INTRODUCTION

Parental care includes the group of behaviors performed by parents aimed at increasing offspring survival and, thus, parents' biological fitness (Clutton-Brock 1991, Royle et al. 2012, Mock 2022). In birds, parental care can have strong effects on reproductive parameters, which influence population dynamics and demography at a local scale (Newton 1998, Mock 2022). Parental care includes activities such as nest building, incubation, rearing of nestlings (provisioning and feeding), brooding and shading, nest defense, and partner-feeding (Clutton-Brock 1991, Mock 2022). Although most aspects of parental care in birds are usually performed by both members of a breeding pair, effort and activities differ between males and females in some species (Cockburn 2006, Webb et al. 2010). Equal sharing of parental duties (biparental care) is usually associated with monogamy (Lack 1968), and the absence of either color or size dimorphism (Remeš et al. 2015).

Among raptors, sex-specific division of parental care is often associated with the degree of sexual size dimorphism. Species with dramatic sexual size dimorphism usually exhibit the most extreme division of parental duties (i.e., the female incubates the eggs and broods and feeds the offspring, while the male provides the food; Remeš et al. 2015, Keeley and Bechard 2017). In contrast, among raptors exhibiting slight or no sexual size dimorphism, the division of parental care duties is often minimal (Margalida and Bertran 2000, Margalida et al. 2007, Rollack et al. 2013). Biparental care is predicted to occur when extensive care by both parents is necessary for successful rearing of young (Margalida and Bertran 2000) and when food is spatially and temporally unpredictable, as is the case for avian scavengers (Newton 1979, Margalida and Bertran 2000).

Parental care activities may vary during the 24-hr cycle and across the breeding season, and/or according to clutch size, brood size, and nestling age (Clutton-Brock 1991, Tinbergen and Williams 2002, Coe et al. 2015). For example, incubation, a key behavior that affects offspring survival, is influenced by environmental temperature (Nord and Nilsson 2016). Parents regulate egg temperature to optimize embryonic development and to ensure hatching (Haftorn 1988). Incubation behavior may differ during the 24-hr cycle due to changes in environmental temperature (Tinbergen and Williams 2002, Zuberogoitia et al. 2018) or predation risk (Fontaine and Martin 2006). Similarly, during the early nestling period, when nestlings cannot thermoregulate, parents adjust nest attentiveness behaviors such as brooding and/or shading in response to heat or cold stress (Coe et al. 2015, Clauser and McRae 2017). Additionally, parents may adjust feeding behaviors to the number and age of the nestlings (Collopy 1984, Clutton-Brock 1991). The energetic needs of nestlings change throughout their growth period, increasing until asymptotic growth has been reached and declining thereafter (Ricklefs 1968, Holthuijzen 1990).

Avian scavengers (e.g., vultures and some eagles) often exhibit minimal dimorphism and biparental care (Bassi et al. 2017, Morant Etxebarria et al. 2019). Understanding factors that influence parental care behaviors in avian scavengers should enhance our comprehension of their breeding biology. We studied parental care in the Chimango Caracara (Milvago chimango, hereafter chimango), an excellent model species because it is a generalist raptor/scavenger that shows minimal sexual-size dimorphism and is common across its geographic range (Solaro and Sarasola 2018, 2023). To date, no studies have examined parental care in the chimango; thus, our specific objectives were to (1) describe nest-focused parental care across the incubation and nestling periods, (2) quantify possible sex-related differences in parental care behaviors, (3) examine whether parental care behaviors differ according to time of day, clutch or brood size, or nestlings' age, and (4) assess the influence of parental care behaviors on nest success and productivity.

METHODS

Study Area. We studied parental care behaviors at a breeding colony of Chimango Caracaras located in a 0.5 km² suburban residential area (La Cuesta del Sur; 36°43′S, 64°16′W) in La Pampa Province, Argentina. The colony consisted of approximately 80–90 nests each year (Solaro and Sarasola 2018, 2023). This suburban area has intense pedestrian and vehicular traffic, and the yards are characterized by small grass plots with native species such as caldén (Neltuma caldenia), molle (Schinus fasciculatus), and chañar (Geoffroea decorticans), and exotic species such as eucalyptus (Eucalyptus spp.) and pine (Pinus spp.). Situated in an ecotone between the Pampas (grasslands) and the Espinal (rough pastures, thorny bush and caldén forests) ecoregions, this area experiences hot and wet summers and cold and dry winters (Cabrera 1976). Average annual temperature and precipitation are 16°C and 600 mm, respectively. Sunrise during summer occurs between 0600–0630 H and sunset occurs between 2015–2045 H.

Study Species. The Chimango Caracara is one of the most abundant and common raptors in southern South America (Bierregaard et al. 2022). This generalist predator and facultative scavenger nests in a wide variety of habitats and exhibits little sexual size dimorphism, with females being only 10–20 g heavier (3–6%) than males (Solaro and Sarasola 2018, 2023). However, adult males and females are easily distinguished by sexual dichromatism of the exposed skin: the tarsi and cere are yellow in males and bluish and pinkish, respectively, in females (Sarasola et al. 2011). In central Argentina, chimangos lay 2–3 eggs in October, which are incubated for 26–32 d, starting with the first egg, and nestlings fledge at 32–41 d during December and January (Solaro and Sarasola 2015, 2023).

Data Collection. We studied Chimango Caracaras during two breeding seasons, from October through January (austral spring and summer) of 2016 and 2017. We located chimango nests during incubation, and we estimated hatching date by monitoring nests every 3 d (Sutherland 2006). Monitoring ceased when nestlings fledged from the nest.

We performed focal observations at all nests using a spotting scope (20–60 3), for 4–6 continuous hours during each observation period, at a distance of 40–50 m from each nest. Observations were performed by four different observers who were previously trained in recognition of the different parental care behaviors as well as in identification of male and female chimangos. During observation periods we recorded parental care behaviors at the nest, including incubation, brooding/shading, and food provisioning (Gaibani and Csermely 2007). To ensure a balanced distribution of field observations for different times of the day, we established three 5-hr time blocks: morning (0600–1059 H), midday (1100–1559 H), and afternoon (1600–2100 H) (Xirouchakkis and Mylonas 2007). After each observation period, we waited until the adult left the nest to check nest status (i.e., number of eggs, number and age of nestlings) with a mirror pole to minimize disturbance to the breeding attempt. We used a photographic guide developed from observations made at nests with known hatching dates to visually estimate nestling age (J. H. Sarasola unpubl. data). We determined that a nest was successful if at least one nestling achieved 80% of mean age at first flight (Steenhof and Newton 2007), which is 30 d post-hatching for chimangos (Solaro and Sarasola 2023). Likewise, we defined productivity as the number of young that achieved that same age, 30 d post-hatching.

To understand division of labor between sexes, we calculated the percentage of time devoted to incubation by each parent as the time spent in incubation divided by the amount of time each parent was actually at the nest. Similarly, during the nestling period, we measured the percentage of time spent brooding/shading the nestling(s) by each parent, again taking into account the time each adult was at the nest. We calculated food delivery rates by dividing the number of food deliveries to the nest made by each parent by the total number of hours that the nest was observed. All time measurements were recorded using a stopwatch, to the nearest second.

Statistical Analyses. To examine the influence of several variables on the different parental care behaviors at nests, we used the following approach: for incubation, we modeled the percentage of time spent in incubation as a function of parental sex (male, female), time of day (morning, midday, afternoon), and clutch size, and the interactions of parental sex with time of day. For the nestling period, we modeled the percentage of time spent brooding/shading as a function of parental sex, time of day, brood size, and nestling age, and the interactions of parental sex with time of day. Lastly, we modeled food delivery rate as a function of parental sex, time of day, brood size, and nestling age and the interaction of parental sex with time of day. When modeling food delivery rate, a quadratic term was included in addition to the linear term to test for a higher feeding rate at intermediate ages before the known pre-fledging period of weight reduction (Holthuijzen 1990, Galmes et al. 2018). Some nests were observed more than once in each year, but because we never observed the same nest during both the incubation and the nestling periods in the same year, and because most parents could not be identified from one year to another, we included nest identity and year (2016 or 2017), each as a random effect, in all models.

The percentage of time each adult spent in incubation and brooding/shading were modeled as response (dependent) variables with a beta distribution and link function logit. Food delivery rate was modeled as the response (dependent) variable with a Poisson distribution (checking for overdispersion in the model) and log link function. We performed generalized linear mixed models (GLMMs) using the package glmmTMB (Douma and Weedon 2019) for the models with incubation and brooding/shading, and the package lme4 (Bates et al. 2015) for the models with food delivery rate.

We also wished to determine influence of care by both parents on nest success and productivity. Because we never observed the same nest during both the incubation and the nestling periods in the same year, we only modeled these parameters using behaviors performed during the nestling period. We combined the percentage of time spent brooding/shading for males and females (total brooding time) and the number of food deliveries by both parents per hour of observation (total food delivery rate). We modeled nest success (binomial distribution, link function = logit) and productivity (Poisson, link function = log) using multivariate GLMMs with lme4 (Bates et al. 2015). In all models, we added the estimated hatching date as a numeric variable (days from the first recorded hatching date of the colony of the season) to account for possible negative effects of breeding late in the nesting season for chimangos (Solaro and Sarasola 2023).

In all cases, we used automated model selection with the MuMIn package (Barton 2009), and models were compared based on Akaike's information criterion adjusted for small sample size (AIC_c, Burnham and Anderson 2004). If candidate models had DAIC_c ≤ 2, they were considered to be equally plausible given the data. All statistical procedures were carried out using R statistical software (R Core Team 2021). Results are presented as mean ± SE.

RESULTS

We conducted observations at a total of 70 Chimango Caracara nests during the two breeding seasons (30 in 2016, 40 in 2017), for a total observation time of 315 hr (  Supplemental Material Table S1 (JRR-23-16 Supplemental Material final.pdf)). Reproductive parameters were similar between the two years; nest success of the studied chimango population for both years combined was 57.1%, and 74.3% of all hatchlings reached the age when we assumed successful fledging (hatchling alive at 30 d post-hatching = fledgling success; Table 1). The first recorded hatching date of the colony was 7 November in 2016 and 11 November in 2017.

Table 1.

Reproductive parameters for Chimango Caracara nests observed during the breeding season in 2016 and 2017. Successful nests are those in which at least one young reached the age of 30 d post hatching. Fledgling success = percentage of hatchlings that reached that same age, the age at which we defined productivity, assuming those young actually fledged. Data are presented either as total number, or as mean ± SE, and percentages are indicated as %.

Division of Parental Roles. The best model that explained variation in the percentage of time spent incubating included parental sex and time of day (  Table S2 (JRR-23-16 Supplemental Material final.pdf)). Females spent a greater percentage of time (59.0 ± 6.1%) incubating the eggs than males (41.0 ± 6.1%; Table 2). For both sexes combined, the percentage of time spent in incubation was higher during morning and midday than in the afternoon (Table 2).

Table 2.

Percentage of time spent in parental care behaviors by adult Chimango Caracaras, according to time of the day (morning: 0600–1059 H; midday: 1100–1559 H; afternoon: 1600–2100 H) and sex ($ = female; # = male; pooled = both sexes). Values are given as mean ± SE; n represents the number of nests observed during the specified time of day. All percentages are calculated based on the total time that either adult chimango was actually present at the nest. “Pooled” refers to percentages that were calculated based on the total time the nest was observed.

The percentage of time spent brooding/shading nestlings was best explained by parental sex, time of the day, and age of the nestlings (Table 3,   S3 (JRR-23-16 Supplemental Material final.pdf)). Females spent a greater percentage of time brooding/shading nestlings (58.4 ± 8.6%) than males (41.6 ± 8.6%; Table 2). For both sexes combined, the percentage of time devoted to brooding/shading was higher during morning and midday than during the afternoon (Table 2) and decreased with increasing age of the offspring (Table 3).

Table 3.

Coefficient estimates and standard errors for each parameter from the top models explaining parental care behaviors of Chimango Caracara (percentage of time in incubation, percentage of time spent brooding/shading, and food delivery rate), as a function of the different covariates described at each stage, at nests in a suburban residential area in La Pampa Province, Argentina (n = 30 nests in 2016, 40 nests in 2017). Dash indicates that the covariate did not appear in the best model. NA indicates that the covariate was not included a priori in the model (i.e., during incubation, nestlings are not present and thus brood size and nestling age cannot be included). TOD indicates time of the day.

The best model to explain the variation in food delivery rates included the time of day, nestling age and the quadratic term of nestling age (Table 3,   S4 (JRR-23-16 Supplemental Material final.pdf)) but did not include sex, indicating that food delivery rates did not differ between males and females. For both sexes combined, food delivery rates were higher in the afternoon than in the morning and midday (Table 2). Also, the food delivery rate for both sexes combined (quadratic relationship) was lower during the early days of the nestling period, reached a peak during the middle of the nestling period, and declined thereafter (Fig. 1).

Figure 1.

Food delivery rates for male and female Chimango Caracaras as a function of nestling age, at a breeding colony in a suburban area of central Argentina. Food delivery rates were calculated at 37 nest attempts observed during the combined breeding seasons of 2016 and 2017. The gray line corresponds to the predictions from the quadratic model, and the gray area corresponds to the 95% confidence interval. The red line represents a simulation of the quadratic relationship between the response variable (number of prey deliveries per hour) and the predictor variable (age of the nestlings).

Effect of Parental Care Activities on Reproductive Parameters. The total percentage of time spent brooding/shading by both parents combined at nests observed throughout the nestling period had no apparent influence on nest success or productivity (  Table S5, S6 (JRR-23-16 Supplemental Material final.pdf)). However, both nest success (estimate: 1.75 ± 0.63) and productivity (estimate: 0.35 ± 0.12) were higher at nests where both parents delivered food at a higher rate.

Hatching date and year were not important variables in any of the final models for any analyses (  Table S5, S6 (JRR-23-16 Supplemental Material final.pdf)).

DISCUSSION

Ours is the first study of parental care behaviors in the Chimango Caracara. At the nests we observed, parental care efforts were independent of clutch or brood size, but both parents adjusted their behaviors to meet the age-specific needs of nestlings (Ricklefs 1968, Galmes et al. 2018). During daylight hours when they were actually at the nest, females allocated a greater percentage of time to incubation and to brooding/shading than males, similar to many other raptors, including avian scavengers (Newton 1979, Keeley and Bechard 2017). Food provisioning rates were similar for females and males, which is in line with other scavenging raptors that show little sexual size dimorphism (Rollack et al. 2013).

Time spent brooding/shading by the parents decreased with nestling age, as predicted, similar to other avian scavengers (Margalida and Bertran 2000). When nestlings are newly hatched, the presence of adults at the nest is important to protect the young from predation, one of the main causes of offspring mortality in raptors (Newton 1998). As nestlings grow, their size may make them too large for certain predators, reducing the nestlings' need for parental protection. Similarly, during the first weeks after hatching, when nestlings cannot thermoregulate, regular protection from extreme temperatures by the adults is essential to their survival (Beecham and Kochert 1975, Visser 1998, Durant 2002).

Food provisioning rates were similar for both sexes, as has been shown for other scavenging raptors that show little sexual size dimorphism (Brunton 1988, Margalida and Bertran 2000, Rollack et al. 2013). Parental food delivery rates showed an overall quadratic relationship with nestling age, in line with other avian species (Ricklefs 1968, Holthuijzen 1990, Galmes et al. 2018). Food delivery rates increased with the nestling age during the first days post-hatching, likely due to higher energy demands of the nestlings during the early days of growth (Ricklefs 1968, Xirouchakkis and Mylonas 2007). However, after the central days of the nestling period, food delivery rates declined. The most important energy requirements of nestlings are a sum of maintenance (proportional to the age of the nestling) and growth rate (which decreases with the age of nestlings; Ricklefs 1968). Because maintenance is more costly when the nestling is more developed and maximum growth rates occur during the first days post-hatching, energetic requirements of nestlings will be higher during the central days of the nestling period (Ricklefs 1968); thus, parents adjust food delivery rates to meet those needs. Increasing energetic requirements of nestlings, together with decreasing needs for parental defense and brooding, may cause females initially focused on incubation and shading to devote more time to securing food, resulting in food delivery rates similar to those of males (Collopy 1984, Margalida and Bertran 2000). Finally, at our study nests, food delivery rate had a positive influence on nest success and productivity even after controlling for the possible effect of hatching date (Solaro and Sarasola 2023).

Both male and female chimangos devoted higher percentages of time spent at the nest to incubation and brooding during morning and midday and exhibited higher food provisioning rates during the afternoon. Birds increase the amount of time they spend at the nest when environmental temperatures fall because lowering egg temperatures for a prolonged period could reduce reproductive success (Clark and Wilson 1981, Webb 1987, Williams 1993). Chimango nestlings hatch during summer, when maximum temperatures (often >35°C) are reached between 1600–1900 H, while early morning temperatures can fall to 12°C (Cabrera 1976). At our study nests, adult chimangos spent more time attending eggs and nestlings during the cooler part of the day likely to ensure optimized egg and nestling temperatures. Finally, food was delivered primarily during the afternoon. Along with scavenging, chimangos often feed on insects, which show increased activity during the afternoon and before sunset (Joern et al. 1986).

Although we provide new information about parental care in the Chimango Caracara, much of the life history of this common species remains unknown. We encourage further research to address knowledge gaps, particularly to evaluate reproductive success across larger regions of the species distribution. Improving our understanding of all aspects of the chimango's breeding biology across its broad geographic range may have benefits when addressing species-related conservation issues (Buechley and Şekercioğlu 2016, Peisley et al. 2017).

SUPPLEMENTAL MATERIAL (available online).   Table S1 (JRR-23-16 Supplemental Material final.pdf): Number of hours Chimango Caracara nests were observed during the breeding season in 2016 and 2017, by reproductive period (incubation and nestling) and by time of the day: morning (0600–1059 H), midday (1100–1459 H), and afternoon (1500–2100 H).   Table S2 (JRR-23-16 Supplemental Material final.pdf): Model selection results of GLMM explaining the percent of time adult Chimango Caracaras (Milvago chimango) spent incubating at nests in a suburban residential area in La Pampa Province, Argentina (n = 30 nests in 2016, 40 nests in 2017).   Table S3 (JRR-23-16 Supplemental Material final.pdf): Model selection results of GLMM explaining the percent of time adult Chimango Caracaras (Milvago chimango) spent brooding/shading nestlings at nests in a suburban residential area in La Pampa Province, Argentina (n = 30 nests in 2016, 40 nests in 2017).   Table S4 (JRR-23-16 Supplemental Material final.pdf): Model selection results of GLMM explaining food delivery rates by adult Chimango Caracaras (Milvago chimango) at nests in a suburban residential area in La Pampa Province, Argentina (n = 30 nests in 2016, 40 nests in 2017).   Table S5 (JRR-23-16 Supplemental Material final.pdf): Model selection results of GLMM explaining nest success at Chimango Caracara (Milvago chimango) nests in a suburban residential area in La Pampa Province, Argentina. Analysis used nests observed only during the nestling period.   Table S6 (JRR-23-16 Supplemental Material final.pdf). Model selection results of GLMM explaining nest productivity at Chimango Caracara (Milvago chimango) nests in a suburban residential area in La Pampa Province, Argentina. Analysis used nests observed only during the nestling period.