Factors Influencing Nest Spacing of a Secondary Cavity-Nesting Parrot: Habitat Heterogeneity and Proximity of Conspecifics

Abstract.

Resource availability in a heterogeneous environment and density-dependent processes may influence the spatial distribution of individuals among habitats. The distribution of nests of secondary cavity nesters is rarely clumped because the birds are constrained by the distribution of existing cavities as nest resources. In this study, to evaluate the interplay of environmental and behavioral processes in the spacing of parrot nests, we compared the spatial distribution of active Lilac-crowned Parrot (Amazona finschi) nests with that of all cavities used as nests over 14 years. Parrots reused 42% of cavities, and the frequency of reuse was significantly associated with a previously successful nesting attempt. Positive fitness benefits of cavity reuse may indicate high-quality nest sites that are used more intensively by resident breeding pairs. Spatial-point-pattern analysis indicated that trees used as nests were significantly clustered within 60 m in the three nesting areas, with average distance of 100–200 m between nest trees. In a given breeding season, active parrot nests were separated by a mean 950 ± 890 m. Parrot nests were also located significantly closer to a tree used as a nest in the previous breeding season than the distance between nearest nesting conspecifics. This pattern suggests that conspecifics influence the spatial distribution of reproductive pairs breeding simultaneously, with nesting pairs occupying areas where suitable cavities are more numerous. The behavioral spacing requirements of nesting parrots may limit breeding densities and restrict management strategies to increase numbers of nesting pairs within protected areas.

Resumen.

La disponibilidad de recursos en un ambiente heterogéneo y los procesos de denso-dependencia pueden influir en la distribución de organismos entre hábitats. En aves anidadores secundarias de cavidades de árboles, los nidos pocas veces presentan una distribución espacial agregada, ya que están limitadas por la distribución de los recursos de anidación existentes. En este estudio, comparamos la distribución espacial de nidos activos de Amazona finschi con todas las cavidades disponibles usadas como nidos por un periodo de 14 años, para evaluar la interacción entre los procesos ambientales y conductuales. El 42% de las cavidades fueron reutilizadas por los loros y la frecuencia de reutilización estuvo significativamente asociada con un intento previo exitoso de anidación. Los beneficios positivos en la adecuación causados por la reutilización de las cavidades pueden indicar sitios de anidación de alta calidad que son utilizados más intensivamente por parejas reproductivas residentes. El análisis del patrón espacial de puntos indicó que todos los árboles utilizados como nidos estuvieron significativamente agrupados a una distancia menor de 60 m en las tres áreas de anidación, con una proximidad promedio de 100 a 200 m entre árboles utilizados como nido. Sin embargo, los nidos activos en una temporada reproductiva estuvieron separados en promedio por 950 ± 890 m. Además, los nidos estuvieron significativamente más cerca de un árbol utilizado como nido el año previo en comparación con la distancia entre los nidos de los individuos conespecíficos. Esto podría indicar la influencia de los individuos conespecíficos sobre la distribución espacial de las parejas reproductivas que crían simultáneamente, de modo que las parejas ocupan las áreas en donde las cavidades apropiadas son más numerosas. Los requerimientos de espaciamiento de los loros que anidan pueden limitar la densidad de individuos reproductivos y restringir las estrategias de manejo para incrementar el número de parejas reproductivas dentro de áreas protegidas.

Introduction

Resource availability and interactions among individuals may influence animals' distribution and habitat choice to maximize fitness. Individuals may be spatially distributed at random among habitats with equal fitness rewards (Fretwell and Lucas 1970). Density-dependent processes and conspecific cueing, however, create deviations from this ideal free distribution of individuals among habitats. Costs such as the attraction of predators or intraspecific competition may arise as a result of clumping of individuals. These costs may create densities lower than those under an ideal free distribution (Cowan 1987, Krause and Ruxton 2002). Conversely, positive density-dependence mechanisms (Allee effect) such as the deterrence of predators and conspecific cueing of habitat quality may create deviation from an ideal free distribution toward higher densities (Danchin and Wagner 1999, Brown et al. 2000, Donahue 2006). A clumped distribution is generally restricted to situations where the benefits of living in proximity outweigh the costs of higher density. Environmental heterogeneity may also modify patterns of use of space (Wiegand and Moloney 2004, Cornulier and Bretagnolle 2006, Roth and Islam 2007). Hence, the spatial patterns observed in nature result from the interaction of individuals and environmental attributes, especially when there is spatial variation in resources, cover, or the distribution of preferred breeding sites.

The nests of secondary cavity-nesting birds are rarely clumped because these species are constrained by the distribution of existing cavities as nest resources (Eberhard 2002). Most parrots are secondary cavity nesters, relying on preexisting cavities, so are unlikely to nest in close proximity to conspecifics (Eberhard 2002). Hence, clustering of their nests would be rare unless either environmental heterogeneity concentrates suitable sites in a given area or density-dependent processes act positively by increasing fitness.

Environmental heterogeneity may contribute to the aggregated nesting of the Thick-billed Parrot (Rhynchopsitta pachyrhyncha), which requires tree cavities in old-growth coniferous forests that are concentrated in isolated forest patches at elevations above 2000 m (Monterrubio-Rico et al. 2006). Psittacines that nest in cavities in cliff walls, such as the Maroon-fronted Parrot (Rhynchopsitta terrisi; Enkerlin-Hoeflich et al. 2006), the Military Macaw (Ara militaris; Bonilla-Ruiz et al. 2007), and the Burrowing Parrot (Cyanoliseus patagonus; Masello and Quillfeldt 2002), also nest colonially. Aggregated nesting could result from the environmental concentration of suitable nest sites in a specific area, though the inaccessibility of high cliff walls may also serve to reduce predation (Masello and Quillfeldt 2002). By comparison, positive density-dependent processes may play a major role in aggregated nesting when parrots are released from this dependence on pre-existing cavities (Eberhard 2002). For example, the aggregated nesting of the Monk Parakeet (Myiopsitta monachus), distinct among parrots in that it constructs its own hanging nests in clusters, may serve to increase the capability of the birds' detecting nest predators (Eberhard 1998).

In parrots, interspecific and intraspecific interactions may also influence the spacing of breeding pairs. A limited availability of cavities suitable for nesting may result in agonistic interactions (Waltman and Beissinger 1992, Heinsohn et al. 2003, Murphy et al. 2003), from which an overdispersed distribution of breeding pairs would be expected. These interactions may limit access to cavities by potential breeding pairs when cavities are clumped (Renton 2004). Few studies, however, have examined the potential interplay of cavity distribution and conspecific interaction on the spatial distribution of parrot nests.

In the present study, we evaluated the spatial requirements of nesting pairs of the Lilac-crowned Parrot (Amazona finschi) over 14 years. We aimed to determine whether the spacing pattern of active nests within a given breeding season corresponded with the spatial distribution of all cavities used as nests. In this way, we aimed to elucidate the interplay of environmental and behavioral processes driving the spacing pattern of nests of this secondary cavity nester, and we evaluate the implications for the conservation and management of breeding populations.

Methods

We studied Lilac-crowned Parrot nests in the tropical dry forest of the 13 142-ha Chamela—Cuixmala Biosphere Reserve, Jalisco, on the Pacific coast of Mexico. Mean annual precipitation at the study site is 748 mm, with 85% of rain falling from June to October; there is a prolonged drought from mid-February to late May (Bullock 1986). The study area is predominantly hilly and dominated by deciduous forest with semi-deciduous forest restricted to the larger drainages and valleys (Rzedowski 1994). A mixture of tree species from both vegetation types is found along seasonally dry streambeds (arroyos). Monospecific stands of Piranhea mexicana also occur within 10 km of the coast (Martijena and Bullock 1994). The Lilac-crowned Parrot nests during the dry season from February to May (Renton and Salinas-Melgoza 1999). Important tree species used for nesting by the Lilac-crowned Parrot are Astronium graveolens, Brosimum alicastrum, and Tabebuia spp., as well as P. mexicana (Renton and Salinas-Melgoza 1999, Monterrubio-Rico et al. 2009). These tree species are all characteristic of semi-deciduous-forest, which is restricted to more humid valleys, creating a marked environmental heterogeneity that could influence the distribution of nesting parrots.

We defined three nesting areas, Chamela (115.2 ha), Careyes (116.6 ha), and Cuixmala (2568.3 ha), on the basis of landscape features distinguishing each area (Fig. 1) and concentrated our search effort for parrot nests within these areas. The Chamela area is at low elevations (20–120 m above sea level) and extensively covered with semi-deciduous forest. The Cuixmala area is hilly and dominated by deciduous forest, with patches of semi-deciduous forest along watercourses; it has the largest elevational range of the three nesting areas (20–320 m above sea level). Finally, the Careyes area corresponded to the lower basin of the Arroyo Careyes, which contains extensive monospecific patches of P. mexicana. The Careyes area ranges from 20 to 200 m above sea level so is intermediate in elevation between Chamela and Cuixmala. The mean distance between the centers of the three nesting areas was 7.3 ± 2.8 km (range 4.7–10.2 km, n = 3).

Habitats outside the reserve have been modified, with low-lying areas converted to agriculture, orchards, or cattle pastures. Most areas within the reserve have not been subjected to timber extraction and cattle ranching, though some anthropogenic disturbance occurred in small areas prior to establishment of the reserve. Small sections of the Careyes and Cuixmala areas were previously subjected to occasional selective logging and free-range cattle grazing. However, these activities were undertaken sporadically in isolated holdings of <1 ha rather than in intensive or systematic timber extraction or cattle ranching.

Data Collection

We surveyed each of the three areas for parrot nests via trails, dry streambeds, and by observations from ridge-top overlooks during the breeding seasons of 1995 to 2008. We considered a cavity an active nest when one parrot remained within the cavity while the other left to forage (Renton and Salinas-Melgoza 1999) and located all nests in January and February at the start of the breeding season. For each cavity used as a nest, we recorded the location of the nest tree in UTM units by using a hand-held GPS (Garmin GPS 12). Finally, we evaluated landscape features of nest-site selection by proximity to dry streambeds, which were defined based on hydrological information from maps of the study site (INEGI 1986). We measured the distance of the nesting trees to dry streambeds with Ilwis open software (ITC 2007). From 1995 to 2008, in the three nest areas, we located a total of 96 nesting trees used by Lilac-crowned Parrots. This number includes 26 nest cavities located from 1995 to 1998 and reported by Renton and Salinas-Melgoza (1999), though we did no spatial analysis on this data set.

Cavity reuse. We determined the frequency of cavity reuse over all years, though we did not include 13 new nest trees located in the final 2008 breeding season as potential reuse of these cavities is yet to be determined. Trees that fell or cavities taken over by bees were not counted as potentially available nest sites in successive years; however, we did not evaluate whether the internal condition of cavities remained suitable for nesting in a given year. In one case, three cavities in the same tree were used as nest sites in different years and were considered as reuse of the same nest tree.

Statistical Analyses

We used a chi-squared contingency table to evaluate the frequency of use as nest sites of the main tree species among the three nesting areas and to determine whether nest-site reuse was associated with the outcome of the previous nesting attempt. Individual identification of nesting pairs was not possible, hence we could not determine whether cavities were reused by the same or different pair of parrots.

Spatial-point-pattern analysis. We analyzed the spatial pattern of points by using the locations of all trees used as nest sites over the 14-year study. Each tree's location was considered only once for the analysis regardless of how many times the tree was reused as a nest site. We determined the spatial pattern of all nest trees in each of the three nesting areas over the duration of the study through a linearized transformation of Ripley's K function, L (r). This function offers a representation of changes in the spatial pattern over distance (Ripley 1977). The estimation of the points' pattern compares the distribution of the distance between pairs of all nest locations with an expected homogeneous Poisson process with complete spatial randomness (Ripley 1977). We used the software Programita (Wiegand and Moloney 2004) to detect spatial patterns. The patchy distribution of the semi-deciduous forest and stands of Piranhea mexicana within a matrix of deciduous forest create environmental heterogeneity with localized areas of different vegetation composition along streambeds that could affect the spatial pattern. Programita allows the analysis of point patterns while dealing with environmental heterogeneity by comparing the pattern observed with a heterogeneous Poisson process (Wiegand and Moloney 2004). Monte Carlo 95% confidence envelopes were created after 1000 simulations (Wiegand and Moloney 2004); deviation from that envelope indicates a significant departure from a random spatial distribution of trees used for nesting. Function values that fall above the upper envelope indicate a clustered spatial pattern of the trees used as nests. Values below the lower envelope indicate an overdispersed pattern of nest-tree distribution and could indicate competition for space. The use of this statistic offers the advantage of representing the spatial pattern over distance visually and detecting the distance over which spatial processes occur for a given area and time span.

In a second procedure, we evaluated spacing among simultaneously nesting pairs of parrots in a given breeding season by calculating the distance to the nearest neighboring active nest. In addition, for each tree used as a nest by parrots we calculated the distance to the nearest neighboring tree that had been used as a nest site. Where two active nests were nearest only to each other, giving a duplicate data point, we incorporated the distance value only once in statistical analyses. We then compared the nearest-neighbor distances between active nests in a given breeding season with the separation distance to the nearest nest tree to determine whether the spacing of breeding pairs differed from the distribution of all nest trees.

The Kolmogorov—Smirnov statistic indicated that the data did not conform to a normal distribution. Therefore, we applied the Mann—Whitney U test to compare distances between active breeding pairs with distances to the nearest potential nest tree for all years combined. Using a paired Wilcoxon test, we further evaluated the influence of conspecifics on the spacing of parrot nests to compare the distance to the nearest active nest vs. the distance to the nearest potential nest tree for each parrot nest active in the 2008 breeding season. We restricted this analysis to the 2008 data set, which had the most complete record of potential nest trees, to avoid overduplication of distance values between years.

To evaluate whether parrots tend to reuse nesting areas in subsequent years, even if they do not reuse the same nest site, we calculated the distance of an active nest at time t from the nearest nest site used in the previous year t - 1 (White et al. 2006). Where the same cavity was reused in a subsequent year we excluded this from the calculation of t - 1 distances. We did not include estimates of the nests' spacing in the study's first year, 1995, when corresponding distances to nests in a previous year were unobtainable. We then used Mann—Whitney U to compare distances between nesting Lilac-crowned Parrots of the current year (time t) with distances to the nearest tree used as a nest in the previous year (t - 1).

Finally, we used Kruskal—Wallis ANOVA to compare the three nesting areas with respect to distances of all trees used for nests and active parrot nests. Where a significant difference was detected, we conducted pairwise comparisons by using the Dunn multiple-comparison test for unequal sample sizes (Zar 1999) to determine which nesting area differed in separation distances. Descriptive statistics are presented as ranges and means with standard deviation, and we applied the P < 0.05 significance level in all statistical tests.

Results

Nesting Requirements

The main trees in which Lilac-crowned Parrots nested were Piranhea mexicana (47% of nest trees), Astronium graveolens (22%), and Tabebuia spp. (13%), accounting for 82% of all nesting trees. Cavities in dead trees (unknown species) accounted for 7% of nest trees, while other species used as nest sites were Caesalpinia sclerocarpa (3%), and Bursera simaruba, Gyrocarpus americanus, and Jatropha sp. (each 2%). One nest was in C. eriostachys, one in an unidentified tree. The three nesting areas differed significantly in the frequency with which the main tree species were used for nesting (χ²₆ = 27, P < 0.001). The use of tree species for nesting was narrowest at Careyes, as reflected in the large proportion of P. mexicana (72%) used as nest sites in this area (Fig. 2). At Chamela a greater proportion of parrot nests was in Tabebuia (35%), while at Cuixmala parrots used P. mexicana (41%) and A. graveolens (35%) as nest sites in equal proportion (Fig. 2). The nests were most frequently lined with wood chips (73%); other material used to line them included leaves (18%) and Tillandsia sp. hanging moss (9%). Nesting trees were located a mean 56 ± 49.5 m of streambeds (range 0.6–250.4 m, n = 94).

On average, any given cavity was used as a nest site 1.8 ± 1.3 times (range 1–7, n = 83) over the 14 years of study, with 35 nest trees used more than once (42% reuse of cavities). Most nest trees were used only once (58%, n = 48), while 22% of nest trees were used twice (n = 18), 12% (n = 10) were used three times, and 8% were used four to seven times (n = 7). Cavities in dead trees were reused most frequently (mean times reused = 2.4 ± 2.0, range 1–6, n = 7); cavities in living trees of Piranhea mexicana were reused second most frequently (mean times reused = 2.0 ± 1.3, range 1–7, n = 36). Reuse of cavities in Astronium graveolens (mean 1.7 ± 1.1, range 1–4, n = 19) and Tabebuia spp. (mean 1.7 ± 1.2, range 1–5, n = 12) was similar.

The 35 cavities reused as nests during the 14-year study period were used for an average duration of 4.9 ± 3.2 years (range 2–13 years) from the first to the last breeding attempt. The longest durations (>12 years) were all in cavities of Piranhea mexicana (n = 4), two of which were reused 6 and 7 times, respectively, over that period. Most instances of cavity reuse were in consecutive breeding seasons (n = 41 yearly reuse intervals), though the average interval between reuse of a cavity was 2 ± 2.1 years (n = 67 intervals). We noted 11 instances of cavity reuse with an interval of 2 years between use, five instances of reuse after a 3-year interval, and four instances of reuse after a 4-year interval. The longest intervals of 5 or more years between cavity reuse (range 5–11 years, n = 6), all involved nest-cavities in P. mexicana, including two cavities that were reused 11 years after first observed being used as a nest.

For 95 nesting attempts it was possible to determine the success (fledging at least one young) or failure of nests and whether these cavities were reused or not in a successive breeding season. The frequency of the parrots' reuse of cavities was associated with the outcome of previous nesting attempts (χ²₁ = 6.2, P < 0.02). Forty-one nesting attempts successfully fledged young, and parrots reused the nest cavity after 25 of these successful nesting attempts (61%). By comparison, 54 nesting attempts failed to fledge young, and the majority (65%) of these cavities were not reused as nests (n = 35).

Spatial-Point Pattern of Nest Trees

In all three nesting areas, the spatial-point pattern of the distribution of nest trees falls above the confidence intervals of a heterogeneous Poisson process for a distance of up to 60 m (Fig. 3), indicating that within this radius trees used as nests were significantly clustered. After this cut-off point, however, the spatial pattern of nest trees became a random process (Fig. 3).

Spacing Among Breeding Pairs

For all years combined, the distance to the nearest active nest was significantly greater than the distance between all trees used as nests (Table 1). Nesting pairs of the Lilac-crowned Parrot were separated by a mean 952 ± 891 m (range 30–5874 m, n = 106), while potential nest trees were a mean 241 ± 352 m apart (range 9–2420 m, n = 60). Furthermore, for nests located in 2008, the same pattern prevailed, a nesting pair being significantly farther from the nearest neighboring pair than from the nearest available nest tree (Table 1). Finally, the distance between conspecific nesting parrots was significantly greater than the distance to the nearest tree used as a nest in the previous year (Table 1).

There was also significant variation among the three nesting areas in the distances between the nearest active nests (H₂ = 27, P < 0.001). Distances between active nests were smaller at Careyes (Fig. 4) than at either Cuixmala (Q₃ = 4.8, P < 0.001) or Chamela (Q₃ = 3.8, P < 0.001). Distances between all nest trees followed the same trend of being shorter at Careyes (Fig. 4), though this difference was not significant (H₂ = 1.9, P = 0.39).

Discussion

Our analysis of nesting pattern of the Lilac-crowned Parrot over 14 years is the first quantitative analysis of the spatial distribution of nesting parrots. Lilac-crowned Parrots used primarily three tree species for nesting. Reuse of a nest cavity was significantly associated with a previously successful nesting attempt in that cavity, possibly indicating high-quality sites used more intensively by resident pairs. Finally, spatial-point-pattern analysis indicated that trees used for nesting were clustered at a small scale of 60 m, with close proximity between all trees used as nests, while breeding pairs of parrots tended to nest farther from another nesting pair.

Most of the Lilac-crowned Parrot nests were located in trees of Piranhea mexicana, Astronium graveolens, and Tabebuia spp. The predominant use of these species could reflect their propensity to form cavities large enough to host parrot nests, because of their characteristic tall, straight trunks (Pennington and Sarukhan 2005). The tree species used most frequently for nesting varied significantly at each site, however, reflecting the sites' differing habitat characteristics.

Cavity Reuse

The 42% cavity reuse by Lilac-crowned Parrots is higher than the average 33% cavity reuse reported for other psittacines (Koenig 2001, Fernandez-Seixas and Mourão 2002, Monterrubio-Rico et al. 2006) and higher than the 10% cavity reuse over 3 years previously reported for this species (Renton and Salinas-Melgoza 1999). However, our estimate of cavity reuse covers a longer time than most other studies, with an average 2-year interval between reuse of cavities and some cavities being reused after 4 or more years. This pattern of infrequent reuse of a cavity after a number of years of inactivity may reflect infrequent breeding by mated pairs (Murphy et al. 2003). Alternatively, it could represent a strategy to reduce parasite infestation of nest cavities (Stanback and Dervan 2001) or to prevent predators from learning the nest's location (Sonerud 1985). Cavity reuse being associated with a previously successful nesting attempt suggests that to increase fitness Lilac-crowned Parrots are actively reusing safer cavities. This in turn may indicate the existence of high-quality nest sites which are used more intensively by resident pairs.

Long-term reuse of nest sites could also be a reflection of philopatric offspring taking over parental nesting areas. Yearling parrots are reported sometimes to accompany parents when they return to the nest area in the subsequent breeding season (Snyder et al. 1987), from which they may learn to identify appropriate nest sites. In one case, a young male Lilac-crowned Parrot >1 year old, with an expired radio collar, was observed with an unmarked mate attempting to take over a nest cavity in an area already occupied by a nesting pair (Salinas-Melgoza and Renton 2007). It is unknown whether the radio-marked male may have been an offspring returning to its parents' nest area. This possibility is unlikely, however, as radio-telemetry studies of Lilac-crowned Parrots demonstrate that young parrots move progressively farther from the nest site after fledging (Salinas-Melgoza and Renton 2007). Furthermore, the family group breaks up 5 months after fledging, well before the onset of the next breeding season, and we have not recorded offspring returning to their natal nest area (Salinas-Melgoza and Renton 2007). Nevertheless, it is unknown whether young parrots develop a search image of an appropriate nest cavity on the basis of the cavity from which they fledged.

Influence of Intraspecific Spacing

Spatial-point-pattern analysis indicated that over a 60-m radius trees used as nest sites were significantly clumped, with nest trees separated by only 100–200 m, whereas in any given year a pair nested an average of 950 m from another nesting pair. This pattern indicates the influence of conspecifics in the spacing of nesting pairs of parrots, while the clustering of cavities used as nest sites suggests that each pair may attempt to maintain a nest territory with a locally high availability of nest cavities. This pattern of use of areas with a greater availability of cavities for nesting has been observed in the Puerto Rican Parrot (Amazona vittata) (Wiley 1985). However, the extent to which the same breeding pair of Lilac-crowned Parrots reuses nest trees or has fidelity to a nesting area is unknown. Fidelity to a nesting site is known in the Eclectus Parrot (Eclectus roratus), the Ouvéa Horned Parakeet (Eunymphicus cornutus uvaeensis), and the Puerto Rican Parrot, particularly when nest sites are limited (Robinet and Salas 1999, Heinsohn and Legge 2003, White et al. 2006). Genetic evidence indicates that a mated pair of the Yellow-naped Parrot (Amazona auropalliata) may maintain fidelity to a particular nest site for at least 7 years (T. Wright, pers. comm.), the cooperatively breeding Eclectus Parrot for 8 years (Heinsohn et al. 2007). The frequent reuse of a nest cavity over a number of years may indicate a breeding pair resident in the area. Conversely, the intermittent reuse of a cavity after 5 years, or even after an 11-year gap since the first nesting attempt, may indicate a new breeding pair occupying the nest area.

Even when Lilac-crowned Parrots do not reuse the same nest cavity, they tend to nest in the same area in the subsequent year, as reflected by the significantly shorter distances between nests in a single year to the nearest tree used as a nest in a previous year. This pattern may indicate that resident pairs maintain favored areas for nesting within which there are a number of options for cavities as nest sites. Alternatively, a parrot nest being located in a specific area of forest may serve as an indication to other parrots that the area is adequate for nesting, stimulating their use of this area in the subsequent year. There is evidence that psittacines attempt to preempt nest cavities well in advance of the breeding season, with macaws fighting over cavity ownership a year in advance of nesting (Renton 2004). In the case of the Lilac-crowned Parrot, the young male with an expired radio collar and its unmarked mate were observed over 3 or 4 years attempting to take over a nest cavity in an area already occupied by a nesting pair; the radio-collared bird eventually nesting in the area in 2005 and 2006 (Salinas-Melgoza and Renton 2007). Analysis of the parentage of nestlings from cavities within presumptive territories over several years could elucidate whether Lilac-crowned Parrots maintain breeding areas over time or whether there is turnover of breeding pairs.

Distances between the nearest active nests varied significantly among the three nesting areas, with parrots nesting significantly closer together at Careyes than in the other two areas. The Careyes area contains extensive monospecific patches of Piranhea mexicana. The density of cavity-bearing trees suitable for nesting by parrots in these monospecific stands may be higher (Martijena and Bullock 1994), permitting shorter distances between nesting pairs.

This difference between study sites in spacing of nests indicates that parrots may be flexible in the size of the area they defend around the nest. Hence it is likely that the clustering of nest trees is not an artifact of the spatial requirements of nesting parrots but rather that nesting pairs defend an area around the nest sufficient to provide them with multiple cavities suitable for nesting. In this study we considered only cavities the parrots used as nest sites; therefore, we may be confident that these represent available cavities the parrots considered acceptable. This conservative approach, however, may underestimate the total of cavities available in the defended area and surrounding habitat. A comprehensive survey of cavity availability to determine variations in cavity density by habitat may elucidate broader landscape effects on the nest-spacing patterns we observed.

Implications of Nesting and Spatial Requirements for Conservation

The nesting and spatial requirements of the Lilac-crowned Parrot suggest that management actions to increase the density of nesting pairs may be limited. Environmental heterogeneity in tropical dry forest means that nest trees suitable for the Lilac-crowned-Parrot are concentrated in patches of semi-deciduous forest and stands of Piranhea mexicana. The distance between active nests being greater than the distance between used cavities indicates that the behavior of Lilac-crowned Parrots limits the use of these clustered resources.

Furthermore, the proximity and aggregation within 60 m of trees used as nests, the shorter distances from an active nest to a tree used as a nest in the previous year, and the frequent reuse of successful nest cavities all suggest that breeding parrots maintain favored high-quality areas with good availability of cavities for nesting with a spacing of an average 1 km between active nests of other pairs. The nest-spacing pattern we observed could indicate that there is a finite number of nesting pairs able to coexist in the habitat suitable for nesting. Not all areas of forest may be equally rich in availability of adequate nest sites, leading to frequent reuse of favored areas and requiring large stands of semi-deciduous forest and P. mexicana to provide sufficient options for nest cavities and adequate spacing among nesting pairs. Hence both the concentration of cavities in habitat patches and the behavior of nesting pairs of parrots could be acting in synergy to influence the spatial distribution of Lilac-crowned Parrot nests.

The application of nest boxes as a strategy to increase the density of nesting pairs may also be limited by the birds' requirements for spacing. Hence the installation of nest boxes in forest areas already occupied by a reproductive pair of parrots is unlikely to result in an increased density of nesting parrots. This hypothesis could be tested through the implementation of a nest-box experiment to determine whether resident pairs may exclude potential breeders from occupying nest boxes. Furthermore, the location of nest boxes needs to take into account the specific habitat and nest-site requirements of nesting parrots. The spatial arrangement of nest boxes should simulate the spatial pattern observed for nesting parrots, with clusters of suitable cavities and adequate spacing between clusters. This distribution would provide a supply of adequate cavities within each nest territory while reducing competition for hollows with other nesting pairs.

Habitat modification outside the protected area is proceeding rapidly, and tropical dry forest is being transformed at a high rate (Masera et al. 1997, Trejo and Dirzo 2000). This change could imply a reduction of habitat with nest sites suitable for parrots, leading to increased competition between potential breeding pairs for nest sites within the reserve. Despite the existence of conserved habitat with a number of cavities available for nesting within the protected area, the capacity for an increase in density of nesting pairs of parrots within the reserve may be limited by the birds' behavioral requirements for space and their need for a number of available cavities within a given nesting area.

Acknowledgments

This long-term study would not have been possible without the consistent logistical and financial support of the Fundación Ecológica de Cuixmala, the World Parrot Trust, the Denver Zoological Foundation, and the Estación de Biología Chamela of the Instituto de Biología, Universidad Nacional Autónoma de México (UNAM). Scholarships were provided to AS-M by the Fundación Ecológica de Cuixmala (1998–2000), and a postgraduate grant from the Consejo Nacional de Ciencia y Tecnología (CONACyT) (20007ndash;2002). The Secretaria del Medio Ambiente y Recursos Naturales granted research permits. We thank A. Gutierrez, A. Miranda, R. Nuñez, and T. Sanchez for assistance with nest inspections. M. A. Salinas-Melgoza assisted with the spatial-point-pattern analysis. The Estación de Biología Chamela, Instituto de Biología, UNAM, and the Department of Biology, New Mexico State University, provided facilities for the preparation of this manuscript. We are grateful to J. R. Eberhard, E. Hobson, T. White, and T. Wright for their constructive comments that improved the manuscript.

Literature Cited