Study Area

We conducted the study in a 56-km² region of Los Chimalapas in northeastern Oaxaca, Mexico, comprising three main areas of Chalchijapa (17° 03′ 15″N; 94° 39′ 23″W), San Antonio Nuevo Paraíso (17° 09′ 38″N; 94° 21′ 9″W), and La Fortaleza (17° 09′ 32.2″N; 94° 13′ 45.3″W) within the municipality of Santa Maria Chimalapa. Mean annual temperature in the region is 22℃ to 26℃, with high annual rainfall of 2,000 to 4,500 mm, presenting a short dry season from March to June (Trejo, 2004). The dominant vegetation in the region is tropical moist forest, comprised of primary evergreen forest that covers 45.7% of the landscape (Martínez-Pacheco, 2012), with common tree species of Dialium guianense, Terminalia amazonia, Brosimum alicastrum, and Cojoba arborea (Rzedowski, 2006; Torres Colín, 2004). Riparian forest occurs along permanent rivers, with common tree species of Ficus sp., Garcinia macrophylla, Vochysia guatemalensis, and Inga vera (Torres Colín, 2004). Nevertheless, in Santa Maria Chimalapa over the last few decades, a total of 2,046.8 km² of primary tropical evergreen forest has been degraded, with a current rate of loss of 5.8% of primary forest per year (Martínez-Pacheco, 2012), mainly due to increased cattle-grazing and selective logging. This contrasts with the 6.8% increase in secondary forest recorded in the region from 2000 to 2003 (Martínez-Pacheco, 2012). Research permits for the study were provided by the Secretaria del Medio Ambiente y Recursos Naturales in Mexico.

Nest-Site Characteristics

We located nests of the Northern Mealy Amazon during the months of February to May over four consecutive breeding seasons in 2013 to 2016, by observation of the behavior of nesting pairs, and with the assistance of local guides. We used single-rope tree-ascending techniques (Houle, Chapman, & Vickery, 2004; Perry & Williams, 1981) to confirm nesting activity by the presence of eggs or chicks in the nest and take measurements of the nest cavity. For each nest-tree located, we recorded tree species, diameter at breast height (dbh), condition (live or dead), and GPS location. We also noted cavity origin as formed by decay processes (decayed) or excavated by primary cavity-nesters (Aitken & Martin, 2007). Finally, we measured cavity characteristics of height from the ground, entrance width and length, cavity depth, internal diameter, and diameter of the supporting structure (trunk or branch) where the cavity was located (Cockle, Martin, & Wiebe, 2008).

We located a total of 48 Northern Mealy Amazon nests in 40 distinct nest-trees, where 8 nest-trees were reused by parrots between seasons. However, we considered only individual nest-trees as the nest-site for all analyses. Of the 40 nest-trees, 11 occurred in primary forest (evergreen = 9 nest-trees, riparian = 2 nest-trees), with an additional 17 nest-sites located in remnant trees in areas cleared for cattle grazing at the edge of primary forest, and 12 nest-trees occurred in secondary forest.

Cavity Availability

To determine the availability of tree-cavities in tropical moist forest, we established 24 1-ha survey plots (100 × 100 m) distributed among the three study areas, with 9 tree-cavity survey plots in evergreen forest, 7 in riparian, and 8 in secondary forest. In each survey plot, we conducted an intensive search for cavities inspecting all trees with 10 × 40 binoculars. On locating a tree-cavity, we measured the same variables as for the parrot nests. We used a 15 -m extendible tree-measuring pole to measure cavity height from the ground and entrance length. A 50-cm length, horizontal plastic tube, with 1 cm graduated markings, was attached to the top of the tree-measuring pole to measure cavity entrance width and internal diameter. Finally, we used a weighted fishing-line that passed through the top of the tree-measuring pole to determine cavity depth by the length the line descended within the cavity (Vázquez & Renton, 2015). This enabled us to measure the dimensions of the majority of cavities; however, for 10 cavities >16 m above the ground, we used a digital dendrometer (Criterion RD 1000) to estimate cavity height, entrance width and length, and support diameter (Cockle et al., 2010) but were unable to measure internal diameter and depth of these cavities.

To be comparable with other studies of tree-cavity availability in tropical forests, we measured all tree-cavities with ≥2 cm entrance diameter and ≥8 cm cavity depth (Cockle et al., 2008). However, we defined a cavity as available for use by parrots based on measurements (Saunders, Smith, & Rowley, 1982) of five specimens of the Northern Mealy Amazon collected in Mexico and located in the Colección Nacional de Aves of the Instituto de Biología at Universidad Nacional Autónoma de Mexico in Mexico City. These Northern Mealy Amazon specimens had a mean diameter at the widest point (shoulder-to-shoulder) of 10.2 ± 1.2 cm (range 8.9–11.5 cm, n = 5), with a breast-to-back measurement of mean 7.5 ± 0.2 cm (range 7.3–7.8 cm, n = 5). Therefore, it is unlikely that Northern Mealy Amazons could enter a cavity with an entrance diameter less than 7 cm, and we considered as available to parrots only cavities with ≥7.0 cm entrance diameter. We also estimated the density of cavities suitable for nesting by Northern Mealy Amazons considering the minimum characteristics of cavities used as nest-sites by parrots.

Statistical Analyses

Although we measured all tree-cavities found in survey plots, we conducted statistical analysis only on cavities accessible to parrots (entrance diameter ≥7 cm) that were considered as available for parrots. Kolmogorov–Smirnov analysis of normality determined that data on tree dbh, cavity height above the ground, entrance width, and internal diameter had a normal distribution. Therefore, we applied one-way analysis of variance (ANOVA) to compare these characteristics of available cavities among the three vegetation types of evergreen, riparian, and secondary forest. Data on number of available cavities in each survey plot, cavity entrance length, cavity depth, and support diameter did not present a normal distribution; therefore, we applied Kruskal–Wallis ANOVAs to compare these characteristics of available cavities among vegetation types. We conducted Tukey post hoc analyses for one-way ANOVAs and Dunn post hoc analyses for Kruskal–Wallis ANOVAs (Zar, 1999).

We calculated the standardized Levins’ (1968) niche breadth index for tree species used as nest-sites by Northern Mealy Amazons, where a value close to 0 indicates that nesting is concentrated on only a few tree species, whereas a value close to 1 indicates a broad use of tree species as nest-sites (Colwell & Futuyma, 1971). We also applied G-test to determine whether use of tree species as nest-sites by the Northern Mealy Amazon corresponded to the availability of accessible cavities in each tree species. Finally, we generated simultaneous confidence intervals with Bonferroni adjusted alpha for the proportional use of each tree species as a nest-site (Byers, Steinhorst, & Krausman, 1984; Nue, Byers, & Peek, 1974). Use of a tree species as a nest-site is considered significantly different when the expected proportion of use based on availability falls outside the confidence interval of observed use (Byers et al., 1984).

We first compared characteristics of Northern Mealy Amazon nest-sites among vegetation types in the modified landscape using one-way ANOVAs with Tukey post hoc comparisons for nest-tree dbh, entrance length, cavity depth, internal diameter, and support diameter, and applied Kruskal–Wallis ANOVAs with Dunn post hoc comparisons for cavity height and entrance width. We determined no significant differences in nest-site characteristics and therefore combined nest-site data in comparisons with available cavities. Combined data did not present a normal distribution; therefore, to determine whether Northern Mealy Amazons selected nest-sites based on cavity characteristics, we used Mann–Whitney U test to compare characteristics of cavities used as nests by parrots with those of all available cavities (entrance diameter ≥7.0 cm) recorded in survey plots.

Finally, we applied multiple logistic regression to determine whether cavity characteristics predicted use of a cavity as a nest-site by Northern Mealy Amazons (nest = 1, available cavity = 0). As cavity entrance diameter would limit access by parrots and potential predators, we considered the smallest entrance dimension (length or width) for multiple logistic regression, although in 95% of cases, the smallest diameter was entrance width. Support diameter was strongly correlated with internal cavity diameter (r = 0.82, p < 0.001); therefore, we excluded the variable of support diameter from the initial logistic regression model. We used the Wald statistic (Quinn & Keough, 2002) to determine which variable (tree dbh, cavity height, smallest entrance diameter, cavity depth, and internal cavity diameter) predicted selection of a cavity as a nest-site by the Northern Mealy Amazon. We also evaluated the odds ratio and the inflection point of the probability curve for significant variables to determine the value above which there is a greater than 50% probability that a cavity would be selected as a nest-site by parrots. Descriptive statistics are presented as mean values with standard deviation, and we considered a value of p = .05 as significantly different for statistical analyses.

Nest-Site Characteristics

The 40 Northern Mealy Amazon nest-trees comprised 13 tree species (Figure 1), although parrots exhibited a narrow 0.39 niche-breadth of tree species used for nesting with over half of all Northern Mealy Amazon nest-sites occurring in live trees of T. amazonia (32.5%; n = 13 nest-trees), and D. guianense (20%; n = 8 nest-trees). The majority of nest-sites occurred in cavities in live trees (75%; n = 30), located either on the main trunk or secondary branch (50%; n = 20 in both cases), and all were formed by decay processes. Overall, Northern Mealy Amazon nest-sites occurred in large trees with mean 101.1 ± 28.6 cm dbh (range 50–184 cm), in cavities located 18 ± 5.1 m above the ground (range 8.1–29.5 m), with a wide 23.5 ± 12.7 cm entrance diameter (range 8–73 cm), and large 45.5 ± 17.6 cm internal diameter (range 14–81 cm), that were on average about a meter deep (mean 93 ± 65.1 cm; range 5–280 cm; Table 1).

Figure 1.

Proportion of tree species used as nests by the Northern Mealy Amazon (Amazona guatemalae), and available cavities (entrance ≥7 cm) in each tree species in the tropical moist forest of Los Chimalapas, Oaxaca. *Expected proportion based on availability falls outside the confidence intervals for observed use of each tree species.

Table 1.

Characteristics (mean ± SD) of tree-cavities used as nests by the Northern Mealy Amazon (Amazona guatemalae) and all available cavities (≥7.0 cm entrance diameter) in tropical moist forest of Los Chimalapas, Mexico, with Mann-Whitney U test of significance.

Tree-Cavity Availability

We recorded a total of 57 cavities in 24 ha of tropical moist forest; however, two cavities had entrance diameters <7 cm and therefore were not available for use by parrots. Of the 55 available cavities, 30 were located in primary evergreen forest, 15 in primary riparian forest, and 10 in secondary forest. The majority of available cavities were formed by decay (85.5%; n = 47) and occurred in live trees (78.2%; n = 43), with most cavities located on the main trunk (77.8%; n = 35).

There was an overall density of 2.3 cavities/ha available for use by Northern Mealy Amazons in tropical moist forest, but number of available cavities per survey plot differed significantly among vegetation types (Table 2). In particular, survey plots in primary evergreen forest had significantly more cavities than survey plots in secondary forest (q = 2.8, p < .01). Furthermore, cavities in secondary forest occurred in significantly smaller trees compared with cavities in primary evergreen (tree dbh: q = 3.5, p < .05) and riparian forest (tree dbh: q = 4.5, p < .01; support diameter: q = 2.6, p < .01; Table 2). Cavities in secondary forest also had smaller entrance dimensions than cavities in primary riparian forest (entrance length: q = 2.4, p < .02; Table 2).

Table 2.

Mean (± SD) characteristics of cavities available for the Northern Mealy Amazon (≥7 cm entrance diameter) in three forest types at Los Chimalapas, Mexico, with parametric (one-way ANOVA) and non-parametric (Kruskal-Wallis ANOVA) test of significance. Letters indicate significantly different post hoc pairwise comparisons among forest types.

Only 38 cavities had characteristics within the range of those used as nest-sites by Northern Mealy Amazons (height above the ground ≥8.1 m, entrance diameter ≥8 cm, internal diameter ≥14 cm, and depth ≥5 cm), giving an overall density of 1.6 cavities/ha with characteristics suitable for nesting by Northern Mealy Amazons. These suitable cavities were concentrated in primary evergreen (2.1 suitable cavities/ha) and riparian forest (1.9 suitable cavities/ha), with only 0.75 suitable cavities/ha in secondary forest.

Nest-Site Selection by Northern Mealy Amazons

Overall, the use of tree species as nest-sites by Northern Mealy Amazons did not differ significantly from that expected by the availability of accessible cavities in those tree species (G₁₂ = 15.5, p = .23). Only in the case of Ficus sp. and Poulsenia armata, Northern Mealy Amazons used these tree species as nest-sites less than may be expected by their cavity availability (Figure 1). However, in both cases, the expected proportion only marginally fell outside the confidence intervals (CI) for the observed proportion of use (Ficus sp.: expected = 0.18, observed CI = [0, 0.15]; P. armata: expected = 0.12, observed CI = [0, 0.10]).

On the other hand, use and availability comparisons determined that Northern Mealy Amazons selected nest-sites based on cavity characteristics. Univariate analyses found significant differences in each cavity characteristic variable between cavities used as nests by Northern Mealy Amazons and available cavities (Table 1). Cavities used as nests by Northern Mealy Amazons occurred in significantly larger trees, at a greater height above the ground, and with larger internal diameter, and greater depth than most of the cavities available for parrots (Table 1). These variables were significantly different even after Bonferroni alpha adjustment to p < .007.

The multiple logistic regression model determined that cavity characteristics explained nest-site use by parrots, where cavity depth (Wald X²₁ = 3.9, p = .047), and internal diameter (Wald X²₁ = 5.2, p = .022) significantly predicted selection of a cavity as a nest-site by the Northern Mealy Amazon. The odds that a cavity would be selected as a nest were raised by 1.4 for each increase in internal diameter and 1.1 for each increase in cavity depth. Calculation of the inflection point for the probability curve demonstrated that a cavity had a greater than 50% chance of being selected as a nest-site if this had >29.5 cm internal diameter and was >45.9 cm deep.

Nest-Site Requirements of the Northern Mealy Amazon

The Northern Mealy Amazon nested in a variety of tree species in Los Chimalapas, Mexico, but demonstrated a narrow niche-breadth of nesting tree species, using predominantly nest-cavities in live trees of T. amazonia and D. guianense. This is similar to the variety of 22 tree species used as nest-sites by the Northern Mealy Amazon in the Petén of Guatemala, where T. amazonia was also the tree species most frequently used for nesting (Bjork, 2004). Other species of Psittaciformes also use predominantly one to three tree species for nesting (Cameron, 2006; de la Parra-Martínez et al., 2015; Monterrubio-Rico, Ortega-Rodríguez, Marín-Togo, Salinas-Melgoza, & Renton, 2009; Renton & Brightsmith, 2009; Renton et al., 2015; Robinet & Salas, 1999; Symes & Perrin, 2004). However, although Northern Mealy Amazons nested most frequently in cavities in T. amazonia and D. guianense, they used these tree species for nesting according to their availability of cavities for parrots. This is similar to the Yellow-crowned Amazon (Amazona ochrocephala) in Panama, which uses tree species for nesting according to the availability of cavities in those trees (Rodríguez Castillo & Eberhard, 2006), but contrasts with the large Military Macaw (Ara militaris), which selects large emergent tree species for nesting (de la Parra-Martínez et al., 2015).

Nevertheless, Northern Mealy Amazons used cavities in Ficus sp. and P. armata slightly less than may be expected by the availability of cavities in these trees. Similarly, the Northern Mealy Amazon in Guatemala rarely used these tree species as nest-sites (Bjork 2004). Both these species are softwood trees in the Moraceae family of latex producing plants (Pennington & Sarukhan, 1998) and may have structural properties that make them less desirable as a nest-site. The Blue-fronted Parrot (Amazona aestiva) was more likely to reuse deep cavities with thick walls (Berkunsky & Reboreda, 2009), and cavities in large, living trees with thick walls tend to maintain more stable temperatures (Maziarz & Wesołowski, 2013; Wiebe, 2001), although microclimatic condition of cavities does not have a large effect on reproductive output (Wiebe, 2001). Nevertheless, we did not evaluate the internal condition of available cavities; therefore, there may be other microclimatic factors making cavities less suitable for use as a nest-site by the Northern Mealy Amazon.

We found that the Northern Mealy Amazon used nest-cavities in large trees of mean 1 m dbh, at a mean 18 m height above the ground, with large mean 23.5 cm entrance diameter, and mean 45.5 cm internal diameter, that were of mean 93 cm deep. Characteristics of nest-sites did not vary among primary and secondary forest or in pastures at the forest edge, as Northern Mealy Amazon nests generally occurred in remnant canopy trees characteristic of primary forest. Most Amazon parrots use nest-cavities of a lower mean height and of smaller mean entrance and internal diameters (Berkunsky & Reboreda, 2009; Enkerlin-Hoeflich, 1995; Renton & Salinas-Melgoza, 1999; Rivera, Politi, & Bucher, 2012; Rodríguez Castillo & Eberhard, 2006; Snyder et al., 1987) than that found for the Northern Mealy Amazon in our study. In fact, the mean nest-site characteristics of tree dbh, height above the ground, entrance diameter, and internal diameter place the Northern Mealy Amazon among the upper quartile of species of Psittaciformes that require large nest-cavities, located high above the ground in large, mature canopy trees (Renton et al., 2015). In particular, the large entrance and internal diameters of Northern Mealy Amazon nests were more similar to those used by large macaws and cockatoos (Berkunsky et al., 2014; Heinsohn, Murphy, & Legge, 2003; Olah, Vigo, Heinsohn, & Brightsmith, 2014; Saunders, Mawson, & Dawson, 2014). Indeed, only about 10% of studied Psittaciformes used nest-cavities with larger mean entrance and internal diameters (Renton et al., 2015). The Northern Mealy Amazon may need to use large nest-cavities to contain the brood. However, the use of nest-cavities with large entrance diameters may permit access by a greater variety of predators, increasing the risks of nest predation for the Northern Mealy Amazon.

Nest-Site Selection by the Northern Mealy Amazon

As found for other parrot species (Renton et al., 2015), the Northern Mealy Amazon selected nest-sites based on cavity dimensions. Parrots selected as nest-sites cavities in larger trees, at a greater height above the ground, and with larger entrance and internal diameters, and greater depth, from the resource of cavities available to them in the landscape. Height of the cavity entrance from the ground is an important criterion for nest-site selection for many cavity-nesting birds (Cockle et al., 2011; Li & Martin, 1991; Nilsson, 1984) and is a key factor influencing predation rate of nests (Li & Martin, 1991; Nilsson, 1984; Wilcove, 1985). Furthermore, cavity height above the ground is a significant predictor of nest success for some parrot species (Berkunsky & Reboreda, 2009; Cockle et al., 2015). Hence, the selection of nest-cavities high above the ground by the Northern Mealy Amazon may be a strategy to reduce predation risk and increase the probability of nest success.

In particular, cavity depth and internal diameter predicted selection of a cavity as a nest-site by the Northern Mealy Amazon. Cavity depth was found to influence nest success of the Eclectus Parrot (Eclectus roratus), with deeper nests producing a greater number of fledglings (Heinsohn, 2008). The importance of internal diameter of the cavity as a criterion predicting nest-site selection may reflect the requirement for a large nest chamber able to accommodate the nest contents for this large-bodied parrot. The Northern Mealy Amazon is the largest Amazon parrot in continental America, only exceeded in size by two Caribbean island parrot species (Forshaw, 1989). Internal diameter of the nest-cavity was found to significantly influence hatching success of the Scarlet Macaw (Ara macao) in Peru, with eggs more likely to hatch in nests with larger internal diameters (Olah et al., 2014). Therefore, the selection of deep cavities with larger internal diameters may increase the probability of nest-success and reproductive output for large-bodied parrots such as the Northern Mealy Amazon.

Cavity Availability for Northern Mealy Amazons

As found for other tropical forests (Cockle, Martin, & Wesołowski, 2011; Vázquez & Renton, 2015), the majority of tree-cavities in the tropical moist forest of Los Chimalapas were formed by decay processes. We found a low overall density of 2.4 cavities/ha in the tropical moist forest of Los Chimalapas, with 2.3 cavities/ha available for Northern Mealy Amazons. Even considering just conserved evergreen and riparian forest, there were only 2.9 cavities/ha (2.8 available cavities/ha). This is much lower than cavity densities recorded in other tropical moist forests of continental America, ranging from 16.8 to 111.7 cavities/ha (Boyle et al., 2008; Saunders et al., 1982), with a density of 4.5 cavities/ha suitable for nesting by birds (Cockle et al., 2010).

Furthermore, in Los Chimalapas, only 1.6 cavities/ha had characteristics suitable for nesting by Northern Mealy Amazons. Studies of smaller bodied Amazon parrot species have found higher densities of 4.6 to 11.3 suitable cavities/ha (Rivera et al., 2012; Snyder et al., 1987). Only in the case of large-bodied macaws or cockatoos have lower densities of 0.3 to 0.7 suitable cavities/ha been recorded (de la Parra-Martínez et al., 2015; Marsden & Pilgrim, 2003; Walker, Cahill, & Marsden, 2005). This low density of tree-cavities suitable for nesting by the Northern Mealy Amazon may be a limiting factor on the number of nesting pairs, creating competition for nest-sites (Heinsohn et al., 2003; Newton, 1994). During the present study, we observed agonistic interactions among four pairs of Northern Mealy Amazons for occupancy of a suitable nest-cavity. Interspecific competition may also limit the availability of nest-cavities for the Northern Mealy Amazon as during the parrot nesting seasons of 2014 to 2016, we found potential nest-cavities occupied by other secondary cavity-nesters, including the Guatemalan Screech Owl (Megascops guatemalae), Bat Falcon (Falco rufigularis), Keel-billed Toucan (Ramphastos sulfuratus), and Kinkajou (Potus flavus).

We found the lowest density of 1.3 available cavities/ha in secondary forest, where only 0.75 cavities/ha were suitable for nesting by Northern Mealy Amazons. Other studies have also found a generally low density of 0.5 to 1.64 cavities/ha suitable for birds in disturbed or human-managed forests (Cockle et al., 2008, 2010; Politi et al., 2010). As determined in the present study, available tree-cavities in secondary forest occurred in smaller trees and had smaller dimensions than in primary forest. Therefore, the increasing transformation of primary tropical moist forest to secondary forest (de Jong et al., 2010) is likely to have consequences in reducing the availability of suitable nest-sites for large-bodied secondary cavity-nesters. Furthermore, as highlighted by Marsden and Pilgrim (2003), long-lived parrots may be able to utilize food resources in disturbed or managed forests, but the reduction in density of suitable nest-sites in modified forests puts at risk the persistence of wild populations in the long-term.