer,
2007a), but we did not include unused display nests
in the analysis of active nests. We selected a 20 m
radial distance because this was the maximum distance from the nest that focal small tree finch males
responded to experimental playback of small tree
finch song (R. Christensen et al., unpubl. data; S.
Kleindorfer, unpubl. data). Estimation of the 20 m
radius was aided by placing two intersecting 10 m
ropes under the focal nest. Decimal longitude and
latitude co-ordinates were transformed into Universal
Transverse Mercator (UTM) coordinates in the form
of Eastings and Northings. These values were used to
calculate the distance between all recorded nests from
a common zero point.
RANDOM
AND TRANSECT SAMPLING
To assess whether our nest searches were biased in
favour of conspicuousness (e.g. we may have found
more mixed species aggregations than solitary nests
because the mixed aggregations were easier to locate),
we conducted two additional surveys to quantify the
prevalence of different spatial nesting patterns. In
2001, we sampled 25 random points in two study
plots and recorded all active nests within a 20 m
radius of the point sample. In 2005, we conducted ten
transect walks (each 200 m in length separated by
50 m) and sampled 50 transect points in areas adjacent to the study plots. For each transect point, we
recorded all active nests within a 20 m radius of the
point sample.
NEST
SITE VEGETATION CHARACTERISTICS
Within 7 days of the nesting outcome of the focal
small tree finch nest, we measured vegetation characteristics using measuring tapes surrounding the
nest within four quadrants (each with a 5 m radius)
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 313–324
S. KLEINDORFER ET AL.
positioned north–south and east–west (Kleindorfer,
Fessl & Hoi, 2005; Kleindorfer, 2007a). The variables
analysed in this study included: (1) nesting height
from ground to base of the nest; (2) nesting tree
height (a visual estimate); (3) percentage canopy leaf
cover for the nesting tree; (4) percentage leaf cover
1 m below the nest; (5) percentage leaf cover 1 m to
the side of the nest; (6) percentage leaf cover 1 m
above the nest; (7) undergrowth plant height (mean of
five point samples per quadrant) (cm); (8) percentage
ground cover within a 5 m nest radius and averaged
over four quadrants (visual estimates); and (9)
number of Scalesia trees (preferred nesting tree of
small tree finches).
RAINFALL
Annual rainfall data was collected daily in the highlands by the Charles Darwin Research Station at
Bella Vista, 194 m a.s.l (Kleindorfer (2007b)).
MALE
COLOUR/AGE AND NESTING PATTERN
Males increase the proportion of black on the chins
and crowns with each year of annual moult until
attaining a fully black head by 5 years of age,
although there is some variation across males in this
pattern (Lack, 1947; Grant, 1999; Kleindorfer, 2007a).
In a previous study, Kleindorfer (2007a) showed that
four out of 24 banded males (16%) resighted across a
single year did not increase colour category, whereas
20 birds increased one (N = 18) or two (N = 2)
plumage categories per year. Thus, in general, male
age covaries with male plumage coloration. This
pattern has also been found in Darwin’s ground
finches but, in this case, males acquire a fully black
body plumage (Grant & Grant, 1983, 1987). We
assigned each male to a unique colour category based
on the length of black on the chin (cm) and the extent
of black on the crown (Kleindorfer, 2007a) (Black 0
males are the youngest and Black 5 males are the
oldest among the population). For some analyses, the
data are combined to compare younger (Brown 0–3)
and older (Black 4–5) males. Small tree finch males
recorded in this study were subjectively assigned to
an age/colour category using binoculars in the field.
Binary logistic regression was used to analyse relationships between the PCA factor scores and predation outcome, nesting status (mixed or solitary), and
male age. Distances of neighbouring nests from focal
nests in relation to nesting pattern and year were
analysed using analysis of variance (ANOVA) and,
where appropriate, multiple linear and logistic
regression.
ETHICAL
NOTE
All procedures followed the Guidelines for the Use of
Animals in Research (Flinders University, Charles
Darwin Research Station, Galapagos National Parks),
the legal requirements of Ecuador (the country in
which the work was carried out), and were approved
by the Animal Welfare Committee of Flinders University (permit E189).
RESULTS
NESTING
PATTERN
The distribution of nests (N = 144) with 0–5 neighbours within 20 m of the focal small tree finch nests
was distinctly bimoda1 (Z = 2.98, P < 0.001, based on
the Kolmogorov–Smirnov test for deviation from a
normal distribution; Fig. 1). We next examined the
percentage of nests in relation to nearest neighbour
distance from the focal nest. Small tree finch
intraspecific nest distance was generally in the range
25–60 m, and in only two cases was another small
tree finch nest within the 20 m radius (Table 1). The
40
Percentage of nests
316
30
20
10
0
STATISTICAL
ANALYSIS
All data were analysed using the statistical software
package SPSS, version 14.0 for Windows (SPSS Inc.).
Variables were checked for normality and variance
homogeneity and normalized, where appropriate, by
recoding or by logarithmic transformations. Nest site
vegetation variables were analysed using principal
components analysis (PCA) with varimax rotation.
0
1
2
3
4
5
Number of neighbours (<20 m)
Figure 1. The percentage of focal nests that had 0–5
neighbours within 20 m of the focal nest (N = 144 nests).
The pattern was bimodal and subsequent data are analysed for nests that had ⱕ 1 neighbour (referred to as
solitary nests) or ⱖ 2 neighbours (referred to as mixed
species nesting associations).
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 313–324
NESTING PATTERN AND PREDATION OUTCOME
317
Table 1. The percentage of small tree finch focal nests that were solitary (N = 78) or in a mixed species nesting
association (N = 66), and had the species indicated as concurrent nest neighbours within a 20 m radius
Neighbouring species
Mass (g)
Solitary nests
Mixed species nesting
associations
Warbler finch
Small ground finch
Woodpecker finch
Large tree finch
Small tree finch
Vermilion flycatcher
Yellow warbler
9.4
13.3
22.0
16.7
12.2
10.0
12.0
26%
27%
8%
7%
0%
0%
0%
74%
73%
92%
93%
100%
100%
100%
(20)
(12)
(3)
(1)
(0)
(0)
(0)
(56)
(33)
(36)
(14)
(2)
(1)
(1)
The mean body mass (g) is shown for adults of each species. Males are on average 5% larger than females in most species.
Sample size is given in parentheses.
Analysed as a contrast according to annual rainfall
(Table 2), the trend in nesting patterns (solitary,
mixed) was almost significant (rpb = -0.16, t1,142 = 1.87,
P = 0.06), with solitary nests being more common
during years of greater rainfall (and resource abundance). The relationship between rainfall and the
proportion of older and younger males was not significant (r = 0.11, t1,142 = -1.34, P = 0.18). This trend
was nevertheless significantly different from that for
nesting patterns (Z = 2.30, P = 0.02, adjusted for the
crosscorrelation, rpb = 0.05), which suggests a possible
link between rainfall, male age, and nesting pattern.
Proportion of nests
0.5
Solitary Nest
Mixed Association
0.4
0.3
0.2
0.1
0.0
0
2
4
6
8
10 12 14 16 18 20 22 24 >26
SPECIES
Nearest neighbour (m)
COMPOSITION AND NESTING ONSET IN
MIXED NESTING ASSOCIATIONS
Figure 2. The proportion of small tree finch nests
had a nearest neighbour within each 2 m distance
egory (N = 128 nests). The data are shown for small
finch nests with ⱕ 1 neighbour (solitary nests) or
neighbours (mixed species nesting associations).
that
cattree
ⱖ2
nearest neighbour distances could exceed 20 m
because we generated all nearest neighbour distances
using UTM coordinates; neighbours in adjoining territories could appear as the closest neighbour but be
up to 60 m away, although the largest distance we
recorded was 90 m. For the purposes of analyses
conducted by means of ANOVA or chi-square tests, we
classified nests with ⱕ 1 heterospecific neighbours
within 20 m as ‘solitary’ associations and those with
ⱖ 2 heterospecific neighbours within 20 m as mixed
species nesting associations (Fig. 2). According to this
coding of ‘number of heterospecific neighbours’, 78 out
of 144 nests were solitary (54%) and 66 out of 144
nests were in mixed associations (46%). The proportion of nests in mixed associations for each year of
study was also comparable (c2 = 4.22, d.f. = 4,144,
P = 0.38) (Table 2).
We analysed the species composition of neighbouring
nests for focal small tree finches in two ways. First,
we examined each neighbouring species in solitary
and mixed nesting associations (Table 1). Five species
of Darwin’s finch were found to commonly nest as
neighbours of small tree finches in both types of
associations; other neighbouring species (vermilion
flycatcher, yellow warbler) were less frequent
(Table 1). Warbler finches were the most common
neighbour in both kinds of nesting associations,
whereas nonfocal small tree finches were the least
common neighbour. Second, we examined the proportion of nests per species that were initiated before or
after the small tree finch started nesting. In all cases,
the large-bodied finches that also commonly occurred
in mixed associations (woodpecker finch and large
tree finch; N = 24 confirmed observations) started
nesting before the focal small tree finch (at least 1
week prior to small tree finch), whereas 86 % of the
small-bodied finches (warbler finch, small ground
finch, N = 72 confirmed observations) started nesting
at the same time as the focal small tree finch.
Because we only made observations of interspecific
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 313–324
318
S. KLEINDORFER ET AL.
Table 2. Annual values are shown for highland rainfall, the percentage of small tree finch nests (count) that were
classified as solitary nests or mixed species nesting associations, and the percentage of nests that were built by younger
(brown 0–3) or older (black 4–5) males (N = 144)
2000
2001
2002
2004
2005
Annual rainfall
(highlands mm)
Solitary nests
Mixed species nesting
associations
Brown males (0–3)
Black males (4–5)
796
825
1591
806
813
44%
54%
67%
47%
53%
56%
46%
33%
53%
47%
72%
73%
67%
89%
76%
28%
27%
33%
11%
24%
(14)
(20)
(26)
(9)
(9)
(18)
(17)
(13)
(10)
(8)
(23)
(27)
(26)
(17)
(13)
(9)
(10)
(13)
(2)
(4)
The data set includes only one observation per colour banded bird. Sample size is given in parentheses.
Table 3. Nest site vegetation factor loadings (calculated using principal components analysis with varimax rotation,
N = 72)
Nest site variable
PC1
Nest height
Tree height
% Vegetation cover above nest
% Vegetation cover side of nest
% Canopy cover
0.97
0.96
PC2
PC3
PC4
PC5
0.54
0.82
0.70
Plant height
% Ground cover
% Vegetation cover below nest
Scalesia trees (N)
0.89
0.72
0.85
0.94
Only factor loadings above 0.50 are shown.
PC, principal component.
nesting status at the onset of small tree finch nesting,
we cannot draw general conclusions about temporal
aspects of interspecific nesting. From the focal small
tree finch perspective, there was an almost significant
trend for nest aggregations to be associated with the
presence of finch species larger than the focal species
(c2 = 2.71, d.f. = 1,177, F = 0.12, P = 0.10). When the
data are contrasted by body mass in a regression by
frequency analysis, there was a significant tendency
for heavier birds to be associated with nest aggregations (c2 = 6.38, d.f. = 1,179, rpb = 0.19, P = 0.01).
RANDOM
AND TRANSECT SAMPLES
The 25 random point samples in 2001 showed 12
single nests (48%) and 13 mixed association nests
(52%), using the criteria above, but without use of
the small tree finch as the focal nest. This finding is
not significantly different from the data on small
tree finch nests (c2 = 0.3, d.f. = 1,169, P > 0.5). The
transect data showed the same pattern: 29 out of 50
were single nests (58%) and 21 out of 50 were mixed
association nests (42%) (c2 = 0.2, d.f. = 1,244, P > 0.6).
NEST
SITE VEGETATION CHARACTERISTICS
Nine nest site vegetation variables were examined
using principal components analysis, as shown in
Table 3. The five components retained for statistical
analysis had an Eigenvalue of > 1 and explained
78.7% of the total cumulative variance. PC1 had high
factor loadings for nest and tree height, PC2 had high
factor loadings for canopy cover and vegetation concealment surrounding the nest, PC3 had high factor
loadings for plant height and amount of ground cover
below the nest, PC4 had high factor loadings for
vegetation concealment immediately below the nest,
and PC5 had high factor loadings for number of
nearby Scalesia trees.
We examined the five derived vegetation variables
(PCA scores) in relation to nesting pattern. There was
no significant difference between any of the derived
vegetation variables and nesting pattern (solitary,
mixed) (all P > 0.1) (Table 4). Our binary measure of
nesting strategy involves a modest loss of statistical
power (assuming that particularly high or low values
of nesting aggregation carry more meaningful infor-
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 313–324
NESTING PATTERN AND PREDATION OUTCOME
319
Table 4. The derived nest site vegetation variables (mean ± SE for principal components analysis scores) are shown in
relation to solitary and mixed associations along with the results of an analysis of variance comparing the variables
between solitary and mixed associations (N = 72 nests with vegetation measurements)
Mixed species nesting
associations
d.f.
t
P
0.04 ± 0.16
-0.07 ± 0.17
1
-0.46
0.65
-0.05 ± 0.16
0.06 ± 0.17
1
0.47
0.64
0.16 ± 0.16
-0.18 ± 0.17
1
-1.48
0.14
-0.14 ± 0.16
0.16 ± 0.17
1
1.26
0.21
-0.03 ± 0.16
0.03 ± 0.17
1
0.25
0.80
Solitary nests
PC1
Tree height
PC2
Canopy
PC3
Undergrowth
PC4
Cover below
PC5
Scalesia (N)
PC, principal component.
mation than other values). We therefore transformed
the data for nesting strategy into four ordinal categories to produce a normal distribution, combining
instances of two and three closest neighbours (N = 6,
N = 34) and, for consistency, cases of four or more
closest neighbours (N = 24, N = 5). We have used this
transformed ordinal variable for nesting pattern
in subsequent analyses involving regression when
expected linear trends are being tested. When we
examined the linear relationship between nesting
pattern, recoded as a normally distributed variable,
and our five principal components, there were two
significant predictors of nest aggregation: a negative
association with PC3 for plant height and associated
ground cover below the nest (pr = -0.23, t1,69 = -2.12,
P = 0.04) and a positive association with PC4 for
vegetation concealment immediately below the nest
(pr = 0.28, t1,69 = 2.47, P = 0.02). Only 10.6% of the
variance in number of nesting neighbours (the
adjusted R-squared) was explained by these two vegetation characteristics. In addition, vegetation differences were not related to the bimodal distribution in
nesting aggregations (based on logistic regression
analysis of vegetation characteristics and a dichotomous contrast between nests involving two close
neighbours versus all other nests; all P > 0.2). Vegetation differences were also unrelated to a graduated
quadratic contrast designed to reflect the bimodal
nature of the data for nesting associations (all
P ⱖ 0.3).
Consistent with results obtained in a previous
study in which older males were found to select more
concealed nesting sites (Kleindorfer, 2007a), we found
that nesting site vegetation was significantly related
to male age/colour. In the present study, older males
preferred nesting sites with greater ground cover
underneath the nest (PC3: r = 0.28, N = 72, P = 0.02).
There was an almost significant trend for older males
to prefer nesting sites with greater canopy cover
(PC2: r = 0.20, N = 72, P = 0.10). Using all five equally
weighted PC scores in a composite measure, we also
found an almost significant relationship between
male age and the overall amount of concealing vegetation near the nest (r = 0.22 N = 72, P = 0.06).
NESTING
OUTCOME
There was a comparable proportion of younger and
older males in the study population across years
(c2 = 3.56, d.f. = 4,144, P > 0.4) (Table 2), although
Brown 2–3 males became more prevalent over time
relative to other age groups (r = 0.32, N = 144,
P = 0.001; based on a quadratic contrast by male
colour). There was also a comparable proportion of
younger and older males in mixed nesting associations (c2 = 0.29, d.f. = 1,144, P > 0.6) (Table 5). We
next examined predation outcome as the dependent
variable (fledged, depredated) against two predictor
variables: male age (0–5 years) and the normalized
measure of number of neighbouring nests within
20 m (N = 63). In a logistic regression model, only
the number of neighbouring nests was significantly
related to predation outcome (rpb = -0.28, b = -0.76,
Wald1,61 = 5.14, P = 0.02) (Fig. 3), whereas male age/
colour had no significant effect (rpb = -0.15, b = -0.20,
Wald1,61 = 1.64, P = 0.20). Although the relationship
between number of neighbouring nests and predation
outcome was significant as a linear trend (with lower
predation occurring in mixed nesting associations),
there was also an almost significant quadratic trend,
controlled for this linear trend (pr = 0.26, b = 1.11,
Wald1,60 = 3.71, P < 0.06). This quadratic trend reflects
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 313–324
320
S. KLEINDORFER ET AL.
Table 5. Nesting outcome for small tree finches in the Santa Cruz highlands (2000–2005) at solitary nests or in mixed
species nesting associations
Total nests (male sings)
Brown males (colour 0–3)
Black males (colour 4–5)
Active nests (pair formed)
Depredated nests
Total brood loss from parasitism*
Nests with fledglings
Total nests
Solitary nests
Mixed species nesting
associations
144
106
38
72
42
10
20
54%
53%
58%
38%
48%
30%
20%
46%
47%
42%
62%
52%
70%
80%
(78)
(56)
(22)
(27)
(20)
(3)
(4)
(66)
(50)
(16)
(45)
(22)
(7)
(16)
*Specific analysis of Philornis downsi parasitism in relation to heterospecific nesting density in Kleindorfer & Dudaniec
(2009).
The two male colour categories are based on male plumage coloration whereby Brown 0–3 corresponds to younger and
Black 4–5 corresponds to older males.
Nest predation (%)
100
80
60
40
20
0
0
1
2
3
4
5
Number of neighbouring nests (<20 m)
Figure 3. The percentage of focal small tree finch nests
that were depredated is shown in relation to the number
of neighbouring nests; see also Table 1. For the bivariate
relationship between predation and normalized number of
neighbouring nests, r = -0.26, b = -0.73, Wald1,60 = 4.72,
P = 0.03, odds ratio = 0.48–1.0.
a decreasing marginal benefit associated with having
an increasing number of nearby nests.
In a separate analysis of predation rates for a
smaller subsample of birds for which nest site
vegetation characteristics were known (N = 38), we
examined the five principal components for vegetation. In logistic regression models, three significant
vegetation characteristics were predictors of predation: tree and nest height (PC1: r = 0.49, b = 2.19,
Wald1,36 = 7.37, P = 0.007), amount of canopy and
lateral cover (PC2: r = -0.44, b = -1.99, Wald1,36 =
7.02, P = 0.008), and amount of concealing vegetation
underneath the nest (PC4: r = -0.34, b = -2.42,
Wald1,36 = 3.91, P < 0.05). Heavily-predated nests
tended to be located high up in trees and lacked
canopy and lateral cover, as well as concealing vegetation immediately below the nest. In addition, controlling the amount of concealing vegetation by means
of a composite measure for all five principal components, a smaller number of neighbouring nests was a
significant predictor of higher levels of predation
(r = -0.38, b = -0.66, Wald1,35 = 4.18, P = 0.04).
In addition, males in mixed nesting associations
had substantially greater pairing success (68%)
than males at solitary nests (35%): c2 = 14.91,
d.f. = 4,144, f = 0.32, P < 0.001). In a previous study,
Kleindorfer (2007a) showed that Black 4–5 males
were chosen as nest partners (31 of 35 males
chosen) more often than Brown 0–3 males (44 of
92 males chosen) (c2 = 17.4, d.f. = 1,126, f = 0.37,
P < 0.001). Here, we show that, in addition to male
colour, nesting pattern was significantly related to
successful pair formation. In a logistic regression
model with males chosen as the dependent variable,
both male colour and number of nearest nesting
neighbours were significant predictors of successful
pairing (male colour: rpb = 0.35, b = 0.52, Wald1,141 =
19.36, P < 0.001; nesting pattern: rpb = 0.30, b = 0.73,
Wald1,141 = 14.09, P < 0.001). The interaction term
was not significant.
Although male age/colour was not related to nesting
strategy as a main effect in analysis of variance, we
did find that male age/colour was associated with
nesting strategy in interaction with year of sampling.
Controlling the main effects for year and male age/
colour (neither of which was significant), the interaction between these two variables in a linear regression
analysis yielded a partial correlation of -0.18
(t1,140 = -2.13, P = 0.04), indicating that older males
shifted from a predominately mixed association
nesting pattern to a predominately solitary pattern
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 313–324
NESTING PATTERN AND PREDATION OUTCOME
during the 5-year period of the study. To elucidate
possible causes of this behavioral shift, we examined
the relationship between male age/colour and other
pertinent variables in the present study, including
nesting site vegetation characteristics as well as
pairing and reproductive success. We found two temporal trends that appeared to be relevant to explaining why older males switched nesting strategies. First,
there was a significant increase in canopy cover
during the 5-year study period (r = 0.69, N = 72,
P < 0.001). As a result of the major El Niño event of
1998, many Scalesia trees fell over, opening up the
forest canopy. Based on a 30-year mean for recorded
rainfall, rains were below normal for the next 7 years
(Hicks & Mauchamp, 2000; Dudaniec, Fessl & Kleindorfer, 2007), with the exception of the relatively
heavy rains in 2002, after which the canopy increasingly filled in again. Because older males were more
likely than younger males to avail themselves of
concealing vegetation at nesting sites, they appear to
have taken advantage of the increase in concealing
canopy cover to nest in more solitary (and hidden)
locations rather than competing for limited resources
in mixed associations. Second, controlling nesting
strategies, we found that there was a linear decline in
the overall rate of pairing and nesting success during
the 5-year study period (pr = -0.36, t1,141 = -4.53,
P < 0.001, with success coded as a linear contrast:
-1 = display nest built, unsuccessful pairing; 0 = successful pairing, eggs or chicks later predated; and
+1 = successful fledging). This decline in nesting
success does not take into account the effects of P.
downsi, the introduced ectoparasite that was first
discovered in 1997 (Fessl, Couri & Tebbich, 2001) and
caused increasing nesting failure between 2000 and
2005 (Dudaniec et al., 2007). Birds with many nesting
neighbours have higher parasitism from P. downsi
(Kleindorfer & Dudaniec, 2009), such that older birds
that decide to nest in more solitary locations may have
been trading off the risk of higher predation rates from
owls and rats for potentially lower parasitism from P.
downsi. Whatever the causes of this shift in nesting
strategies by male age, older males were more inclined
than younger males to adopt what would normally be
considered a riskier nesting alternative during the
last 2 years of the study. We did not find, however, that
older males increased the amount of concealing vegetation that they chose near the nest after 2002;
rather, they took advantage of the greater prevalence
of concealing vegetation at solitary sites.
DISCUSSION
The number of neighbouring nests in a 20 m radius of
Darwin’s small tree finch showed a distinctly bimodal
distribution (Fig. 1). The proportion of nests in each
321
pattern (solitary, mixed) was corroborated by our
random and transect sampling in 2001 and 2005,
respectively, which revealed comparable patterns
irrespective of our sampling method.
PATTERNS
OF HETEROSPECIFIC AGGREGATIONS
IN OUR STUDY
One of the most surprising results obtained in the
present study was the almost complete absence of
focal nests with exactly two neighbours. This result is
consistent with an ecological trade-off in which the
benefits stemming from heterospecific nesting follow
an increasing, and accelerating function, whereas the
costs of competition from close neighbours follow a
linear function. The net effect of two such contrasting
trends will be larger net benefits, compared to costs,
for birds nesting either near few or many neighbours,
but not for birds nesting in proximity to an intermediate number of neighbours (for a similar argument
regarding ecological similarity trade-offs in social
information use, see Seppänen et al., 2007). Controlling the linear trend between nesting outcome and
number of nearest neighbours, we did find an almost
significant curvilinear relationship based on a quadratic contrast. This quadratic trend, however, indicates a decreasing rather than increasing benefit from
nesting in mixed aggregations. Moreover, had parasitism by P. downsi been included in our measure of
predation rates, it would likely have augmented this
quadratic trend, given the higher rates of infestation
that are found in mixed nesting aggregations (Kleindorfer & Dudaniec, 2009). Hence, the source of the
bimodal distribution in nesting patterns is not readily
explained by the data available to us and requires
further study.
Using a normally distributed coding for number of
nesting neighbours, rather than a binary contrast, we
found two significant vegetation differences. Denselyaggregated nests had greater vegetation cover 1 m
below the nest, but these same nests also had less
ground cover and lower plant height at the base of
the nesting tree. Although this pattern appears to be
inconsistent, evidence of greater vegetation cover
immediately below the nest is probably more relevant
to successful nest concealment than is ground cover.
Three other aspects of nest site vegetation were not
significant predictors of nesting associations. More
importantly, after controlling for vegetation differences, birds nesting in mixed associations incurred
significantly reduced predation. Hence, vegetation
characteristics, although they appear to explain some
aspects of nesting associations, do not fully account
for the benefits derived from such associations. More
specifically, the effect size for number of nesting
neighbours on predation outcome, controlling vegeta-
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 313–324
322
S. KLEINDORFER ET AL.
tion characteristics (pr = 0.38) is more than two-fold
greater than the mean effect reported in a metaanalysis of selection gradients in natural populations
(Hoekstra et al., 2001).
A previous study on small tree finches found that
females preferred well-concealed nests and older
males as nest partners (i.e. older males tended to build
more concealed nests higher in the canopy) (Kleindorfer, 2007a). Counter to expectation, in the present
study, we found that older males did not exhibit a
consistent preference for mixed nesting aggregations.
Instead, they manifested a variable strategy, preferring to nest in mixed aggregations during the first 3
years of the study and switching to more solitary
nesting sites during the last 2 years of the study. In
accordance with expectation, males in mixed associations had substantially higher pairing success than
males at solitary nests (68% versus 36%), and mixed
associations had substantially lower predation (49%
versus 75%). Also significant as predictors of predation
were nests located high up in trees that lacked concealment above, to the sides, and immediately below
the nest. Two of the three vegetation characteristics
that predicted predation were different, however, from
the two vegetation characteristics that predicted
nesting associations. This finding suggests that vegetation characteristics do not have a simple relationship with breeding behaviour.
attempt to test for habitat selection because we did
not measure habitat sampling behaviour.
MALE
AGE AND VARIABLE NESTING STRATEGY
Although male age was not related to nesting strategy in a linear manner, it was associated with nesting
strategy in interaction with the year of sampling.
Older males chose mixed nesting aggregations during
the first 3 years of the study and then, subsequent to
the heavy rains in 2002, took advantage of a greater
availability of concealing vegetation (particularly
canopy and lateral nest cover) to choose more solitary,
but well-hidden nesting sites. Older males may also
have changed their previous preference for mixed
nesting aggregations in response to a significant
decline in pairing and nesting success during the
5-year study period. In addition, older males may
have been responding to an increase in the prevalence
of Brown 2–3 males competing for mixed aggregation
nesting sites during the last 2 years of the study.
Because greater rainfall is related to fledging success,
this relative increase in the proportion of Brown 2–3
males appears to be a consequence of the particularly
heavy rains in 2002 during what was otherwise a
period of below-average rainfall.
NESTING
AGGREGATIONS AND NEIGHBOURING
FINCH BODY SIZE
VEGETATION
ASSESSMENT VERSUS
HABITAT SAMPLING
Studies of nest site selection in birds are often based
on population level relationships between nesting
density and microhabitat variables, such as vegetation structure in used and unused sites (Van Horne,
1983; Martin & Roper, 1988). This approach provides
only limited information about habitat selection,
because: (1) no information is available on whether
birds sampled information from multiple habitat
types before ‘selecting’ one type in which to breed and
(2) the fitness consequences of breeding in one habitat
versus another are not compared (Martin, 1998;
Doerr, Doerr & Jenkins, 2006). Understanding the
process of habitat or nest site selection is further
complicated by studies demonstrating that nesting
density may be based on aggregation tendencies that
are conspecific (Slagsvold, 1980; Stamps, 1988; Muller
et al., 1997; Mönkkönen et al., 1999) or heterospecific
(Fletcher, 2007), copying behaviour (Bradbury, 1981;
Pruett-Jones, 1992) or public information about
breeding performance (Doligez, Etienne & Clobert,
2002). Aware of these pitfalls, we examined whether
nesting density was related to habitat features (nest
site vegetation assessment) and whether breeding
success was predicted by nesting density. We did not
Nest aggregations involving the small tree finch
tended to be increasingly common by mass of the
neighbouring finch species. The least common combination of neighbouring species was for the large tree
finch and woodpecker finch; both species are the
largest of the highland tree finch species (Table 1).
This apparent avoidance between the two large
species points to possible niche overlap between the
large tree finch and woodpecker finch, which is supported by a study of their foraging behaviour (Tebbich
et al., 2004). We recorded earlier nesting onset in the
large-bodied species than in our focal species. It is
likely that large-bodied birds have more energy
reserves and can initiate earlier breeding for this
reason.
This is one of few studies addressing nesting patterns in Darwin’s tree finches in the highlands (Kleindorfer & Dudaniec, 2009) and the first long-term
study to look at these patterns in relationship to
nesting success in Darwin’s small tree finch. It is
therefore unclear whether the aggregated nesting
patterns reported in the present study have always
been characteristic of Darwin’s tree finches in the
highlands of Santa Cruz Island, or whether they are
the by-product of recent habitat loss as a result of
encroaching agricultural practices, severe climatic
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 313–324
NESTING PATTERN AND PREDATION OUTCOME
events (Grant et al., 2000), or introduced species
(Wikelski et al., 2004; Causton et al., 2006; Fessl,
Kleindorfer & Tebbich, 2006; Fessl, Sinclair & Kleindorfer, 2006; Dudaniec & Kleindorfer, 2006; Kleindorfer & Dudaniec, 2006; Wiedenfeld et al., 2007).
In a previous study, Kleindorfer & Dudaniec (2009)
showed the costs of mixed species nesting associations
in Darwin’s tree finches: nests with many neighbours
had high parasite intensity. In the present study, we
show the benefits of mixed species nesting associations: nests with many neighbours had lower nest
predation over the 5-year period of the study. Furthermore, females preferred males that built nests in
mixed associations. Future research should address
the changing selective pressures on survival (parasitism, predation) that will influence the relative costs of
nesting with heterospecific neighbours.
ACKNOWLEDGEMENTS
We thank the Galapagos National Park Service and
the Charles Darwin Research Station for the opportunity to work on the Galapagos Archipelago, and
TAME airlines for the reduced airfare to the Galapagos. We thank Max Planck Institute for Ornithology
for logistical support. This study was funded by the
Austrian Academy of Sciences between 2000–2002
and Flinders University through an Establishment
Grant in 2004 and 2005 with awards to S.K. We
thank Carlos Vinueza, Santiago Torres, Rebekah
Christensen, Rachael Dudaniec, and Jeremy Robertson for their assistance with field work. We thank
Mark Lethbridge and Kat Goss for assistance with
UTM nest distance calculations, and Kat for her help
in the field. We are also grateful to Janne-Tuomas
Seppänen for insightful comments on the paper.
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