The importance of scale-dependent ravine characteristics on breeding-site selection by the Burrowing Parrot, Cyanoliseus patagonus

Study species

Cyanoliseus patagonus bloxami, Olson, 1995, is one of the four subspecies of Burrowing Parrots and is the only representative of the species in Chile. The Burrowing Parrot has suffered a clear reduction in its range since the early nineteenth century, mainly due to loss and degradation of its natural habitat, leading to the fragmentation of their populations (Galaz, 2005). Currently, C. patagonus bloxami is the most endangered subspecies and is divided into two isolated populations located north and south within central Chile. In Chile, the subspecies is classified as endangered to the populations of the north, and those of the south are classified as threatened. The main causes of its decline are habitat loss and poaching (Galaz, 2005; Vargas-Rodríguez & Squeo, 2014). The northernmost population inhabits a semi-desert ecosystem, while the southern population inhabits a Mediterranean habitat (Masello & Quillfeldt, 2012; Vargas-Rodríguez & Squeo, 2014). The northern population is known for living under extreme environmental conditions, where resource availability is scarce. Studies with other subspecies from Argentina have shown that resource availability (water and food) at nesting ravines influences population sizes of this species (Masello & Quillfeldt, 2012). The species has a very extensive home range, making long daily trips to different sites such as foraging areas, reproductive ravines, water bodies and roosting areas. For example, individuals can make daily trips from ravines to their feeding areas, moving an average distance of 40–60 km. Colonies are located close to water bodies and roosting areas, in which at sunset breeding colonies cluster to rest, are located away from reproductive ravines (Masello et al., 2006; Vargas-Rodríguez & Squeo, 2014). The burrowing parrots have a monogamous breeding system with intensive biparental care and high coloniality (Juniper & Parr, 2010). At a ravine, individual pairs excavate nests used in previous seasons enlarging them every year. Nests have an average depth of 1.5 m ending in an incubation chamber where eggs are laid on bare ground. Each nest is occupied by a single pair that lays between two to five eggs per season. The species is very sensitive to disturbance during the incubation period (Masello & Quillfeldt, 2004; Masello & Quillfeldt, 2012).

Study area

We conducted the study during the breeding seasons of 2013 and 2014 in northern Chile where the northernmost population of C. patagonus bloxami is located. This region is composed of an arid ecosystem dominated by xerophytic vegetation where fluvial ravines are positioned on the slopes located on both sides of creeks. We covered an area of ca. 1,300 km², within the first 54 km along the Andean foothills, covering the entire altitudinal range of the species (180–2,000 m) (Fig. 1). Mean annual precipitation is lower than 80 mm, and heavily influenced by ENSO events (Squeo et al., 2009).

Ravines can be classified as reproductive and non-reproductive depending on the presence of nests. In turn, reproductive ravines can be active or inactive, depending on the presence of individuals along a given breeding season. We quantified 12 variables in all ravines present in the study area (n = 105), which were accurately georeferenced (UTM WGS84). Seven of these variables were related to morphological and intrinsic characteristics of ravines: area, height, slope, orientation, type of substratum, geological origin and the nature of the ravine (origin geological or artificial of the ravine). Every ravine was photographed with its respective reference scale in order to calculate its area and maximum height (represented from the base of ravine to the highest point) using Photoshop. A compass was used to determine orientation and a clinometer to record the slope at the midpoint of every ravine. In order to evaluate the effect of the type of ravine, we determined the substrate based on its geomorphological and morphodynamic origin, in addition to the presence and size of rocks (Fairbridge, 1968; Huggett, 2003). Moreover, ravines were categorized depending on whether they were of natural origin (geological processes) or artificial origin (extraction of gravel by human activity).

Three of the variables analyzed were related to the presence and availability of resources in the study area. We estimated the distance to water bodies and roosting areas (protected valley bottoms with high densities of tall cactus where individuals perch) closest to each ravine using Google Earth as a proxy of the availability of these resources. Food availability was estimated based on the abundance of plant species that are the main food source of C. patagonus bloxami (e.g., Balsamocarpon brevifolium, Cordia decandra and Krameria cystoidea) (Vargas-Rodríguez & Squeo, 2014) in a radius of 50 m around each ravine. Abundance data of each plant species were summed to form a single value of food in the areas near the ravine. In addition, we calculated the distance from ravines to the nearest places with human disturbance (e.g., human settlements: settlements that house between one and five basic family houses of rural type that are dedicated to cattle raising; and roads: unpaved rural roads transited with medium and low frequency of vehicles) in order to evaluate the effect of landscape modification on nest-site selection. Finally, to evaluate the relationship between nest-site selection and fitness, we measured the number of nests and egg production (with or without eggs) for each reproductive ravine during both reproductive seasons.

Statistical analyses

To determine differences between non-reproductive and reproductive ravines and between active and inactive ravines in intrinsic and extrinsic variables, independent PERMANOVAs (Anderson & Walsh, 2013) were performed for both sets of ravines using 1,000 permutations for each comparison. We used all continuous variables in the analyses because none had a high degree of correlation (<r_s = 0.9) as indicated by independent spearman correlation tests. Subsequently, to graphically observe the interrelationship among variables that explain the difference between groups of ravines we performed non-metric multidimensional scaling (NMDS) using 9,999 permutations, based on a Euclidean distance matrix to preserve the ordering relationships among objects in the specified number of axes. This matrix results in a less deformed representation of the distance relationships among objects than other distance methods in the same number of dimensions (Borcard, Gillet & Legendre, 2011). To assess whether there was a significant relationship among the ordination axis scores and ravine characteristics and the percent of variance explained by each variable (R²), we used the envfit()-function with 9,999 permutations from the vegan package. Moreover, to determine if characteristics of active ravines are related to the number of nests, a generalized linear model (GLM) was performed using a Poisson distribution and a log-link function. The model included seven continuous variables that were relevant to the number of nests on a ravine (area, height, distance to water bodies, food availability, distance to roosts, distance to human settlements and distance to roads). In order to test for variable significance we conducted Likelihood Ratio Tests (LRT). In order to test if characteristics of active ravines are related to the probability of laying eggs at a ravine, a similar analysis, to the one mentioned above was conducted, except that the GLM model was performed using a Binomial distribution and a logit-link function with the variable with or without eggs as the response. All statistical analyses mentioned previously were performed using the R statistical environment ver. 2.15.3 (R Core Team, 2013). Finally, mean orientation angle was calculated as a measure of ravine orientation using circular statistics and homogeneity distribution based on a Rayleigh test (Zar, 1984). This analysis was performed using the software Oriana ver. 4. (Kovach, 2014).

Reproductive and non-reproductive ravine comparison

There are significant differences between non-reproductive and reproductive ravines in their intrinsic and extrinsic characteristics (F = 3.5, df = 1, p = 0.0049); however, we found no differences between reproductively active and reproductively inactive ravines (F = 1.35, df = 1, p = 0.26). Of the eleven variables considered in this analysis nine explained significant variance across the non-reproductive and reproductive ravine gradient (Table 1). The variables that explain variation are related to intrinsic morphological characteristics such as, area, substrate or geological origin and extrinsic variables associated to human disturbance, like distance to human settlements had the greatest explanatory power (Table 1). On average, reproductive ravines are larger, taller and have higher slope than non-reproductive ravines. In addition, they are closer to human settlements and roads (Table S1, Fig. 2).

The multidimensional environmental gradient of variation between ravines revealed by the NMDS shows that the height and area of the ravine and distance to roads and human settlements (urbanization) are the variables that generate the gradient across sites. Moreover, distance to human settlements explained most of the variation among ravines (Fig. 2). Although reproductive ravines tend to be closer to populated areas, differences with non-reproductive ravines are more in line with ravine size (height and the area) indicating that reproductive ravines are larger than non-reproductive ravines. The type of geological origin is highly dispersed throughout the environmental gradient, so its importance in differentiation between ravines is variable. Specific categories, however, are more present in reproductive that non-reproductive ravines. For example, cones of dejection (CD) are more common in reproductive ravines. These cones are alluvial fans with very steep slopes that are generally higher and narrower than a fan, and are composed of coarser and thicker material believed to have been deposited by large streams (Herrmann & Bucksch, 2013). Moreover, all sites in study area with alluvial terrace are active reproductive ravines (Fig. S1). Importantly, the ravines of anthropogenic origin (sand and gravel extraction) present in the area are used more frequently significantly (R² = 0.22, p = 0.001). The use of this type of ravines for reproduction reveals the adjustability of this species to human pressure. Food availability near reproductive ravines and distance to water bodies were less important for ravine selection.

Finally, we found that non-reproductive ravines have a uniform orientation along coordinate axes, while reproductive ravines (active and inactive) are non-uniformly orientated but with a significant directionality towards the south, with mean vector μ of 190° ± 79°. (Circular Standard Deviation (CSD)) (R = 5.79, p = 0.003) (Fig. 3). Reproductively active ravines are not homogeneously distributed around the southern axis (μ = 190°± 5° CDS, R = 10.54, p < 0.0001), while inactive ravines are homogeneously distributed although their orientation is non-significant (μ = 12 ± 94° CDS, R = 0.65, p = 0.53).

Reproductive success

Overall, the number of nests was significantly related to all the studied variables except for distance to roads (X² = 1.43, p = 0.2318), and distance to human settlements (X² = 2.83, p = 0.0927). Reproductive ravines with greater height have more nests (X² = 858.59, p < 0.0001). Those that have greater area (X² = 9.44, p = 0.0021), that have lower food availability (X² = 730.15, p < 0.0001), are closer to water bodies (X² = 69.37, p < 0.0001) and closer to roosting sites (X² = 242.68, p < 0.0001) also have more nests (Fig. 4). Finally, the probability of producing eggs for an active ravine was significant only with distance to roads (X² = 7.04, p = 0.0079) and human settlements ( X² = 6.80, p = 0.0091). Reproductive ravines have a greater probability to produce eggs if they are farther away from roads and closer to human settlements (Fig. 5).

Intrinsic morphological characteristics of reproductive ravines

The size of a ravine is a fundamental aspect for reproduction in colonies. Our study shows that from the available pool of ravines, burrowing parrots are selecting those that are larger and taller, which allow individuals to build their nests farther from the ground, probably as a response to terrestrial predation (Corrales et al., 2013). Our results also confirm that the largest ravines are the ones with the highest number of nests and egg production. These findings are consistent with a positive correlation previously found between ravine size and the number of breeding pairs (Tella et al., 2014). One of the reasons why the size of the wall plays a key role in the selection of reproductive ravines is that bigger ravines can host larger breeding colonies, increasing the benefits of group living by way of a dilution effect that reduces predation risk, increases detectability, and enhances deterrence more than smaller ravines Alcock, 2012. The adaptive advantage of group living has been demonstrated for gregarious species where a larger colony size increases the benefits it offers in terms of foraging efficiency and reduced predation risk (Lack, 1968; Wittenberger & Hunt, 1985; Sachs et al., 2007). In addition, there may be an association between a colonial nesting strategy, scarce in other Psittacidae, and reproductive ontogeny because lower predation rates allow greater brood development time compared to other similar parrots (Masello & Quillfeldt , 2002). Our study is the first to show that larger colonies have a higher reproductive success as observed in two consecutive seasons. Future studies should address if a higher reproductive success is also associated to the advantages of group life, and whether predation or foraging strategies changes across colonies of different sizes.

Physical soil characteristics of reproductive ravines are also crucial for burrowing birds (Heneberg & Simecek, 2004). The presence and distribution of certain substrates has been suggested as a driver of the presence of European burrowing birds because of the correlation between the distribution patterns of sediments and nesting areas (Wesolowski, 2007). Moreover, nest construction leads to high-energy expenditure that is conditional to the type of substrate in which construction takes place. Thus, particle size is essential given the “Heneberg compromise” which establishes a trade-off between tunnel stability (reasonable strength of substrate) and the ease of drilling (cohesion) and construction (Martin, Aitken & Wiebe, 2004; Smalley et al., 2013a). In this sense, our study shows that the type of substrate is a determining factor in the selection of reproductive ravines and the substrate more preferable is sand with stones of small size present in ninety percent of reproductive ravines. This type of substrate is predominant in ravines whose morphodynamic origin is colluvial deposits; however, most reproductive ravines with this material are present in cones of dejection (Fig. S1). This means that despite having a greater availability of ravines with a suitable substrate in the form of colluvial deposits, individuals prefer this type of substrate in cones of dejection. The combination of these features may provide a series of benefits not provided by deposits with different origin. Alluvial terraces are uncommon in the study area, there are only three formations and all are reproductively active and present a very fine sedimentary substrate composed of sand and clay in lesser proportion, which originates from sporadic heavy rainfall scenarios, slightly recurrent in this type of ecosystem (Cepeda, 2009).

Studies with burrowing bird species have determined a correlation between soil particle size and structure of the nest tunnel, where longest tunnels are formed by substrates with smaller particles positively affecting breeding success (Heneberg, 2009; Yuan et al., 2006). Substrates with low particle size confer tunnel stability, ease of excavation due to their metastable nature and allow gas movement. In addition, these optimal substrates must have low clay content (less than 10%) for good compaction (neither too strong nor too soft) in order to be resistant to penetration (Heneberg, 2009; Heneberg, 2013a; Smalley et al., 2013a; Smalley et al., 2013b). Studies at the specific substrate level are needed in Neotropical burrowing birds because nesting substrates have a different origin then those used by European burrowing birds, and could have other relevant physical characteristics not previously evaluated.

In cavity-nesters, nest selection is guided in part by the correlation between the resultant microclimate inside the nest and its orientation because the thermal stability provided by substrate characteristics and cavity orientation influences their reproductive success (Hooge, Stanback & Koenig, 1999; Wiebe, 2001; Ardia, Perez & Clotfelter, 2006; White, Brown & Collazo, 2006; Salaberria et al., 2014). Due to the arid environment in which C. patagonus bloxami is distributed, the choice of the ravine and the place of the cavity must be precise in order to maintain a stable microenvironment for proper brood development. Because this species is located in the southern hemisphere, north facing slopes (equatorial exposure), exhibit greater insolation than south facing slopes (polar exposure) that are usually less dry (Cepeda, 2009). In fact, the majority of reproductive ravines were located facing south (polar exposure), were shade is prevalent all day and where the temperature of the wall remains more stable compared to north facing walls (equatorial exposure). Therefore, ravines with equatorial exposure tend to be susceptible to reaching high temperatures because of the intense radiation that in turn makes them unviable for nesting. This explanation is in accord with the chosen directionality found in reproductive ravines (i.e., slopes of polar exposure). Furthermore, this directionality is most prevalent in reproductively active ravines. Choosing ravines with equatorial exposure usually ends in reproductive failure. For example, it is common for young inexperienced pairs to construct nests in ravines with non-optimal orientation. These ravines do not provide a stable microclimate and are unviable for brood development resulting in nest desertion. We have been able to observe such events in the field across seasons. After failed events, ravines are not used by the same breeding pair the following season. These nests represent a portion of those nests that are found on ravines that are not facing directly south. Similar results have been found in studies of forest excavators, where individuals nesting in warmer holes were more likely to be successful (Wiebe, 2001; Ardia, Perez & Clotfelter, 2006). An additional strategy in order to avoid high temperatures in this type of extreme dry ecosystem could be depth of the incubation chamber present in the cavity. Although deeper chambers would have lower incidence of radiation, there are other parameters that need to be taken into account, such as structural stability or gas exchange with outside (Wiebe & Swift, 2001). The burrowing parrot builds its nest forming one to three meter galleries that end in an incubation chamber without any substrate (Vargas-Rodríguez & Squeo, 2014). Depth variability may be associated to the external temperature of the ravine or to its degree of isolation. Further evaluation of the influence of nest orientation and gallery length on the thermal variation within the incubation chamber and its influence on fitness is merited.

Extrinsic ravine characteristics (landscape level)

Our results show that the presence of anthropogenic elements within the landscape significantly influences the selection of reproductive ravines at a large scale. For example, ravines with the highest number of nests tend to be closer to roads and human settlements, although only ravines with greater reproductive success (i.e., more eggs production) are closer to human settlements. This inconsistency in the pattern can be explained by the topographical relief of the area, which makes proximity to human elements unavoidable. Reproductive ravines have a fluvial origin and therefore, tend to be located within small canyons that also run along orographic elements where roads that lead into the Andean foothills have been constructed. Therefore, proximity to roads and human settlements is unavoidable in most cases. The overlap of human influence and reproductive ravines could have important consequences for the viability and continuity of reproductive colonies. There are numerous studies that address the effects of human perturbation on nesting success in this species (e.g., Masello & Quillfeldt, 2002; Masello & Quillfeldt, 2004). They report that human disturbance negatively influences nest success, especially during the incubation period and the first week after hatching, with effects that can lead to abandonment of the nest. Other studies, however, show that there is a high inter-individual variability in the fear against humans and thus, a large potential for dealing well with an anthropic disturbance event as described for other species (Carrete & Tella, 2011). In fact, in this study we report that C. patagonus bloxami has the ability to use artificial ravines for reproduction; moreover, all artificial reproductive ravines produced eggs. Therefore, newly created ravines are being exploited by the colonies, and these ravines may contain malleable and suitable substrates for nesting. This has also been reported in Argentina where large nesting colonies are located in urban centers that provide artificial ravines (pits or quarries) (Masello et al., 2011; Tella et al., 2014). This type of behavior has been referred to as an innovation for the species.

The fact that food is not a significant variable indicates that the presence of items near ravines is not relevant for choosing them as sites for reproduction. Disposition of the colony in space is not related to the proximity to the food, which was also observed in other digging birds, where there was no relation between colony size and food availability (Hoi, Kristofik & Darolov, 2015). This pattern is in accord with previous studies on this species in Argentina and Chile, where foraging groups are able to move between 40 km and 60 km one to four times a day from the ravine to foraging areas (Masello & Quillfeldt, 2012; Vargas-Rodríguez & Squeo, 2014). Nevertheless the proximity of water to ravines is key for site-selection. Water bodies are places that not only provide water, but that also act as meeting places for the different colonies. The arid conditions around the habitat makes the availability of natural watersheds scarce or absent in some areas. Therefore, colonies in the area depend entirely on water that is available near human settlements. This foraging behavior is common in the area, where individuals use water sources daily (Vargas-Rodríguez & Squeo, 2014). This could in part explain why ravines with more egg production are closer to human settlements.

Because initially parrots selected ravines for reproduction following the criteria identified in this study, active and inactive ravines should have similar characteristics explaining the lack of significant differences between reproductively active and inactive ravines. Their subsequent inactivity may be due to factors not evaluated in our study, such as predation, competition or by the population decline that has suffered. Subsequent ravine inactivity may be an exploratory phenomenon of juvenile pairs as described above. We have observed the formation of a new active ravine composed of a single pair on a wall of small size, polar exposure and located at the edge of a busy road. The couple incubated two eggs but broods did not survive. The following year, the couple did not return to the nest. Similar behavior has also been reported by Tella et al. (2014) and reported for facultative colonial birds, where solitary pairs can colonize new nesting sites and establishes a new colony.