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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. 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